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Living on the edge van Egmond, E.M.

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Download date: 05. Oct. 2021 LIVING ON THE EDGE LIVING ON THE EDGE INVITATION Resource availability and macroinvertebrate community dynamics To attend the public defence of my in relation to sand nourishment PhD thesis entitled: LIVING ON THE EDGE

Resource availability Emily van Egmond and macroinvertebrate community dynamics in relation to sand nourishment

By Emily van Egmond

Thursday 13th of December 2018 at 11.45 hours

In the Aula of the Vrije Universiteit Amsterdam You are kidnly invited to join the reception following the defence.

Emily van Egmond [email protected]

Emily van Egmond Paranymphs

Milou Huizinga Björn van Loon [email protected]

Living on the edge: Resource availability and macroinvertebrate community dynamics in relation to sand nourishment

Emily van Egmond

VRIJE UNIVERSITEIT

Living on the edge: Resource availability and macroinvertebrate community dynamics in relation to sand nourishment

ACADEMISCH PROEFSCHRIFT

ter verkrijging van de graad Doctor aan de Vrije Universiteit Amsterdam, op gezag van de rector magnificus prof.dr. V. Subramaniam,

in het openbaar te verdedigen ten overstaan van de promotiecommissie van de Faculteit der Bètawetenschappen op donderdag 13 december 2018 om 11.45 uur in de aula van de universiteit,

De Boelelaan 1105

Emily van Egmond Living on the edge: Resource availability and macroinvertebrate community dynamics in relation to sand nourishment PhD thesis, 2018

Department of Ecological Science, Vrije Universiteit Amsterdam, the Netherlands ISBN: 978-94-6332-422-9 door This research was funded by grant 12689 from the Technology Foundation STW within the Emely Marie van Egmond NatureCoast program (P11-24). geboren te Amsterdam This thesis was printed by GVO drukkers & vormgevers, Ede.

VRIJE UNIVERSITEIT

Living on the edge: Resource availability and macroinvertebrate community dynamics in relation to sand nourishment

ACADEMISCH PROEFSCHRIFT

ter verkrijging van de graad Doctor aan de Vrije Universiteit Amsterdam, op gezag van de rector magnificus prof.dr. V. Subramaniam,

in het openbaar te verdedigen ten overstaan van de promotiecommissie van de Faculteit der Bètawetenschappen op donderdag 13 december 2018 om 11.45 uur in de aula van de universiteit,

De Boelelaan 1105

Emily van Egmond Living on the edge: Resource availability and macroinvertebrate community dynamics in relation to sand nourishment PhD thesis, 2018

promotor: prof.dr. M.A.P.A. Aerts copromotoren: prof.dr. P.M. van Bodegom prof.dr. M.P. Berg

To Maja

promotor: prof.dr. M.A.P.A. Aerts copromotoren: prof.dr. P.M. van Bodegom prof.dr. M.P. Berg

To Maja

Contents

Chapter 1 General introduction 9

Chapter 2 A mega-nourishment creates novel habitat for intertidal 31 macroinvertebrates by enhancing habitat relief of the sandy beach

Chapter 3 Non-additive effects of consumption in an intertidal 57 macroinvertebrate community are independent of food availability but driven by complementarity effects

Chapter 4 Strong seasonal and macroinvertebrate community 77 effects on nutrient mineralisation in wrack on sandy beaches

Chapter 5 Growth of pioneer beach plants is strongly driven by buried 99 macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Chapter 6 General discussion 135

References 153

Summary 173

Samenvatting 179

Acknowledgements 185

About the author 189

Publications 193

Contents

Chapter 1 General introduction 9

Chapter 2 A mega-nourishment creates novel habitat for intertidal 31 macroinvertebrates by enhancing habitat relief of the sandy beach

Chapter 3 Non-additive effects of consumption in an intertidal 57 macroinvertebrate community are independent of food availability but driven by complementarity effects

Chapter 4 Strong seasonal and macroinvertebrate community 77 effects on nutrient mineralisation in wrack on sandy beaches

Chapter 5 Growth of pioneer beach plants is strongly driven by buried 99 macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Chapter 6 General discussion 135

References 153

Summary 173

Samenvatting 179

Acknowledgements 185

About the author 189

Publications 193

Chapter 1

General introduction

Chapter 1

General introduction

10 Chapter 1

Sandy beaches are among the most prevalent coastal ecosystems in the world and are 1.1 The sandy beach ecosystem on the interface between sea and land estimated to cover up to 70% of the ice-free coasts (McLachlan and Brown 2006). They 1.1.1 Physical environment of sandy beaches harbour unique ecological communities with many species only found on sandy beaches and provide a wide variety of ecosystem functions, including nutrient cycling (McLachlan and In its essence, sandy beaches are enormous aggregations of sand particles on the interface Brown 2006). Due to the very dynamic character of sandy beaches, the in situ primary between sea and land. These ecosystems are highly dynamic, as sandy beaches are subject to production is low and resource availability in the form of phytoplankton (intertidal zone) and the interaction between wind, waves and tides that continuously change the abiotic wrack (supratidal zone) is spatially and temporally highly heterogeneous (Colombini and environment and beach profile (McLachlan and Brown 2006). The perpetual movement of Chelazzi 2003, Liebowitz et al. 2016). The sandy beach food web heavily depends on this input sand particles and water across the beach results in a range of beach types (Short and Wright of marine exogeneous organic matter (Polis et al. 1997, Liebowitz et al. 2016). In particular, 1983, Wright and Short 1984). This distinction among beach types can be made based on their the macroinvertebrate community of the intertidal and supratidal zone together form the link morphodynamical features: reflective beaches are narrow and steep with waves braking between marine primary production and higher trophic levels, connecting the marine and directly on the beach, while dissipative beaches are wide and flat with waves being broken by terrestrial food webs (Speybroeck et al. 2008a). It remains unclear, however, how resource an extensive surf zone before reaching the beach. Moreover, fine sand and a large tidal range availability influences species interactions and community assembly of the macroinvertebrate are found on dissipative beaches as opposed to reflective beaches with coarse sand and a community on sandy beaches, and how this influences ecosystem functioning. small tidal range. Intermediate beaches are found between these two extremes (Short and Wright 1983, Short 1996). A beach can furthermore be categorised based on the degree of While of critical importance, on a global scale, sandy beach ecosystems are subject to coastal wave exposure, being either exposed, where the beach is subject to a high wave energy squeeze: beaches are trapped between the rising sea level and an increase in storm events regime, sheltered, where the beach is more protected and subject to a low wave energy due to climate change on the sea side, and static anthropogenic structures on the land side regime (such as in a lagoon), or in between (McLachlan and Brown 2006). (Schlacher et al. 2007). The coastal zone, sandy beaches included, is densely populated by humans (Small and Nicholls 2003) and coastal populations are only expected to further Perpendicular to the coast, the sandy beach is generally divided into two main zones divided increase (Neumann et al. 2015). This combination of factors causes severe erosion of the by the water line as a dynamic border: the intertidal and the supratidal zone (McLachlan and sandy beach, threatening the human population and livelihood as the sea advances inland and Jaramillo 1995, Dugan et al. 2013; see Figure 1.1). The intertidal zone is defined as the zone leaving only a narrow strip for ecological communities to reside. Sand nourishment has been between the mean high water line at spring tide (MHWS) and the mean low water line at applied to mitigate the effects of beach erosion, but recently a mega-nourishment has been spring tide (MLWS). Twice a day, this part of the beach is submerged by the sea under proposed as a more ecologically and sustainable alternative (Stive et al. 2013). A mega- influence of the lunar tidal cycle, moving the water line up and down along the beach. The nourishment is created by placing a very large volume of sand in a concentrated location along water column overlaying the intertidal zone during high tide is also termed the surf zone the coast, which is intended to gradually nourish up-stream beaches over a long period of (Morgan et al. 2018). Intertidal systems therefore alternate between being either dry or moist, time. This lowers the number of pulse disturbances to the sandy beach ecosystem compared or fully saturated by sea water (McArdle and McLachlan 1991). The supratidal zone of the to regular sand nourishment practices. After application of a mega-nourishment, ecological sandy beach is defined as the part of the beach above MHWS up to the dune foot where communities have to re-assemble, but community assembly may be directly or indirectly primary and secondary dunes begin to emerge. In contrast to the intertidal zone, this zone is influenced by the characteristics of the mega-nourishment. The effect of a mega-nourishment not submerged by the sea during the tidal cycle and the sand remains dry, except for heavy on the macroinvertebrate community and how this compares to regular sand nourishment storms creating high waves passing the MHWS and occasional precipitation. Thus, the abiotic thus remains unknown. environment, including water, salinity and oxygen content, differs notably between these two beach zones. The intertidal zone borders the subtidal zone (below MLWS) which is Below, I will first explain the physical characteristics of the beach and its effect on resource permanently submerged by the sea (Figure 1.1). availability, followed by a description of the sandy beach food web and its components. I will give a definition of the macroinvertebrate community and indicate the main drivers of 1.1.2 Effect of the physical environment on resource availability community assembly in general and of the macroinvertebrate community on the sandy beach Sandy beaches provide a unique coastal interface between sea and land linking marine and in particular, with a focus on resource competition. I will explain how sand nourishment has terrestrial ecosystems (Polis et al. 1997, Liebowitz et al. 2016). The ecosystem boundaries of been applied and what the ecological impacts have been thus far, followed by a description sandy beaches are continually crossed by (in)organic matter, nutrients and, where biologically of a mega-nourishment and its expected effects on the macroinvertebrate community. Finally, possible, organisms (Barrett et al. 2005, Heck et al. 2008). Sandy beaches are considered to the aims, research questions and outline of this thesis are given. be primarily recipient ecosystems, because they receive large amounts of exogenous organic matter that has been produced by primary and secondary producers in the sea (Liebowitz et al. 2016). Marine exogenous organic matter mainly enters the sandy beach ecosystem in the

General introduction 11

12 Chapter 1 form of organic matter particles and plankton in intertidal waters or beach-cast sea weed and Also, the location of wrack on the beach, i.e. the distance to mean sea level, is strongly sea grass, collectively termed wrack (Colombini and Chelazzi 2003). Due to the dynamic determined by tidal amplitudes which change monthly to annually (e.g. Plag and Tsimplis character of sandy beaches, the input of marine exogenous organic matter and thus resource 1999). Fresh wrack is primarily present in younger drift lines around the high water line (Orr availability to the sandy beach ecosystem is spatially and temporally highly heterogeneous. et al. 2005). If fresh wrack is not resuspended into the sea, wrack may either remain in its current location or be transported further up-shore by wind until the material is buried in the Within the surf zone, a diverse mixture of dissolved and particulate organic matter, sand, caught by other structures (e.g. plants) or has reached a wind-dead location (Hammann phytoplankton and zooplankton is present. Once these organic matter particles and plankton and Zimmer 2014). This older wrack is thus generally present in drift lines higher up the beach have entered the surf zone, their distribution is strongly driven by hydrodynamic processes and closer to the dune foot than young drift lines consisting of fresh wrack. Old wrack is no which are related to the coastal morphology of a certain beach (Shanks et al. 2017, Morgan et longer directly influenced by sea water and decomposes through a variety of abiotic and biotic al. 2018). For example, the abundance of phytoplankton in the surf zone is dependent on processes, further changing the nutritional quality of the wrack (Colombini and Chelazzi 2003). along-shore variation in hydrodynamics, with a higher abundance in dissipative than in Abiotic processes that work on deposited wrack include drying by the sun, erosion of organic reflective surf zones (Shanks et al. 2017). The same pattern has been observed for zooplankton material by wind and coverage by a layer of sand, while biotic processes include the (Morgan et al. 2018). Phytoplankton community composition may also be affected by decomposition of wrack by microbes and detritivores (Colombini and Chelazzi 2003). hydrodynamic processes. Only a small number of species are adapted to the high wave energy conditions at certain beaches and considered as surf diatoms (e.g. Thalassiosira sp. Cleve), 1.1.3 Sandy beach food web while other phytoplankton species mainly occur outside the surf zone (Odebrecht et al. 2014). Although sandy beaches may appear void of life upon first glance, sandy beaches harbour Offshore phytoplankton is transported by waves and currents to the surf zone where it is an unique ecological communities consisting of many species that are not found in any other important component of phytoplankton communities, as surf diatom taxa may only compose ecosystem. On sandy beaches, three food webs that have traditionally been considered to 1% of the phytoplankton community (Morgan et al. 2018). Unlike phytoplankton show little connectivity, can be distinguished: 1) the interstitial food web in intertidal sands communities, zooplankton community composition may be further determined by the (benthic microalgae, bacteria, protozoa and meiofauna (including mites and spring tails)), 2) interaction between hydrodynamic processes and the ability of most zooplankton to actively the microbial food web in the surf zone (phytoplankton, zooplankton, bacteria and protozoa) move in the water column (Morgan et al. 2018). and 3) the macroscopic food web (including macrofauna, fish and birds) (McLachlan and Wrack supply on sandy beaches depends on the availability, transport and deposition of wrack Brown 2006). The macroscopic food web, however, has more recently been linked to the (Liebowitz et al. 2016). Sea weeds and sea grasses are primary producers that grow attached microbial food web via the consumption of phytoplankton by macrofauna and to the to a substratum, but become detached as a result of severe hydrodynamic conditions, such as interstitial food web via the shared consumption of benthic microalgae by meio- and storm events (Suursaar et al. 2014). Detachment may be influenced by both abiotic factors, macrofauna (Lercari et al. 2010, Bergamino et al. 2011, Maria et al. 2011, Bergamino et al. including substratum type and near-bed current velocity, and biotic factors, including strength 2013). In this thesis, the focus is on the macroscopic food web while including phytoplankton of attachment and senescence (Liebowitz et al. 2016). The transportation and deposition of and benthic microalgae, and is here referred to as the sandy beach food web. wrack subsequently depends on a complex interplay between factors such as wind, waves and The sandy beach food web spans across the intertidal and supratidal zones and is connected currents in the surf zone, wrack traits related to buoyancy capacity, size and life form, and to the subtidal zone and dune foot (Speybroeck et al. 2008a). The spatially separate intertidal beach morpho-dynamic type (Orr et al. 2005, Liebowitz et al. 2016). Combined, these factors and supratidal food webs are connected at the higher trophic level by predators that consume influence the amount, composition, location and nutritional quality of wrack present on a from the lower trophic level in both beach zones, intertwining these food chains to create the beach. As such, wrack input is highly variable. For example, wrack input ranged between 0.2 sandy beach food web (Figure 1.1). Dissolved nutrients in the sea water and sunlight drive the and 43.1 kg m-1 y-1 on Spanish beaches (measured as the wrack cover within a 1 m wide strip production of phytoplankton, benthic microalgae, sea weed and sea grass, the so-called green of beach along a transect running from the dune foot to the lowest swash level, adapted from web. In the intertidal zone, the benthic microalgae attached to sand grains and phytoplankton Barreiro et al. 2011), but ranged between 1000 and 2000 kg m-1 y-1 on Californian beaches in the water column are consumed by grazers. In the supratidal zone, detached sea weed and (Polis et al. 1997). sea grass cast upon the beach serve as a food source for bacteria and detritivores, the so- Several semi-continuous bands of wrack are usually formed parallel to the coast line. On a called brown web. Different primary predators in the intertidal and supratidal zone feed on tide-dominated beach, multiple drift lines are formed as the water slowly recedes from spring these lower trophic levels and are in turn consumed by secondary predators. Together with to neap tide, allowing patches of wrack to deposit on the beach at different tidal heights solar energy, nutrients that become available at different trophic levels through decay of (Hammann and Zimmer 2014). In contrast, tide-independent beaches mainly accumulate organic matter in the supratidal zone may finally flow to terrestrial plants. Below I will expand wrack just above the high water line and wrack may be redistributed by extreme high sea on the food web components of the sandy beach. water levels or high wind speeds to form multiple drift lines (Hammann and Zimmer 2014).

General introduction 13 form of organic matter particles and plankton in intertidal waters or beach-cast sea weed and Also, the location of wrack on the beach, i.e. the distance to mean sea level, is strongly sea grass, collectively termed wrack (Colombini and Chelazzi 2003). Due to the dynamic determined by tidal amplitudes which change monthly to annually (e.g. Plag and Tsimplis character of sandy beaches, the input of marine exogenous organic matter and thus resource 1999). Fresh wrack is primarily present in younger drift lines around the high water line (Orr availability to the sandy beach ecosystem is spatially and temporally highly heterogeneous. et al. 2005). If fresh wrack is not resuspended into the sea, wrack may either remain in its current location or be transported further up-shore by wind until the material is buried in the Within the surf zone, a diverse mixture of dissolved and particulate organic matter, sand, caught by other structures (e.g. plants) or has reached a wind-dead location (Hammann phytoplankton and zooplankton is present. Once these organic matter particles and plankton and Zimmer 2014). This older wrack is thus generally present in drift lines higher up the beach have entered the surf zone, their distribution is strongly driven by hydrodynamic processes and closer to the dune foot than young drift lines consisting of fresh wrack. Old wrack is no which are related to the coastal morphology of a certain beach (Shanks et al. 2017, Morgan et longer directly influenced by sea water and decomposes through a variety of abiotic and biotic al. 2018). For example, the abundance of phytoplankton in the surf zone is dependent on processes, further changing the nutritional quality of the wrack (Colombini and Chelazzi 2003). along-shore variation in hydrodynamics, with a higher abundance in dissipative than in Abiotic processes that work on deposited wrack include drying by the sun, erosion of organic reflective surf zones (Shanks et al. 2017). The same pattern has been observed for zooplankton material by wind and coverage by a layer of sand, while biotic processes include the (Morgan et al. 2018). Phytoplankton community composition may also be affected by decomposition of wrack by microbes and detritivores (Colombini and Chelazzi 2003). hydrodynamic processes. Only a small number of species are adapted to the high wave energy conditions at certain beaches and considered as surf diatoms (e.g. Thalassiosira sp. Cleve), 1.1.3 Sandy beach food web while other phytoplankton species mainly occur outside the surf zone (Odebrecht et al. 2014). Although sandy beaches may appear void of life upon first glance, sandy beaches harbour Offshore phytoplankton is transported by waves and currents to the surf zone where it is an unique ecological communities consisting of many species that are not found in any other important component of phytoplankton communities, as surf diatom taxa may only compose ecosystem. On sandy beaches, three food webs that have traditionally been considered to 1% of the phytoplankton community (Morgan et al. 2018). Unlike phytoplankton show little connectivity, can be distinguished: 1) the interstitial food web in intertidal sands communities, zooplankton community composition may be further determined by the (benthic microalgae, bacteria, protozoa and meiofauna (including mites and spring tails)), 2) interaction between hydrodynamic processes and the ability of most zooplankton to actively the microbial food web in the surf zone (phytoplankton, zooplankton, bacteria and protozoa) move in the water column (Morgan et al. 2018). and 3) the macroscopic food web (including macrofauna, fish and birds) (McLachlan and Wrack supply on sandy beaches depends on the availability, transport and deposition of wrack Brown 2006). The macroscopic food web, however, has more recently been linked to the (Liebowitz et al. 2016). Sea weeds and sea grasses are primary producers that grow attached microbial food web via the consumption of phytoplankton by macrofauna and to the to a substratum, but become detached as a result of severe hydrodynamic conditions, such as interstitial food web via the shared consumption of benthic microalgae by meio- and storm events (Suursaar et al. 2014). Detachment may be influenced by both abiotic factors, macrofauna (Lercari et al. 2010, Bergamino et al. 2011, Maria et al. 2011, Bergamino et al. including substratum type and near-bed current velocity, and biotic factors, including strength 2013). In this thesis, the focus is on the macroscopic food web while including phytoplankton of attachment and senescence (Liebowitz et al. 2016). The transportation and deposition of and benthic microalgae, and is here referred to as the sandy beach food web. wrack subsequently depends on a complex interplay between factors such as wind, waves and The sandy beach food web spans across the intertidal and supratidal zones and is connected currents in the surf zone, wrack traits related to buoyancy capacity, size and life form, and to the subtidal zone and dune foot (Speybroeck et al. 2008a). The spatially separate intertidal beach morpho-dynamic type (Orr et al. 2005, Liebowitz et al. 2016). Combined, these factors and supratidal food webs are connected at the higher trophic level by predators that consume influence the amount, composition, location and nutritional quality of wrack present on a from the lower trophic level in both beach zones, intertwining these food chains to create the beach. As such, wrack input is highly variable. For example, wrack input ranged between 0.2 sandy beach food web (Figure 1.1). Dissolved nutrients in the sea water and sunlight drive the and 43.1 kg m-1 y-1 on Spanish beaches (measured as the wrack cover within a 1 m wide strip production of phytoplankton, benthic microalgae, sea weed and sea grass, the so-called green of beach along a transect running from the dune foot to the lowest swash level, adapted from web. In the intertidal zone, the benthic microalgae attached to sand grains and phytoplankton Barreiro et al. 2011), but ranged between 1000 and 2000 kg m-1 y-1 on Californian beaches in the water column are consumed by grazers. In the supratidal zone, detached sea weed and (Polis et al. 1997). sea grass cast upon the beach serve as a food source for bacteria and detritivores, the so- Several semi-continuous bands of wrack are usually formed parallel to the coast line. On a called brown web. Different primary predators in the intertidal and supratidal zone feed on tide-dominated beach, multiple drift lines are formed as the water slowly recedes from spring these lower trophic levels and are in turn consumed by secondary predators. Together with to neap tide, allowing patches of wrack to deposit on the beach at different tidal heights solar energy, nutrients that become available at different trophic levels through decay of (Hammann and Zimmer 2014). In contrast, tide-independent beaches mainly accumulate organic matter in the supratidal zone may finally flow to terrestrial plants. Below I will expand wrack just above the high water line and wrack may be redistributed by extreme high sea on the food web components of the sandy beach. water levels or high wind speeds to form multiple drift lines (Hammann and Zimmer 2014).

14 Chapter 1

1.1.3.1 Primary producers 1.1.3.2 Consumers The in situ primary production of sandy beaches is low due to the intense and continuous Consumers of the intertidal zone are dominated by deposit- and filter-feeders (grazers) and reworking of sandy sediments, providing an unstable environment for primary producer depend on particulate organic matter, phytoplankton and benthic microalgae as food sources establishment (McLachlan and Brown 2006). In the intertidal zone, benthic microalgae grow (McLachlan and Brown 2006; see Figure 1.2). Taxonomic groups mainly include polychaete attached to sand grains and communities are dominated by diatoms (Speybroeck et al. 2008a). worms and crustaceans (McLachlan and Jaramillo 1995, Degraer et al. 2003). Foraging occurs Benthic microalgae can be an important food source for deposit-feeders or, if resuspended in during high tide, when the water column containing food particles overlays the intertidal zone. the water column, for filter-feeders (Miller et al. 1996). In temperate beaches, vascular plants For example, the polychaete worm Scolelepis squamata Müller remains in its burrow during are only present in the supratidal zone, where the drift line forms the lower boundary for plant high tide but protrudes its palps from the burrows opening and moves its palps to collect any settlement (Speybroeck et al. 2008a). Most plants are annuals and adapted to a dynamic organic particles floating in the water or deposited on the sediment surface (Dauer 1983). The environment, with Cakile maritima Scop. and Honckenya peploides (L.) Ehrh. as examples of amphipod Bathyporeia pilosa Lindström, on the other hand, feeds by scraping the organic common species on sandy beaches, growing in the neighbourhood of old wrack (Davy et al. material from sand grains using its mouth parts (Nicolaisen and Kanneworff 1969). Consumers 2006, Speybroeck et al. 2008a). Nutrient supply for these plants originates from of the supratidal zone are dominated by detritivores and depend on wrack and other drift line decomposition of organic matter from the supratidal zone, primarily wrack (Williams and components, such as faeces and carrion (Colombini and Chelazzi 2003). In addition, it is Feagin 2010, Del Vecchio et al. 2013). suggested that some detritivores not (only) feed on wrack itself but on the wrack-associated biofilm (Porri et al. 2011). Taxonomic groups mainly include amphipods and insects of the orders Coleoptera and Diptera (Olabarria et al. 2007). The amphipod Talitrus saltator Montagu is an abundant species in wrack (Ruiz-Delgado et al. 2016) and is a key consumer on sandy beaches and may consume up to 11% of its dry body weight in wrack per day (Lastra et al. 2008). During the day, the amphipod remains in its burrows but emerges at night to feed on stranded wrack (Fallaci et al. 1999). Another abundant group of wrack consumers are Diptera larvae. After egg hatching, the emerged Diptera larvae bury themselves into the wrack and start feeding immediately, consuming up to 1.8 times their dry weight in wrack per day (Stenton-Dozey and Griffiths 1980). 1.1.3.3 Predators

Both primary and secondary predators occur in the sandy beach food web and predators include polychaete worms, isopods, crabs, shrimp, fish and birds in the intertidal zone (Van Tomme et al. 2014) and insects of the order Coleoptera and birds in the supratidal zone (Speybroeck et al. 2008a). In the intertidal zone, the common isopod Eurydice pulchra Leach predates actively during high tide but remains buried in the sand during low tide (Reid 1988).

Figure 1.1 A schematic representation of the sandy beach food web, spanning across the open sea, the intertidal and supratidal zone. Grey boxes indicate the components of the macroinvertebrate Figure 1.2 An individual of the macroinvertebrate species Scolelepis squamata from the intertidal zone community in both the intertidal and supratidal zone. HWL = high water line at spring tide, LWL = low (left) and Talitrus saltator from the supratidal zone (right). water line at spring tide.

General introduction 15

16 Chapter 1

Eurydice pulchra tries to feed on any animal that it encounters (Holdich 1981), including the surf zone, e.g. stimulating phytoplankton blooms (McLachlan 1980, McLachlan et al. 1981). co-occurring intertidal species Bathyporeia sarsi Watkin, B. pilosa and S. squamata (Van For example, macroinvertebrates (including both macrobenthos and zooplankton (e.g. Tomme et al. 2014). It is a primary predator as it may be consumed by secondary predators. Eurydice longicornis Studer)) were estimated to recycle 2990 g N m-1 y-1 (across the beach from With incoming tide, fish, shrimp and crabs can access the intertidal zone to forage on the the highest drift line to 10 m depth) or 6.0 g N m-2 y-1, producing 23% of N needed by the intertidal macroinvertebrates (Beyst et al. 2001). For example, juvenile flat fish (such as phytoplankton community on an exposed sandy beach in South Africa (adapted from Pleuronectes platessa L. and Scophthalmus maximus L.) and the shrimp Crangon crangon L. Cockcroft and McLachlan 1993). Beach-specific estimates of the contribution of the consumed large and equal amounts of S. squamata and B. pilosa in a feeding experiment (Van macroinvertebrate community on total carbon and nitrogen budgets are, however, Tomme et al. 2014). In the supratidal zone, shorebirds may feed on wrack-associated dependent on many factors, such as local species abundances and the functional diversity of macroinvertebrates using visual and tactile cues. For example, a positive correlation was the macroinvertebrate community, e.g. variation in excretion rates (Villéger et al. 2012). The found between the abundance of two plover species (Pluvialis squatarola L. and Charadrius effect of changes in community composition on nutrient cycling has, however, not been alexandrinus nivosus Cassin) and both wrack mass and macroinvertebrate abundance (Dugan intensively studied. Processing of wrack by the supratidal macroinvertebrate community may et al. 2003). These species are expected to catch prey from the sand and wrack surface, while also lead to a flow of nutrients back to the sea to support marine primary production, as bird species that mainly use tactile cues (such as Calidris alba Pallas) are more efficient at nutrients leach from partly decomposed wrack around the high water line (Colombini and capturing buried macroinvertebrates, also from the intertidal zone (Vanermen et al. 2009, Chelazzi 2003). Alternatively, nutrient hot spots may be created in the supratidal zone, locally Dugan et al. 2003). supporting terrestrial primary (Hemminga and Nieuwenhuize 1990, Del Vecchio et al. 2013) and secondary production (Polis and Hurd 1996, Schlacher et al. 2017). When these nutrients 1.1.4 Key role for the macroinvertebrate community on sandy beaches become available for plant uptake, this may facilitate pioneer beach plant species to establish Within the sandy beach food web, grazers, detritivores and primary predators together form on the sandy beach (Dugan et al. 2011). Finally, this could initiate embryo dune formation as the macroinvertebrate community (see grey boxes in Figure 1.1). Macroinvertebrates are in pioneer plant species colonise the older, comprised of lots of decomposed material, and this thesis defined as all invertebrate animals that are >1 mm as adults, thus being retained higher positioned drift lines (Hemminga and Nieuwenhuize 1990). Total carbon and nitrogen when sieved over a 1-mm sieve. A distinction is made between the macroinvertebrate budgets of the supratidal zone that include wrack and its consumers are lacking from the community of the intertidal and supratidal zone (Mariani et al. 2017), because literature, but supratidal macroinvertebrates are estimated to consume up to 80% (Griffiths macroinvertebrates have specific adaptations to the environmental conditions of the zone and Stenton-Dozey 1981, Griffiths et al. 1983) and even 100% (Lastra et al. 2015) of the organic they inhabit and seldomly move between these zones (Speybroeck et al. 2008a). This is matter input entering the beach. Hence, the supratidal macroinvertebrate community especially true for macroinvertebrates in the intertidal zone, which are bound to a moist potentially plays an important role in recycling nutrients from wrack deposits but needs to be environment and bury into the sand to avoid being swept into the sea or desiccate during low studied further. tide (McLachlan and Brown 2006). In the supratidal zone, many macroinvertebrate species are 2.2 Drivers of macroinvertebrate community assembly on sandy beaches air-breathers (e.g. insects) and may only visit the intertidal zone during low tide to forage. Since macroinvertebrate densities can locally be very high for certain species (e.g. S. Since the macroinvertebrate community is a key component of the sandy beach ecosystem, it squamata), the macroinvertebrate community holds the potential to have a significant effect is crucial to understand what drives the assembly of macroinvertebrate communities on sandy on ecosystem functioning. beaches. As indicated above, after application of a mega-nourishment, the macroinvertebrate community has to re-assemble, but community assembly may be directly or indirectly The focus of this thesis will be on the macroinvertebrate community of the intertidal and influenced by the characteristics of the mega-nourishment. Altered local hydrodynamics supratidal zone, because these two communities form the link between marine primary around a mega-nourishment may for example change macroinvertebrate dispersal patterns production and higher trophic levels, connecting the marine and terrestrial food webs. As and resource availability (by influencing the distribution of phytoplankton, benthic microalgae such, the macroinvertebrate community serves two main ecosystem functions: 1) nutrient and wrack). This in turn may influence species interactions and drive community assembly, cycling and 2) food to support higher trophic levels, while adding to a unique biodiversity resulting in the actual macroinvertebrate community composition present on a sandy beach. exclusively associated with sandy beaches (Schlacher et al. 2007). Both functions are Below, I will first discuss general community assembly theory, followed by the main drivers of supported by the intertidal and the supratidal zone, where the latter has briefly been covered macroinvertebrate community assembly on sandy beaches in particular, with a focus on in section 1.3.3 and the former will be shortly discussed below. resource competition. 1.1.4.1 Macroinvertebrate community effects on nutrient cycling 2.2.1 Assembly theory Nutrient cycling is mainly driven by the activity of intertidal macroinvertebrates who Identifying the processes that drive and control community assembly are crucial to assimilate and mineralise organic particles, resulting in a release of inorganic nutrients to the understand the actual composition of biological communities on sandy beaches. One way to

General introduction 17

18 Chapter 1 approach this is to determine the relative importance of abiotic and biotic drivers of the idea has been postulated as the habitat harshness hypothesis (Defeo et al. 2001). Towards assembly process and if the factors can be captured in ‘rules’ (HilleRisLambers et al. 2012). more dissipative beaches, however, the physical environment becomes more benign and Classical assembly rules are proposed by Diamond (1975) stating that interspecific interactions biological interactions may become more important as a driver of community assembly. (mainly competition) lead to a non-random co-existence of species within a community. This Abundance and species richness increase towards these more dissipative beaches, leading to view was expanded by Keddy (1992), proposing that both the biotic and abiotic environment a greater potential for encounters between individuals and hence biological interactions act like a filter, or set of filters, selecting species based on their traits from the species pool (McLachlan and Brown 2006, Defeo and McLachlan 2011). This is not merely due to the effect (see Figure 1.4, upper part). Through the stochastic processes dispersal and migration, a set of beach width itself, but a wide beach contains more areas that are less severely influenced of species is selected from the regional species pool (dispersal filter). Then, species are filtered by abiotic stress caused by the sea, allowing for more different species to inhabit this beach by local, deterministic processes from the environment (environmental filter) and via (McLachlan and Dorvlo 2007). biological interactions, especially competition (limiting similarity filter). In the end, a Evidence indicating that biological interactions may be more important for intertidal community is assembled of which the composition depends on the influence of each filter community assembly on sandy beaches than previously recognised, is slowly accumulating. present and what these filters comprise of in a specific ecosystem (Márquez and Kolasa 2013, Previous studies have primarily focused on physical control of macroinvertebrate Götzenberger et al. 2011). Contrasting thoughts on assembly rules are given by Hubbell (2001) communities but did not include main drivers such as competition for resources or who proposed the ‘unified neutral theory of biodiversity and biogeography’, which is based investigated the relative effect of the environment and biological interactions on final on the assumption that differences between individuals of the same trophic level are ‘neutral’, community composition (exceptions include Defeo et al. 1997, Dugan et al. 2004, Van Tomme and therefore these differences are irrelevant for their success. It means that all individuals et al. 2012). Studies that included biological interactions were mainly aimed at understanding within a trophic level have the same chances for migration, birth and death. Communities are zonation patterns of co-occurring species, instead of community responses. Ortega-Cisneros then assembled by dispersal limitation, speciation and ecological drift (Rosindell et al. 2011). et al. (2011), however, found that the intertidal macroinvertebrate community composition Hubbell’s theory basically states that by replacing one species for another or by eliminating all of a South African sandy beach did not primarily respond to physical changes, but that these species but one, this will have no effect on the community functioning (e.g. nutrient cycling). communities were assembled through a complex mixture of environmental factors and To date, there is continuous debate about the importance of niche-based and neutral resource availability, including salinity, beach width and nutrient quality and availability. community assembly (Rosindell et al. 2011), but consensus is emerging that niche-based Moreover, Lastra et al. (2006) found on a Spanish sandy beach that in addition to an increase community assembly and stochastic processes may operate simultaneously to assemble in intertidal species richness with a decrease in mean grain size and an increase in beach width, biological communities (Weiher et al. 2011, Vellend et al. 2014, Conradi et al. 2017). there was a positive relationship between food availability (measured as chlorophyll-a in the 2.2.2 Assembly processes on sandy beaches water column) and intertidal species richness. A recent global meta-analysis indicated that beach slope, tidal range and chlorophyll-a combined were the most important explanatory In sandy beach ecology, the existing paradigm is that biological communities are primarily variables of intertidal macroinvertebrate richness, closely followed by grain size (Defeo et al. structured by physical control, i.e. the environmental filter, while biological interactions such 2017). This suggests that environmental factors and biological interactions related to resource as competition, i.e. the limiting similarity filter, are considered to be less influential (Defeo and availability combined may alter intertidal macroinvertebrate community composition. It may McLachlan 2005). First, many intertidal macroinvertebrate species depend on local be that physical factors on their own have a less powerful predictive ability of intertidal hydrodynamic forces for dispersal, i.e. the dispersal filter (Günther 1992, Van Tomme et al. macroinvertebrate community composition, and that the changes in resource availability 2013). ‘Source’ populations with a continuous age population structure may seed sandy elicited by these physical factors and subsequent competition are more important drivers of beaches with harsh environmental conditions that harbour ‘sink’ populations containing few community assembly. Finally, environmental factors may act on the macro-scale (between age classes, postulated as the source-sink hypothesis (Defeo and McLachlan 2005). The climate zones and morphodynamic beach types) and meso-scale (between beaches), while autecological hypothesis states that communities in a physically stressed environment, such biological interactions may determine the final intertidal macroinvertebrate community as the intertidal zone of an exposed sandy beach, are structured by the independent composition on the micro-scale (within beaches) (Defeo and McLachlan 2005). responses of individual species to this environment, rendering biological interactions largely unimportant (Noy-Meir 1979, McLachlan 2001). More specifically, the swash exclusion Less theory related to community assembly has been developed for the macroinvertebrate hypothesis states that on reflective beaches the hasher swash climate excludes, or filters, community of the supratidal zone. The habitat safety hypothesis states that microtidal, species from the regional species pool (McLachlan et al. 1993). The combination of coarse reflective beaches, due to their narrow swash and steep slope, provide a more stable habitat sand and a turbulent swash make it difficult for species to burrow in the intertidal zone, for supratidal macroinvertebrates, such as talitrids (Defeo and Gómez 2005). On these leading to a lower abundance and species richness on reflective beaches (Defeo and beaches, supratidal macroinvertebrates run a lower risk to be submerged by the sea as the McLachlan 2011). As a result, intertidal macroinvertebrates on reflective beaches must supratidal zone is not frequently inundated and macroinvertebrates are not affected by the attribute more energy to maintenance, while less energy is available for reproduction and this interaction between coarse sand and turbulent swash (Defeo and Gómez 2005). This results

General introduction 19 approach this is to determine the relative importance of abiotic and biotic drivers of the idea has been postulated as the habitat harshness hypothesis (Defeo et al. 2001). Towards assembly process and if the factors can be captured in ‘rules’ (HilleRisLambers et al. 2012). more dissipative beaches, however, the physical environment becomes more benign and Classical assembly rules are proposed by Diamond (1975) stating that interspecific interactions biological interactions may become more important as a driver of community assembly. (mainly competition) lead to a non-random co-existence of species within a community. This Abundance and species richness increase towards these more dissipative beaches, leading to view was expanded by Keddy (1992), proposing that both the biotic and abiotic environment a greater potential for encounters between individuals and hence biological interactions act like a filter, or set of filters, selecting species based on their traits from the species pool (McLachlan and Brown 2006, Defeo and McLachlan 2011). This is not merely due to the effect (see Figure 1.4, upper part). Through the stochastic processes dispersal and migration, a set of beach width itself, but a wide beach contains more areas that are less severely influenced of species is selected from the regional species pool (dispersal filter). Then, species are filtered by abiotic stress caused by the sea, allowing for more different species to inhabit this beach by local, deterministic processes from the environment (environmental filter) and via (McLachlan and Dorvlo 2007). biological interactions, especially competition (limiting similarity filter). In the end, a Evidence indicating that biological interactions may be more important for intertidal community is assembled of which the composition depends on the influence of each filter community assembly on sandy beaches than previously recognised, is slowly accumulating. present and what these filters comprise of in a specific ecosystem (Márquez and Kolasa 2013, Previous studies have primarily focused on physical control of macroinvertebrate Götzenberger et al. 2011). Contrasting thoughts on assembly rules are given by Hubbell (2001) communities but did not include main drivers such as competition for resources or who proposed the ‘unified neutral theory of biodiversity and biogeography’, which is based investigated the relative effect of the environment and biological interactions on final on the assumption that differences between individuals of the same trophic level are ‘neutral’, community composition (exceptions include Defeo et al. 1997, Dugan et al. 2004, Van Tomme and therefore these differences are irrelevant for their success. It means that all individuals et al. 2012). Studies that included biological interactions were mainly aimed at understanding within a trophic level have the same chances for migration, birth and death. Communities are zonation patterns of co-occurring species, instead of community responses. Ortega-Cisneros then assembled by dispersal limitation, speciation and ecological drift (Rosindell et al. 2011). et al. (2011), however, found that the intertidal macroinvertebrate community composition Hubbell’s theory basically states that by replacing one species for another or by eliminating all of a South African sandy beach did not primarily respond to physical changes, but that these species but one, this will have no effect on the community functioning (e.g. nutrient cycling). communities were assembled through a complex mixture of environmental factors and To date, there is continuous debate about the importance of niche-based and neutral resource availability, including salinity, beach width and nutrient quality and availability. community assembly (Rosindell et al. 2011), but consensus is emerging that niche-based Moreover, Lastra et al. (2006) found on a Spanish sandy beach that in addition to an increase community assembly and stochastic processes may operate simultaneously to assemble in intertidal species richness with a decrease in mean grain size and an increase in beach width, biological communities (Weiher et al. 2011, Vellend et al. 2014, Conradi et al. 2017). there was a positive relationship between food availability (measured as chlorophyll-a in the 2.2.2 Assembly processes on sandy beaches water column) and intertidal species richness. A recent global meta-analysis indicated that beach slope, tidal range and chlorophyll-a combined were the most important explanatory In sandy beach ecology, the existing paradigm is that biological communities are primarily variables of intertidal macroinvertebrate richness, closely followed by grain size (Defeo et al. structured by physical control, i.e. the environmental filter, while biological interactions such 2017). This suggests that environmental factors and biological interactions related to resource as competition, i.e. the limiting similarity filter, are considered to be less influential (Defeo and availability combined may alter intertidal macroinvertebrate community composition. It may McLachlan 2005). First, many intertidal macroinvertebrate species depend on local be that physical factors on their own have a less powerful predictive ability of intertidal hydrodynamic forces for dispersal, i.e. the dispersal filter (Günther 1992, Van Tomme et al. macroinvertebrate community composition, and that the changes in resource availability 2013). ‘Source’ populations with a continuous age population structure may seed sandy elicited by these physical factors and subsequent competition are more important drivers of beaches with harsh environmental conditions that harbour ‘sink’ populations containing few community assembly. Finally, environmental factors may act on the macro-scale (between age classes, postulated as the source-sink hypothesis (Defeo and McLachlan 2005). The climate zones and morphodynamic beach types) and meso-scale (between beaches), while autecological hypothesis states that communities in a physically stressed environment, such biological interactions may determine the final intertidal macroinvertebrate community as the intertidal zone of an exposed sandy beach, are structured by the independent composition on the micro-scale (within beaches) (Defeo and McLachlan 2005). responses of individual species to this environment, rendering biological interactions largely unimportant (Noy-Meir 1979, McLachlan 2001). More specifically, the swash exclusion Less theory related to community assembly has been developed for the macroinvertebrate hypothesis states that on reflective beaches the hasher swash climate excludes, or filters, community of the supratidal zone. The habitat safety hypothesis states that microtidal, species from the regional species pool (McLachlan et al. 1993). The combination of coarse reflective beaches, due to their narrow swash and steep slope, provide a more stable habitat sand and a turbulent swash make it difficult for species to burrow in the intertidal zone, for supratidal macroinvertebrates, such as talitrids (Defeo and Gómez 2005). On these leading to a lower abundance and species richness on reflective beaches (Defeo and beaches, supratidal macroinvertebrates run a lower risk to be submerged by the sea as the McLachlan 2011). As a result, intertidal macroinvertebrates on reflective beaches must supratidal zone is not frequently inundated and macroinvertebrates are not affected by the attribute more energy to maintenance, while less energy is available for reproduction and this interaction between coarse sand and turbulent swash (Defeo and Gómez 2005). This results

20 Chapter 1 in a less harsh environment and a less narrow environmental filter, allowing more supratidal a North-American coast (McLachlan 1990). Supratidal macroinvertebrates may also reach high macroinvertebrates to inhabit this sandy beach. Although abundance and species richness of densities in wrack patches up to 455 individuals m-2 on an Australian beach (adapted from Ince crustaceans in the supratidal zone increased towards reflective beaches, supporting the et al. 2007) and up to 6098 individuals m-2 on a Baltic sandy beach (adapted from Jędrzejczak habitat safety hypothesis, insects showed the opposite trend with higher species richness at 2002b). These high densities enhance the chance to encounter and interact, which may lead more dissipative beaches (Defeo and McLachlan 2011). This difference may be related to their to intra- and interspecific competition for space and resources, such as food. Food supply has distribution, with crustaceans extending towards the sea and insects extending landwards into been shown to be important for structuring both intertidal and supratidal communities on the dunes, but the drivers of insect communities in the supratidal zone remain largely sandy beaches, in the form of phytoplankton in the water column (Lastra et al. 2006, unknown (Defeo and McLachlan 2011). Bergamino et al. 2016), in situ production by benthic microalgae (Schlacher and Hartwig 2013) and beach cast sea weed (e.g. Ince et al. 2007). As the supratidal macroinvertebrate community is less directly influenced by the sea, resource availability such as wrack input has an important structuring effect on the supratidal Intra- and interspecific competition affect the cross-shore zonation of intertidal macroinvertebrate community (Colombini and Chelazzi 2003). This is especially the case since macroinvertebrates, and hence community composition (Defeo and McLachlan 2005). supratidal macroinvertebrates associated with wrack are generally characterised by a limited Intraspecific encounter competition has for example been observed for Bathyporeia sarsi, dispersal ability and a direct larval development (e.g. talitrids), making them heavily especially under low food conditions, which may explain its limited distribution in the higher dependent on this resource (Grantham et al. 2003, Dugan et al. 2000, Schooler et al. 2017). intertidal zone compared to the co-occurring B. pilosa (Van Tomme et al. 2012). In addition, Wrack provides both food and habitat, e.g. refuge from severe environmental conditions and higher up the intertidal zone environmental conditions are harsher and food availability lower space for reproduction, to the supratidal macroinvertebrate community (Dugan et al. 2003, than in the mid intertidal zone, to which B. pilosa is better adapted than B. sarsi (Van Tomme Ince et al. 2007). Freshly deposited wrack is swiftly colonised by supratidal macroinvertebrates et al. 2012). Interspecific competition, for example, between two intertidal isopod species after which a succession of macroinvertebrate species is initiated (Colombini et al. 2000, resulted in the displacement of Excirolana braziliensis Richardson to coarser sands and higher Olabarria et al. 2007). The spatial distribution, amount, identity (i.e. sea weed species), quality up the intertidal zone by Excirolana armata Dana (Defeo et al. 1997). Furthermore, and microhabitat features of wrack on the beach all drive the supratidal macroinvertebrate interference competition for space has been recorded between a hippid crab and a bivalve at composition (Colombini and Chelazzi 2003). For example, macroinvertebrate species richness the moment of burrowing in the intertidal zone, resulting in longer burrowing times and is greater in wrack patches deposited higher on the beach than wrack patches lower on the greater exposure to the swash climate (Dugan et al. 2004). This could in turn affect both beach, with a higher temperature and lower moisture content of wrack at high tidal levels zonation and community composition of intertidal macroinvertebrates. Interspecific (Ruiz-Delgado et al. 2015). Smaller patches of wrack harboured less macroinvertebrate species competition for food was suggested by a stable isotope study, revealing that intertidal and individuals than larger wrack patches (Olabarria et al. 2007), following the rules of island macroinvertebrates had a high niche-overlap in a low-food environment, thus species are biogeography (MacArthur and Wilson 1967). Native versus invasive sea weed species in wrack expected to compete strongly for these food sources (Ortega-Cisneros et al. 2017). In another showed a different macroinvertebrate colonisation pattern, possibly related to differences in study, the intertidal zonation of four amphipod species was related to differences in feeding nutritional quality, temperature and humidity of wrack (Rodil et al. 2008). With an increase in habits and preferred food source, thereby avoiding food competition (Yu et al. 2002). wrack age, macroinvertebrate succession occurs and macroinvertebrate abundance, richness Biological interactions have also been documented for supratidal macroinvertebrates within and community composition change over time (Colombini et al. 2000, Jędrzejczak 2002b, wrack patches (Colombini and Chelazzi 2003). Both intra- and interspecific competition Olabarria et al. 2007). As the wrack is less fresh and more decomposed, the quality of the litter occurred at high densities of the Diptera larvae Coelopa frigida Fabricius and Coelopa pilipes decreases and differences in wrack quality may attract a varied macroinvertebrate community Haliday in wrack, which was likely related to food limitations (Leggett et al. 1996). These (Olabarria et al. 2010). Thus, supratidal macroinvertebrate communities, as is the case for Diptera larvae were able to co-exist within a wrack patch by inhabiting either cooler (C. frigida) intertidal macroinvertebrate communities, appear to be structured by a complex interaction or warmer (C. pilipes) parts, hence avoiding competition (Phillips et al. 1995). In addition, the between environmental factors and biological interactions related to resource availability. larvae of C. frigida, C. pilipes and Thoracochaeta zosterae Haliday were found occupying wrack 2.2.3 The role of resource competition on sandy beaches patches at the same time in high abundances, indicating a potential for competitive interactions (Hodge and Arthur 1997). This was confirmed in a laboratory experiment showing Biological interactions have long been proven to be a major driver of community assembly in that of these three Diptera species, the larvae of C. frigida were the strongest competitor for a wide range of ecosystems. On sandy beaches, biological interactions, such as competition, food (Hodge and Arthur 1997). For two supratidal amphipod species (Talitrus saltator and have the potential to structure macroinvertebrate communities where macroinvertebrates Talorchestia brito Stebbing) and an isopod species (Tylos europaeus Arcangeli), a strong are densely aggregated in a small area. Intertidal macroinvertebrate densities can locally be temporal effect on niche-partitioning was observed when foraging on freshly deposited wrack, high and may be up to 13.000 individuals m-2 of surface area on Belgium beaches (Degraer et reducing competition and promoting co-existence among these species (Lastra et al. 2010). al. 2003), but have even been reported to exceed 280.000 individuals m-2 of surface area along

General introduction 21 in a less harsh environment and a less narrow environmental filter, allowing more supratidal a North-American coast (McLachlan 1990). Supratidal macroinvertebrates may also reach high macroinvertebrates to inhabit this sandy beach. Although abundance and species richness of densities in wrack patches up to 455 individuals m-2 on an Australian beach (adapted from Ince crustaceans in the supratidal zone increased towards reflective beaches, supporting the et al. 2007) and up to 6098 individuals m-2 on a Baltic sandy beach (adapted from Jędrzejczak habitat safety hypothesis, insects showed the opposite trend with higher species richness at 2002b). These high densities enhance the chance to encounter and interact, which may lead more dissipative beaches (Defeo and McLachlan 2011). This difference may be related to their to intra- and interspecific competition for space and resources, such as food. Food supply has distribution, with crustaceans extending towards the sea and insects extending landwards into been shown to be important for structuring both intertidal and supratidal communities on the dunes, but the drivers of insect communities in the supratidal zone remain largely sandy beaches, in the form of phytoplankton in the water column (Lastra et al. 2006, unknown (Defeo and McLachlan 2011). Bergamino et al. 2016), in situ production by benthic microalgae (Schlacher and Hartwig 2013) and beach cast sea weed (e.g. Ince et al. 2007). As the supratidal macroinvertebrate community is less directly influenced by the sea, resource availability such as wrack input has an important structuring effect on the supratidal Intra- and interspecific competition affect the cross-shore zonation of intertidal macroinvertebrate community (Colombini and Chelazzi 2003). This is especially the case since macroinvertebrates, and hence community composition (Defeo and McLachlan 2005). supratidal macroinvertebrates associated with wrack are generally characterised by a limited Intraspecific encounter competition has for example been observed for Bathyporeia sarsi, dispersal ability and a direct larval development (e.g. talitrids), making them heavily especially under low food conditions, which may explain its limited distribution in the higher dependent on this resource (Grantham et al. 2003, Dugan et al. 2000, Schooler et al. 2017). intertidal zone compared to the co-occurring B. pilosa (Van Tomme et al. 2012). In addition, Wrack provides both food and habitat, e.g. refuge from severe environmental conditions and higher up the intertidal zone environmental conditions are harsher and food availability lower space for reproduction, to the supratidal macroinvertebrate community (Dugan et al. 2003, than in the mid intertidal zone, to which B. pilosa is better adapted than B. sarsi (Van Tomme Ince et al. 2007). Freshly deposited wrack is swiftly colonised by supratidal macroinvertebrates et al. 2012). Interspecific competition, for example, between two intertidal isopod species after which a succession of macroinvertebrate species is initiated (Colombini et al. 2000, resulted in the displacement of Excirolana braziliensis Richardson to coarser sands and higher Olabarria et al. 2007). The spatial distribution, amount, identity (i.e. sea weed species), quality up the intertidal zone by Excirolana armata Dana (Defeo et al. 1997). Furthermore, and microhabitat features of wrack on the beach all drive the supratidal macroinvertebrate interference competition for space has been recorded between a hippid crab and a bivalve at composition (Colombini and Chelazzi 2003). For example, macroinvertebrate species richness the moment of burrowing in the intertidal zone, resulting in longer burrowing times and is greater in wrack patches deposited higher on the beach than wrack patches lower on the greater exposure to the swash climate (Dugan et al. 2004). This could in turn affect both beach, with a higher temperature and lower moisture content of wrack at high tidal levels zonation and community composition of intertidal macroinvertebrates. Interspecific (Ruiz-Delgado et al. 2015). Smaller patches of wrack harboured less macroinvertebrate species competition for food was suggested by a stable isotope study, revealing that intertidal and individuals than larger wrack patches (Olabarria et al. 2007), following the rules of island macroinvertebrates had a high niche-overlap in a low-food environment, thus species are biogeography (MacArthur and Wilson 1967). Native versus invasive sea weed species in wrack expected to compete strongly for these food sources (Ortega-Cisneros et al. 2017). In another showed a different macroinvertebrate colonisation pattern, possibly related to differences in study, the intertidal zonation of four amphipod species was related to differences in feeding nutritional quality, temperature and humidity of wrack (Rodil et al. 2008). With an increase in habits and preferred food source, thereby avoiding food competition (Yu et al. 2002). wrack age, macroinvertebrate succession occurs and macroinvertebrate abundance, richness Biological interactions have also been documented for supratidal macroinvertebrates within and community composition change over time (Colombini et al. 2000, Jędrzejczak 2002b, wrack patches (Colombini and Chelazzi 2003). Both intra- and interspecific competition Olabarria et al. 2007). As the wrack is less fresh and more decomposed, the quality of the litter occurred at high densities of the Diptera larvae Coelopa frigida Fabricius and Coelopa pilipes decreases and differences in wrack quality may attract a varied macroinvertebrate community Haliday in wrack, which was likely related to food limitations (Leggett et al. 1996). These (Olabarria et al. 2010). Thus, supratidal macroinvertebrate communities, as is the case for Diptera larvae were able to co-exist within a wrack patch by inhabiting either cooler (C. frigida) intertidal macroinvertebrate communities, appear to be structured by a complex interaction or warmer (C. pilipes) parts, hence avoiding competition (Phillips et al. 1995). In addition, the between environmental factors and biological interactions related to resource availability. larvae of C. frigida, C. pilipes and Thoracochaeta zosterae Haliday were found occupying wrack 2.2.3 The role of resource competition on sandy beaches patches at the same time in high abundances, indicating a potential for competitive interactions (Hodge and Arthur 1997). This was confirmed in a laboratory experiment showing Biological interactions have long been proven to be a major driver of community assembly in that of these three Diptera species, the larvae of C. frigida were the strongest competitor for a wide range of ecosystems. On sandy beaches, biological interactions, such as competition, food (Hodge and Arthur 1997). For two supratidal amphipod species (Talitrus saltator and have the potential to structure macroinvertebrate communities where macroinvertebrates Talorchestia brito Stebbing) and an isopod species (Tylos europaeus Arcangeli), a strong are densely aggregated in a small area. Intertidal macroinvertebrate densities can locally be temporal effect on niche-partitioning was observed when foraging on freshly deposited wrack, high and may be up to 13.000 individuals m-2 of surface area on Belgium beaches (Degraer et reducing competition and promoting co-existence among these species (Lastra et al. 2010). al. 2003), but have even been reported to exceed 280.000 individuals m-2 of surface area along

22 Chapter 1

This finding was supported by a stable isotope study, showing that these co-occurring species supratidal zones (Speybroeck et al. 2006, Schlacher et al. 2012). During foreshore adopt different feeding strategies when wrack availability is low (Bessa et al. 2014a). nourishment, sand is usually deposited on the seaside part of the bar closest to the beach. This does prevent direct mortality of intertidal and supratidal organisms as sand is gradually 2.3 Sand nourishment effects on the macroinvertebrate community deposited onto the beach, but local subtidal communities are heavily affected instead 2.3.1 A history of sand nourishment and its ecological impacts (Speybroeck et al. 2006). Sand nourishments typically have to be applied every three to five years to prevent beaches from further erosion and to maintain the coast line in position (van Coastal squeeze, where beaches are trapped between the rising sea level and static Dalfsen and Aarninkhof 2009). As ecological communities need time to recover after a anthropogenic structures on the land side (Defeo et al. 2009), causes severe erosion of the disturbance such as sand nourishment, the timing, frequency and size of the sand sandy beach, threatening the human population and livelihood as the sea advances inland and nourishment are crucial for its impact on the sandy beach food web (Speybroeck et al 2006). leaving only a narrow strip for ecological communities to reside. To mitigate the effects of Even though intertidal macroinvertebrate species can recolonise a beach that has received beach erosion, effective coastal defence strategies are needed. Up until the second half of the regular beach nourishment within one year after disturbance, community composition does 20th century, hard coastal defence structures, including seawalls, groynes and dykes, had been differ from beaches without nourishment (Leewis et al. 2012). Changes in the intertidal extensively employed to protect the coast (Hanley et al. 2014). The construction of hard macroinvertebrate community due to beach nourishment may propagate upwards in the food coastal defence structures changes the coastal environment and directly impacts local web to e.g. birds, with fewer birds foraging on a nourished beach with a lower intertidal biodiversity as soft-sediment habitat is replaced by artificial hard substrate (Airoldi et al. macroinvertebrate abundance (Peterson et al. 2006). This indicates that although 2005). Indirect effects are the disruption of coastal hydrodynamics and reduction of habitat macroinvertebrate species are well adapted to the highly dynamic environment of the connectivity altering the flow of sand, nutrients and organisms between adjacent sandy intertidal zone and can quickly colonise bare sands (McLachlan and Brown 2006), there may beaches that are separated by hard coastal defence structures, which impact sandy beach nevertheless be long-term negative impacts of sand nourishment on the macroinvertebrate communities (Hanley et al. 2014). Thus, even though hard coastal defence structures can community and the sandy beach food web (Speybroeck et al. 2008a). Therefore, alternative locally be effective to protect against flooding, adjacent sandy beaches may suffer from low nourishment strategies are called for to limit negative effects on these intertidal sediment supply and increased erosion (Hanley et al. 2014). This hampers coastal protection macroinvertebrate communities of the sandy beach. along a wider stretch of coast, as complementary measures to the hard coastal defence structures would be needed. 2.3.2 A novel approach: The Sand Motor mega-nourishment To account for the dynamic nature of the sandy coast and its biogeochemical linkages, soft- As a more ecologically and sustainable alternative to current regular beach and foreshore sediment strategies have become more common as a sustainable form of coastal defence nourishment, a mega-nourishment has been proposed. To test the economic, anthropogenic (Hanson et al. 2002). A common soft-sediment strategy is sand nourishment, where eroded and environmental implications of this novel approach, the so-called ‘Sand Motor’ project was beaches are nourished by frequently applying a large volume of sand to increase coastal started in 2011 along the Dutch main coast (Stive et al. 2013; Figure 1.3). A very large volume sediment budgets and to widen the beach (Cooke et al. 2012). Depending on the cross-shore of sand (approximately 20 Mm3) was strategically deposited in connection to the coast, placement of the sand, several types of sand nourishment are distinguished, including forming a hook-shaped artificial peninsula initially extending 2 km along the coast and foreshore (placement in the shallow subtidal zone), backshore (placement in the dunes), and protruding 1 km into the sea (de Schipper et al. 2016). This mega-nourishment is a regular beach or profile nourishment (placement in the intertidal and supratidal zones) combination of regular beach and foreshore nourishment, but it is unique in its size and low (Speybroeck et al. 2006). Sand nourishments were first employed in the 1950s and have been frequency of placement. Instead of regularly applying smaller-scale sand nourishments every increasingly applied from the 1990s onwards within Europe (Hanson et al. 2002). In the three to five years as is the current practice in the Netherlands, this mega-nourishment has Netherlands, the first sand nourishments were deployed in 1970, but from 1990 onwards sand an expected life time of about twenty years (van Dalfsen and Aarninkhof 2009). After nourishments have been used on a larger scale to prevent further coastal erosion and construction, the sand is gradually redistributed through hydrodynamics and aeolian maintain the current coast line (Hanson et al. 2002; Baptist and Wiersinga 2012). In the transport, nourishing beaches further along the coast (de Schipper et al. 2016). This is in sharp beginning, mostly beach nourishments were used, but around 2000 foreshore nourishments contrast with regular beach nourishments, where a sandy beach is nourished directly and became more common (Baptist and Wiersinga 2012). locally with the desired volume. A mega-nourishment thus decreases the number of local pulse disturbances to the sandy beach ecosystem over time, as a very large, concentrated Although sand nourishment has been considered as an ecologically friendly alternative to hard volume of sand is placed at one single occasion. The primary management goal of the Sand coastal defence structures (Hanley et al. 2014), it generally causes temporal local extinction Motor mega-nourishment is coastal protection, with increased space for recreation and of sandy beach flora and fauna (Speybroeck et al. 2006, Leewis et al. 2012). During regular nature as additional goals. beach nourishment, a thick layer of sand (up to a few meters) is deposited on top of the beach, causing burial and mortality of primary vegetation and invertebrates of both the intertidal and

General introduction 23

24 Chapter 1

2.3.3 Potential mega-nourishment effects on the macroinvertebrate community different from an undisturbed community in an adjacent area (Dernie et al. 2003). For the intertidal macroinvertebrate community, recovery primarily depends on the dispersal Sand nourishment can be viewed as a significant disturbance to the sandy beach ecosystem capacity of juveniles and adults, i.e. the dispersal filter, and their species-specific habitat with various effects on its ecological communities (Speybroeck et al. 2006). As mentioned requirements during and after settlement, i.e. the environmental filter (Van Tomme et al. earlier, one direct effect is the burial and local extinction of ecological communities during 2013). Dispersal of intertidal macroinvertebrates can be either passive or active in the water application of the sand nourishment (Speybroeck et al. 2006, Schlacher et al. 2012). The same column, at the sediment surface and within the sediment, which is affected by hydrodynamic holds for a mega-nourishment, which may even have a larger initial impact on forces (Günther 1992). The shape of the Sand Motor mega-nourishment is expected to change macroinvertebrate communities due to its large size. However, as the frequency of the strength and direction of local currents around the hook, especially during the first three nourishment is much lower and along shore beaches are gradually nourished by the mega- years after completion when the hook-shape is most pronounced (Meirelles et al. 2017). This nourishment, potentially limiting disturbance by sand deposition, it may finally have a lower may influence the dispersal of intertidal macroinvertebrates and may be reflected in an combined impact on the macroinvertebrate community compared to regular beach and impoverished macroinvertebrate community, with lower abundances and/or a subset of foreshore nourishment. Therefore, I will focus here on the potential effects of a mega- species from surrounding beaches. Beach geomorphology and local hydrodynamics can thus nourishment on the macroinvertebrate community after completion of sand deposition. create either a barrier or an opportunity for successful dispersal (Van Tomme et al. 2013). Effects on macroinvertebrate community assembly processes can be both direct (change in After dispersal, the settlement of intertidal macroinvertebrates is determined by its habitat characteristics) and indirect (change in dispersal and food availability; Figure 1.4). After interactions with the new habitat (Todd 1998). For a successful recovery, the individual species completion, the mega-nourishment itself will, as is the case with regular beach nourishments, must match the specific habitat conditions and one factor for intertidal macroinvertebrates is initially provide a new beach that can be recolonised by organisms. Recovery by recolonisation the median grain size of the substrate (Speybroeck et al. 2006). The amphipod B. sarsi and the can be assumed to be completed when the disturbed community is no longer significantly isopod E. pulchra have a preference for fine sediments, while the amphipod B. pilosa and to a greater extent the polychaete worm S. squamata prefer coarser sediments (Van Tomme et al. 2013). As the median grain size of the Sand Motor mega-nourishment is slightly courser than the original beach and shows spatial heterogeneity in the years after completion, this may be one structuring factor of intertidal communities at the Sand Motor mega-nourishment (Huisman et al. 2014). When macroinvertebrates have established in the intertidal zone, post-settlement processes such as competition, i.e. the limiting similarity filter, will finally shape the intertidal macroinvertebrate community present at a sandy beach (Todd 1998). The change of local hydrodynamics around the hook of the Sand Motor mega-nourishment is, in addition to macroinvertebrate dispersal, expected to change resource availability by influencing the distribution of phytoplankton and benthic microalgae. Phytoplankton may become an important food source in highly hydrodynamic environments (Menge 2000). Sediments that are continuously disturbed by waves and currents have a lower benthic microalgae biomass in comparison to sheltered, less disturbed beaches (Forehead et al. 2013). At the Sand Motor mega-nourishment, low hydrodynamic conditions are expected to be present in the lagoon which is sheltered from the high hydrodynamic forces of the open sea. These changes in the quantity and quality of food may impact the outcome of species interactions and community composition, as macroinvertebrate species exhibit differences in feeding preference. For example, S. squamata and E. pulchra did not make a clear choice between phytoplankton and benthic microalgae, where B. sarsi and B. pilosa did show a preference for benthic microalgae (Maria et al. 2011). When competition for food occurs for these intertidal macroinvertebrate Figure 1.3 Aerial pictures of the Sand Motor mega-nourishment along the Dutch coast. Left: Overall species, species may focus on other food sources or relocate to an area where shape of the Sand Motor mega-nourishment, protruding from the relatively straight Dutch coast line macroinvertebrate densities are lower. into the sea. Upper right: Sand Motor mega-nourishment shortly after completion in July 2011. Lower right: Sand Motor mega-nourishment four years after completion in January 2015. Another envisioned advantage of a mega-nourishment is that the large volume of sand allows for the construction of certain geomorphological shapes, which gives the possibility to

General introduction 25

26 Chapter 1 increase the diversity of habitats, for example by creating sheltered intertidal zones, attracting relevant. Finally, the Sand Motor mega-nourishment is expected to lead to an increase in a wider variety of species. An increase in environmental heterogeneity at landscape level recreational visitors, which is an additional management goal. High recreational pressure may, generally leads to an increase in species diversity (Stein et al. 2014, Tamme et al. 2010). For however, have a negative effect on supratidal macroinvertebrates, for example by human coastal systems in particular, it is found that habitat heterogeneity on a larger scale, up to 1 trampling, high use of off-road vehicles and wrack removal during beach cleaning (Defeo et al. km, is a driver of intertidal macroinvertebrate species richness (Archambault and Bourget 2009). 1996). Thus, the hook-shape of the Sand Motor mega-nourishment has the potential to Overall, the Sand Motor mega-nourishment is expected to have a significant effect on various increase species richness and diversity through a local increase in large-scale heterogeneity of community assembly processes, hence altering macroinvertebrate community composition, the sandy beach. The potential effects of a mega-nourishment on the supratidal food web dynamics and ecosystem functioning of the sandy beach. macroinvertebrate community are less clear. As wrack input may depend on beach type, hydrodynamic forces and buoyancy characteristics of wrack (Orr et al. 2005), wrack may be 1.4 Thesis aims and outline heterogeneously distributed around the hook-shaped Sand Motor mega-nourishment, Sandy beach ecology is a relatively new discipline and although progress has been made in potentially affecting macroinvertebrate community composition. Other effects may be broadening the scope and integrating general ecological theory, many research challenges related to the increase in beach width after application of the mega-nourishment, allowing for remain (Nel et al. 2014). Sandy beaches are not expected to be conceptually different from the formation of multiple drift lines and increasing the potential for embryo dune formation other ecosystems, but there are some specific and strong physical forces acting on this (van Puijenbroek et al. 2017). Since the major goal of sand nourishment is coastal protection ecosystem and the relative importance of community assembly filters may therefore be and dune formation contributes to this goal, understanding the interactive effect of wrack and different compared to other marine and terrestrial ecosystems. In the field of community macroinvertebrate community composition on plant establishment on sandy beaches is highly assembly, the importance of e.g. species interactions and colonisation rates needs to be

studied in macroinvertebrate communities of sandy beaches to test the generality of 2 + 4 community assembly theory from other ecosystems (Schlacher et al. 2015). In addition, macroinvertebrate communities of sandy beaches show widespread functional redundancy, especially in the intertidal zone (Schlacher et al. 2008), allowing for critical ecological testing. In the field of ecosystem functioning, sandy beaches as a whole provide many ecosystem functions, including nutrient cycling, but this has rarely been quantified (Schlacher et al. 2008, 3 + 5 Nel et al. 2014). It also remains largely unknown what the effect is of changes in macroinvertebrate community composition on ecosystem functioning. Finally, more emphasis can be placed on general concepts regarding cross-boundary connectivity across an ecological interface in the context of sandy beaches, as they represent a wide-spread interface region in the coastal zone (Schlacher et al. 2015, Gounand et al. 2018). Many knowledge gaps related to the integration of ecological attributes in sandy beach management are also in need to be addressed (Jones et al. 2017). These include studying the effect of nourishment on ecological communities and their recovery trajectories, providing management information on the design of monitoring programs to track community changes over time and guiding the design and development of (nourished) beaches for specific (ecological) purposes (Schlacher et al. 2008). It is clear from the above that many questions remain unanswered regarding the ecology of macroinvertebrate communities on sandy beaches, especially in the light of resource Figure 1.4 A model of niche-based community assembly and the impact of changes in coastal zone availability and biological interactions. Although abiotic drivers strongly determine geomorphology (placement of a mega-nourishment) on the three filters: dispersal, environmental and macroinvertebrate community composition on sandy beaches, research endeavors indicating limiting similarity. A change in the coastal zone geomorphology can have both direct effects (continuous arrows in the lower part of the figure) and indirect effects (dotted arrows in the lower part the importance of biological interactions are steadily increasing. However, detailed studies on of the figure) on the assembly filters. After each filter, less species remain in the species pool, finally the role of biological interactions, resource competition in particular, are needed to further resulting in a specific biological community (the far-right and smallest circle). This actual biological understand the assembly and composition of macroinvertebrate communities and its effect community then influences ecosystem functioning. Numbers correspond to the chapters in this thesis on ecosystem functioning. The effect of marine organic matter crossing the land-ocean and indicate which part of the conceptual model was studied. interface on terrestrial organisms (supratidal macroinvertebrates and plants) and nutrient

General introduction 27 increase the diversity of habitats, for example by creating sheltered intertidal zones, attracting relevant. Finally, the Sand Motor mega-nourishment is expected to lead to an increase in a wider variety of species. An increase in environmental heterogeneity at landscape level recreational visitors, which is an additional management goal. High recreational pressure may, generally leads to an increase in species diversity (Stein et al. 2014, Tamme et al. 2010). For however, have a negative effect on supratidal macroinvertebrates, for example by human coastal systems in particular, it is found that habitat heterogeneity on a larger scale, up to 1 trampling, high use of off-road vehicles and wrack removal during beach cleaning (Defeo et al. km, is a driver of intertidal macroinvertebrate species richness (Archambault and Bourget 2009). 1996). Thus, the hook-shape of the Sand Motor mega-nourishment has the potential to Overall, the Sand Motor mega-nourishment is expected to have a significant effect on various increase species richness and diversity through a local increase in large-scale heterogeneity of community assembly processes, hence altering macroinvertebrate community composition, the sandy beach. The potential effects of a mega-nourishment on the supratidal food web dynamics and ecosystem functioning of the sandy beach. macroinvertebrate community are less clear. As wrack input may depend on beach type, hydrodynamic forces and buoyancy characteristics of wrack (Orr et al. 2005), wrack may be 1.4 Thesis aims and outline heterogeneously distributed around the hook-shaped Sand Motor mega-nourishment, Sandy beach ecology is a relatively new discipline and although progress has been made in potentially affecting macroinvertebrate community composition. Other effects may be broadening the scope and integrating general ecological theory, many research challenges related to the increase in beach width after application of the mega-nourishment, allowing for remain (Nel et al. 2014). Sandy beaches are not expected to be conceptually different from the formation of multiple drift lines and increasing the potential for embryo dune formation other ecosystems, but there are some specific and strong physical forces acting on this (van Puijenbroek et al. 2017). Since the major goal of sand nourishment is coastal protection ecosystem and the relative importance of community assembly filters may therefore be and dune formation contributes to this goal, understanding the interactive effect of wrack and different compared to other marine and terrestrial ecosystems. In the field of community macroinvertebrate community composition on plant establishment on sandy beaches is highly assembly, the importance of e.g. species interactions and colonisation rates needs to be

28 Chapter 1 cycling also requires further attention. In addition, the effect of a novel mega-nourishment on using two contrasting plant species. Plant dry mass and N and P contents of the shoot and the macroinvertebrate community, and how this relates to communities present on beaches roots were determined to assess the effect of either buried or surface wrack and subjected to regular beach nourishment, has not been studied before and requires an in-depth macroinvertebrate presence or absence on plant growth. This allows to experimentally study evaluation. the link between beach-cast sea weed and terrestrial primary production, via macroinvertebrates. In this thesis, I will therefore address two main aims. First, I aim to improve our understanding of the effect of resource availability on species interactions and community assembly of the In Chapter 6 I synthesise and discuss the results of the previous chapters in order to address macroinvertebrate community on sandy beaches, and how this influences ecosystem the main aims and research questions of this thesis. I discuss how resource availability and functioning. Secondly, I aim to investigate the effect of a mega-nourishment on the species interactions shape intertidal and supratidal macroinvertebrate communities on sandy macroinvertebrate community of the sandy beach and identify implications for future sand beaches and how this influences ecosystem functioning. In the end I formulate an answer to nourishments. the question whether a mega-nourishment can be considered a more ecological-friendly alternative than regular beach nourishment for the macroinvertebrate community and This thesis focusses on Dutch sandy beaches that are exposed to high hydrodynamics. The provide recommendations for future coastal management. outline of the chapters in this thesis will briefly indicate which research questions are considered in relation to the thesis aims. How does the intertidal macroinvertebrate community develop after a mega-nourishment?

In Chapter 2 I compare the macroinvertebrate community of the intertidal zone present at a mega-nourishment, beaches subject to regular beach nourishment and unnourished beaches along the Dutch sandy coast. To do this, I constructed a database by combining data from three different sources and performed analyses on macroinvertebrate abundance and richness across the intertidal zone. Macroinvertebrate community patterns at the mega- nourishment are compared before and after implementation (across years and between locations) and between nourishment types. How does resource availability affect the non-additive effects of consumption between intertidal macroinvertebrate species? In Chapter 3 I focus on the effect of a limiting resource, here diatom availability, on the non- additive effects of consumption by a simple intertidal macroinvertebrate community. Diatom consumption was determined in both species’ monocultures and three-species communities based on stable isotope signatures to disentangle positive and negative species interactions at low and high diatom availabilities, driving potential non-additive effects of consumption. Is the supratidal macroinvertebrate community a driver of wrack mineralisation and does this differ between drift lines and seasons? In Chapter 4 I address the question whether the supratidal macroinvertebrate community, in terms of abundance, richness and diversity, is a driver of N and P mineralisation of wrack. Also, I determine whether drift line position and season are drivers of mineralisation. A litter bag experiment was performed in the field for two weeks, where wrack was subjected to natural process to obtain a range of mineralisation and macroinvertebrate community compositions. What is the effect of wrack burial and supratidal macroinvertebrate presence on nutrient availability and beach pioneer plant growth? In Chapter 5 I assess the effects of wrack burial and macroinvertebrate presence on decomposition-driven nutrient availability and subsequently beach pioneer plant growth,

General introduction 29 cycling also requires further attention. In addition, the effect of a novel mega-nourishment on using two contrasting plant species. Plant dry mass and N and P contents of the shoot and the macroinvertebrate community, and how this relates to communities present on beaches roots were determined to assess the effect of either buried or surface wrack and subjected to regular beach nourishment, has not been studied before and requires an in-depth macroinvertebrate presence or absence on plant growth. This allows to experimentally study evaluation. the link between beach-cast sea weed and terrestrial primary production, via macroinvertebrates. In this thesis, I will therefore address two main aims. First, I aim to improve our understanding of the effect of resource availability on species interactions and community assembly of the In Chapter 6 I synthesise and discuss the results of the previous chapters in order to address macroinvertebrate community on sandy beaches, and how this influences ecosystem the main aims and research questions of this thesis. I discuss how resource availability and functioning. Secondly, I aim to investigate the effect of a mega-nourishment on the species interactions shape intertidal and supratidal macroinvertebrate communities on sandy macroinvertebrate community of the sandy beach and identify implications for future sand beaches and how this influences ecosystem functioning. In the end I formulate an answer to nourishments. the question whether a mega-nourishment can be considered a more ecological-friendly alternative than regular beach nourishment for the macroinvertebrate community and This thesis focusses on Dutch sandy beaches that are exposed to high hydrodynamics. The provide recommendations for future coastal management. outline of the chapters in this thesis will briefly indicate which research questions are considered in relation to the thesis aims. How does the intertidal macroinvertebrate community develop after a mega-nourishment?

Chapter 2

A mega-nourishment creates novel habitat for intertidal Chapter 2 macroinvertebrates by enhancing habitat relief A mega-nourishment creates novel habitat for intertidal of the sandy beach macroinvertebrates by enhancing habitat relief

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jeroen W.M. Wijsman, of the sandy beach Lies Leewis, Gerard M. Janssen and Rien Aerts

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jeroen W.M. Wijsman, Lies Leewis, Gerard M. Janssen and Rien Aerts

This chapter has been published in: Estuarine, Coastal and Shelf Science (2018), 207: 232-241 doi: 10.1016/j.ecss.2018.03.003 This chapter has been published in: Estuarine, Coastal and Shelf Science (2018), 207: 232-241

doi: 10.1016/j.ecss.2018.03.003

Chapter 2

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jeroen W.M. Wijsman, of the sandy beach Lies Leewis, Gerard M. Janssen and Rien Aerts

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jeroen W.M. Wijsman, Lies Leewis, Gerard M. Janssen and Rien Aerts

doi: 10.1016/j.ecss.2018.03.003

32 Chapter 2

2.1 Abstract beach, causing burial and mortality of primary vegetation and invertebrates of the intertidal and supratidal zones (Speybroeck et al. 2006, Schlacher et al. 2012). Additional indirect effects Globally, sandy beaches are subject to coastal squeeze due to erosion. Soft-sediment of regular beach nourishment include constraining macroinvertebrate colonisation when strategies, such as sand nourishment, are increasingly applied to mitigate effects of erosion, there is a mismatch in sediment characteristics (e.g. median grain size) between the fill but have long-term negative impacts on beach flora and fauna. As a more ecologically and sediment used for nourishment and the original sediment of the eroded beach (Speybroeck sustainable alternative to regular beach nourishments, a mega-nourishment has been et al. 2006, Vanden Eede et al. 2014). This potentially leads to long-term negative impacts of constructed along the Dutch coast by depositing 21.5 Mm3 of sand, from which sand is sand nourishment on the macroinvertebrate community (Speybroeck et al. 2008a), even gradually redistributed along the coast by natural physical processes. The ‘Sand Motor’ mega- though intertidal macroinvertebrate species are well adapted to the highly dynamic nourishment was constructed as a long-term management alternative for coastal protection environment of the intertidal zone and can quickly colonise bare sands (McLachlan and Brown and is the first large-scale experiment of its kind. We evaluated the development of intertidal 2006). Intertidal macroinvertebrate species can recolonise a beach that has received regular macroinvertebrate communities in relation to this mega-nourishment, and compared it to beach nourishment within one year after disturbance, though community composition does species composition of beaches subject to regular beach or no nourishment. We found that a differ from beaches without nourishment (Leewis et al. 2012). Therefore, alternative mega-nourishment resulted initially in a higher macroinvertebrate richness, but a lower nourishment strategies are called for to constrain negative effects on these intertidal macroinvertebrate abundance, compared to regular beach nourishment. As there was no macroinvertebrate communities on the sandy beach. effect of year after nourishment, this finding suggests that colonisation and/or local extinction were not limiting macroinvertebrate richness at the mega-nourishment. In addition, a mega- As a more ecologically and sustainable alternative to current beach and foreshore nourishment does not converge to an intertidal macroinvertebrate community similar to nourishment practices, a mega-nourishment has been proposed. To test the economical, those on unnourished beaches within a time scale of four years. Beach areas at the mega- anthropogenic and environmental implications of this novel approach, the so-called ‘Sand nourishment sheltered from waves harbored a distinct macroinvertebrate community Motor’ pilot experiment was started in 2011 along the Dutch main coast (Stive et al. 2013). compared to typical wave-exposed sandy beach communities. Thus, a mega-nourishment Instead of regularly applying smaller-scale beach nourishments every three to five years as is temporally creates new habitat for intertidal macroinvertebrates by enhancing habitat relief the current practice in the Netherlands, this mega-nourishment has an expected life time of of the sandy beach. We conclude that a mega-nourishment may be a promising coastal about twenty years, thus decreasing the number of local pulse disturbances to intertidal defence strategy for sandy shores in terms of the macroinvertebrate community of the organisms as a very large volume of sand is placed at one single occasion. After construction, intertidal beach. the mega-nourishment continuously changes in shape over time as deposited sand is gradually transported by wind and waves and nourishes up-stream beaches. On these beaches, 2.2 Introduction intertidal and supratidal macroinvertebrate communities potentially experience limited Sandy beaches are among the most prevalent coastal ecosystems on the planet, harbouring disturbance by sand deposition. Another envisioned advantage of a mega-nourishment is that unique ecological communities that provide a wide variety of ecosystem functions and the large volume of sand allows for the construction of certain geomorphological shapes, services (McLachlan and Brown 2006). Globally, sandy beach ecosystems are subject to coastal which gives the possibility to increase habitat diversity, for example by creating sheltered squeeze, where beaches are negatively affected by both the rising sea level and storm events intertidal zones, attracting a wider variety of species. Enhanced habitat relief generally leads on the sea side and static anthropogenic structures on the land side (Schlacher et al. 2007). to an increase in species diversity (Stein et al. 2014, Tamme et al. 2010). This combination of factors causes severe erosion of the sandy beach, threatening local Here, we focus on species of the macroinvertebrate community of the intertidal sandy beach. ecological communities by leaving only a narrow strip of beach habitat as the sea advances The intertidal macroinvertebrate community is essential for the functioning of the sandy inland. beach ecosystem, including nutrient cycling and the provision of prey species to support A common management strategy to combat coastal squeeze is to replenish eroded sandy predator biodiversity (Defeo et al. 2009). Hence, the intertidal macroinvertebrate community beaches by frequently adding a large volume of sand either in the upper beach zones or in the is at the core of the sandy beach food web, linking primary production by e.g. microalgae to nearshore, thus increasing coastal sediment budgets and widening the beach (Cooke et al. higher trophic levels such as shore birds (Lercari et al. 2010, Bergamino et al. 2011). It thereby 2012). Although sand nourishment has been considered as an ecologically friendly alternative also connects marine and terrestrial food webs and promotes the flow of nutrients across the to hard coastal defence structures (Hanley et al. 2014), it generally causes temporal local coastal boundary (Polis and Hurd 1996, Catenazzi and Donnelly 2007). It is, however, unknown extinction of sandy beach flora and fauna (Speybroeck et al. 2006, Leewis et al. 2012). During what the spatiotemporal effects of a mega-nourishment are on the intertidal regular beach nourishment, a thick layer of sand (up to a few meters) is deposited on the

Mega-nourishment creates novel habitat 33

34 Chapter 2 macroinvertebrate community and, ultimately, whether a mega-nourishment can be sand. These transects are further referred to as the transects at the hook. In 2012, a transect considered a promising coastal defence strategy in terms of sandy beach ecology. was positioned in the lagoon of the mega-nourishment and in 2013 a second transect was added to the lagoon, resulting in two transects at the lagoon that were sampled in 2013, 2014 In this study, we aimed to assess 1) the spatial and temporal effects within a mega- and 2015. Moreover, from 2013 onwards, one transect was added south and the most nourishment on the intertidal macroinvertebrate community up to four years after northern of the four initial southern transects was dropped. This was done to track the effect establishment, and 2) whether the intertidal macroinvertebrate community of wave-exposed of more sand moving southwards than was anticipated. To create a robust design, despite the beaches of mega-nourishments differs from those with regular beach nourishments or changes made while accounting for expected differences in the intertidal macroinvertebrate without nourishment. We hypothesised that 1) the most common intertidal community across the mega-nourishment, the beach was divided into four locations for macroinvertebrate species are present at the mega-nourishment within one year after analysis: North (four (or three) transects), South (four (or five) transects), Hook (four establishment; 2) enhanced habitat relief within the mega-nourishment will attract other transects) and Lagoon (two transects) (Figure 2.1). macroinvertebrate species than those encountered on wave-exposed sandy beaches alone, thus locally enhancing species richness; 3) the wave-exposed locations at the mega- With receding tide starting at the HWL, every 75 minutes one sample was taken around the nourishment will have a similar macroinvertebrate community composition as those subject water line with the last sample taken at the LWL, ensuring that sediment moisture levels were to regular beach nourishment, and 4) beaches subject to no nourishment are expected to have similar for each sample. This resulted in a total of five sampled zones per transect for the a community composition most dissimilar from the mega-nourishment and beaches subject intertidal region. With a GPS tracking device, the transects as established in 2012 were located to regular beach nourishment. each year to standardise transects over time. As the shape of the mega-nourishment changed over time, corresponding samples were taken at slightly different positions each year. Each 2.3 Methods sample was taken with a steel rectangular corer of 27 by 37 cm (surface area 999 cm2) until a 2.3.1 Data collection and description depth of 15 cm. Sediment was sieved and upon collection macroinvertebrates were transferred to a 4% formalin solution and later stored in 70% ethanol. Abundance and richness Our focus was on the macroinvertebrate community, which comprises all sandy beach were determined for each of the five zones separately within each mega-nourishment invertebrates that are obtained by sieving sand over a 1 mm mesh. Unnourished beaches were location, treating all transects within a location as replicates. We thus assumed that variation considered those that had not received any nourishment from the year 1990 onwards, when in the intertidal macroinvertebrate community between zones is greater than between sand nourishment became an active management strategy in the Netherlands (van Dalfsen adjacent transects within a mega-nourishment location (c.f. Schlacher et al. 2008). and Aarninkhof 2009). In light of our study aims, we compiled and analysed data originating from three data sets. Macroinvertebrates were identified to species level where possible. 2.3.1.2 Data set 2; the Leewis data set

2.3.1.1 Data set 1; the Sand Motor experiment Leewis et al. (2012) collected data on the intertidal macroinvertebrate community at seventeen Dutch beaches in August 2007. Here, only the nine beaches (seven nourished and The Sand Motor mega-nourishment was created along the coast near Den Haag, the two unnourished) in the provinces North-Holland and South-Holland were used. We excluded Netherlands (52.05 N, 4.19 E) as a hook-shaped peninsula attached to the original coast line sites from the Wadden Sea (in the north of the Netherlands) and the Zeeland Delta (in the (Stive et al. 2013). Sand nourishment started in 2010 and was completed in 2011. Data on the south of the Netherlands), as these beaches were more dissimilar to the mega-nourishment intertidal macroinvertebrate community was collected in five years, 2010 (prior to for environmental conditions (e.g. tidal range and calcium and mud content). As the original establishment), 2012 (t=1), 2013 (t=2), 2014 (t=3) and 2015 (t=4), in September or October to study was designed as a chronosequence, the time since the last regular beach nourishment, reduce seasonal effects between years. Twelve transects were directed perpendicular to the ranged from 1 to 13 years and sampling occurred at a single moment in time. The intertidal coast and spanned from the high water line (HWL, 1 m above mean sea level) to the low water region was randomly sampled between HWL and directly below the mean tidal level. At each line (LWL, 0.6 m below mean sea level). Transect length varied according to the slope of the beach, over a 25 m wide beach part parallel to the coast, a total of twenty samples was taken beach at each transect. Four transects were positioned north (down-stream), south (up- using a stratified random design. Perpendicular to the coast, the beach between HWL and stream; both 1000 m between transects) and in the centre (800 m between transects) of the directly below the mean tidal level was divided into four zones, each spanning 1/8 of the tidal mega-nourishment (Figure 2.1). With this set-up, a full spatial range of impacts on the height. With receding water starting at HWL, five samples were randomly taken from each of macroinvertebrate communities adjacent to the mega-nourishment could be monitored. The four zones. Each sample was taken with a circular steel corer with a diameter of 20 cm (surface sampling points on the central transects were, after placement of the mega-nourishment, re- area 314 cm2) and depth of 20 cm. Macroinvertebrates were collected by sieving sediment positioned on the outside of the hook as the original sampling points were now covered by and animals were stored in 10% formalin.

Mega-nourishment creates novel habitat 35 macroinvertebrate community and, ultimately, whether a mega-nourishment can be sand. These transects are further referred to as the transects at the hook. In 2012, a transect considered a promising coastal defence strategy in terms of sandy beach ecology. was positioned in the lagoon of the mega-nourishment and in 2013 a second transect was added to the lagoon, resulting in two transects at the lagoon that were sampled in 2013, 2014 In this study, we aimed to assess 1) the spatial and temporal effects within a mega- and 2015. Moreover, from 2013 onwards, one transect was added south and the most nourishment on the intertidal macroinvertebrate community up to four years after northern of the four initial southern transects was dropped. This was done to track the effect establishment, and 2) whether the intertidal macroinvertebrate community of wave-exposed of more sand moving southwards than was anticipated. To create a robust design, despite the beaches of mega-nourishments differs from those with regular beach nourishments or changes made while accounting for expected differences in the intertidal macroinvertebrate without nourishment. We hypothesised that 1) the most common intertidal community across the mega-nourishment, the beach was divided into four locations for macroinvertebrate species are present at the mega-nourishment within one year after analysis: North (four (or three) transects), South (four (or five) transects), Hook (four establishment; 2) enhanced habitat relief within the mega-nourishment will attract other transects) and Lagoon (two transects) (Figure 2.1). macroinvertebrate species than those encountered on wave-exposed sandy beaches alone, thus locally enhancing species richness; 3) the wave-exposed locations at the mega- With receding tide starting at the HWL, every 75 minutes one sample was taken around the nourishment will have a similar macroinvertebrate community composition as those subject water line with the last sample taken at the LWL, ensuring that sediment moisture levels were to regular beach nourishment, and 4) beaches subject to no nourishment are expected to have similar for each sample. This resulted in a total of five sampled zones per transect for the a community composition most dissimilar from the mega-nourishment and beaches subject intertidal region. With a GPS tracking device, the transects as established in 2012 were located to regular beach nourishment. each year to standardise transects over time. As the shape of the mega-nourishment changed over time, corresponding samples were taken at slightly different positions each year. Each 2.3 Methods sample was taken with a steel rectangular corer of 27 by 37 cm (surface area 999 cm2) until a 2.3.1 Data collection and description depth of 15 cm. Sediment was sieved and upon collection macroinvertebrates were transferred to a 4% formalin solution and later stored in 70% ethanol. Abundance and richness Our focus was on the macroinvertebrate community, which comprises all sandy beach were determined for each of the five zones separately within each mega-nourishment invertebrates that are obtained by sieving sand over a 1 mm mesh. Unnourished beaches were location, treating all transects within a location as replicates. We thus assumed that variation considered those that had not received any nourishment from the year 1990 onwards, when in the intertidal macroinvertebrate community between zones is greater than between sand nourishment became an active management strategy in the Netherlands (van Dalfsen adjacent transects within a mega-nourishment location (c.f. Schlacher et al. 2008). and Aarninkhof 2009). In light of our study aims, we compiled and analysed data originating from three data sets. Macroinvertebrates were identified to species level where possible. 2.3.1.2 Data set 2; the Leewis data set

36 Chapter 2

2.3.2 Combining and preparing data

2.3.2.1 General considerations

Abundance data was standardised by calculating the macroinvertebrate abundance per m2 for each sample based on the sample surface area. Richness was determined per zone and location (i.e. North, South, Hook or Lagoon) within the mega-nourishment or for each separate regularly nourished or unnourished beach. This amounted to an area sampled of 0.4 m2 (0.2 m2 for Lagoon) (data set 1), 0.16 m2 (data set 2) and 0.08 m2 (data set 3). A difference in sampling area makes it difficult to directly compare richness, but further correction was not possible because the species-area relationship was not known. Richness in data set 3, and to a lesser extent data set 2, may therefore to a certain degree be an underestimation of actual richness. Only taxa that were representative of the intertidal macroinvertebrate community were included in the analysis. Macroinvertebrates belonging to the class Insecta were removed, because these are short-term visitors from the supratidal and the dunes (Defeo and McLachlan 2013). In addition, the amphipod Talitrus saltator (two observations) and animals that could not be further identified in the order Amphipoda (two observations) were removed as these are considered to be supratidal inhabitants. Finally, three taxa (Schistomysis kervillei (Mysidae), Actiniaria and Hydrozoa) were removed as they were likely washed ashore after a storm.

2.3.2.2 Spatial and temporal effects within a mega-nourishment

location to obtain total abundance, which was log10(n+1)-transformed. The number of taxa was counted per zone and location within each year to determine richness. For multivariate analysis within the mega-nourishment, 73 taxa were included.

2.3.2.3 Mega-nourishment versus beach- and no nourishment

To compare the intertidal macroinvertebrate community across nourishment types, the zone from which the sample was taken was standardised between HWL (1) and LWL (0), where all sampling locations were placed in between 0 and 1 based on emersion time during the tidal cycle. An intertidal position of 0.5 thus corresponds with being emersed for half of the time. Furthermore, in the comparison of nourishment types, the focus is on the intertidal macroinvertebrate community of the wave-exposed beaches, therefore excluding the lagoon at the mega-nourishment as it is sheltered from hydrodynamic forces. In addition, the data collected at the mega-nourishment in 2010 was not included as sampling occurred prior to establishing the mega-nourishment. As a result of this selection, a total of 66 taxa were included in the multivariate analysis. For both data set 2 and 3, abundance and richness were calculated in analogy to the procedure applied to data set 1.

Mega-nourishment creates novel habitat 37

2.3.2 Combining and preparing data

2.3.2.1 General considerations

2.3.2.2 Spatial and temporal effects within a mega-nourishment

To analyse spatial and temporal effects of a mega-nourishment on community composition, we further processed the data from data set 1. First, the average abundance per taxon was calculated per zone and location. Abundance was then summed over all taxa per zone and location to obtain total abundance, which was log10(n+1)-transformed. The number of taxa was counted per zone and location within each year to determine richness. For multivariate analysis within the mega-nourishment, 73 taxa were included.

2.3.2.3 Mega-nourishment versus beach- and no nourishment

38 Chapter 2

2.3.3 Statistical analysis 2.4 Results

Of all potentially important abiotic factors explaining macroinvertebrate community 2.4.1 Spatial and temporal effects on the macroinvertebrate community within a mega- composition, we only had data available for median grain size for all data points, except for nourishment the mega-nourishment in 2014. When including median grain size in the analysis, median grain 2.4.1.1 Abundance and species richness size alone did not have a significant effect on macroinvertebrate abundance and richness, even though there were differences in median grain size between locations and years at the Macroinvertebrate abundance varied significantly with intertidal position within the mega- mega-nourishment and between nourishment types (see Appendix). This supports the nourishment (F=5.3, df=2.6, p=0.006) with a more than four times higher abundance close to recommendation to analyse the full suite of abiotic factors, but minimally include median LWL (78 ± 5 against 13 ± 12 individuals m-2 at LWL and HWL, respectively; Figure 2.2). Overall grain size, beach slope and tidal range (McLachlan and Brown 2006, Schlacher et al. 2008). As variation in abundance was large, ranging from 0 to 1580 individuals m-2. South of the mega- this was not possible, we treat nourishment and year as factors instead to include all relevant nourishment, macroinvertebrate abundance was significantly higher compared to the other abiotic factors in the analysis. locations (t=3.7, p<0.001). In 2014, macroinvertebrate abundance was significantly lower than in any other year (t=-3.6, p<0.001). In light of the unbalanced number of replications, we ran a GAM to test the effect of intertidal position (continuous factor, fitted with a polynomial spline (k=5)) and mega-nourishment Macroinvertebrate species richness also varied significantly with intertidal position (F=13.1, location (discontinuous factor, four locations) on intertidal macroinvertebrate abundance and df=1, p<0.001) with a higher species richness close to LWL (5.9 ± 4.1 against 2.9 ± 3.5 species richness. Another GAM was used to determine the effect of intertidal position (continuous on average at zone LWL and HWL, respectively, Figure 2.3). South of the mega-nourishment, factor, fitted with a polynomial spline (k=5)) and year (discontinuous factor, five years) on species richness was significantly higher compared to the other mega-nourishment locations intertidal macroinvertebrate abundance and richness over the five-year period prior and post (t=3.4, p=0.001). There was strong variation in species richness among years with higher application of the mega-nourishment. Macroinvertebrate community composition at the richness in 2012, 2013 and 2015 than in 2010 and 2014 (GAM, t=2.6, p=0.01; t=2.8, p=0.007; mega-nourishment was evaluated with NMDS ordination which was run for 100 iterations at t=3.5, p<0.001, respectively). k=3 (decreased number of dimensions). Similarities of macroinvertebrate communities 2.4.1.2 Community composition between groups, either location (four levels) or year (five levels), were tested with ANOSIM. For this analysis of similarities, the null-hypothesis is that the similarity between groups is The macroinvertebrate communities North and at the Hook of the mega-nourishment were greater than or equal to the similarity within groups, and the test statistic R is constrained most similar (Figure 2.4). South of the mega-nourishment, the beach harboured a more between -1 and 1 (Clarke 1993). dissimilar macroinvertebrate community composition compared to locations North and at the Hook, with no overlap in group means (Figure 2.4A). The most distinct macroinvertebrate We also ran a GAM to test the effect of intertidal position (continuous factor, fitted with a community was found in the lagoon, with no overlap in group means and a larger variation in polynomial spline (k=5)) and nourishment type (discontinuous factor; mega-nourishment, community composition than for any other location at the mega-nourishment (Figure 2.4A). regular beach nourishment and unnourished beaches) on macroinvertebrate abundance and These differences in macroinvertebrate community composition between locations were richness. Macroinvertebrate community composition for each nourishment type was plotted significant (R=0.31, p<0.001), despite an overlap in community composition for individual with NMDS ordination which was run for 100 iterations at k=3 (decreased number of sampling points at the mega-nourishment (Figure 2.4A). There were significant differences in dimensions). Similarities of macroinvertebrate communities between nourishment types macroinvertebrate community composition and variation between years (R=0.08, p<0.001). were again tested with ANOSIM. As data set 2 was focused on the higher intertidal position In 2010, the macroinvertebrate community composition was least variable and showed an underestimation of the lower position community may exist, however, this overlap in group means with all the other years (Figure 2.4B). The macroinvertebrate underestimation is divided over both beaches subject to regular beach nourishment and no community composition showed the largest variability in 2012, followed by 2013 (Figure 2.4B). nourishment. All statistical analyses were done in R, version 3.2.3 (R Core Team 2015). Two main clusters of taxa were identified, with species of exposed sandy beaches, such as the

polychaete worm Scolelepis squamata, the amphipods Bathyporeia pilosa and Haustorius arenarius and the isopod Eurydice pulchra at the core of one cluster (Figure 2.5, left) and typical mudflat species, such as the amphipod Corophium volutator and the polychaete worm

Heteromastus filiformis at the core of the other cluster (Figure 2.5, right). This coincides with

Mega-nourishment creates novel habitat 39

2.3.3 Statistical analysis 2.4 Results

Heteromastus filiformis at the core of the other cluster (Figure 2.5, right). This coincides with

40 Chapter 2

A A

B B

Figure 2.2 Macroinvertebrate abundance (log-transformed; individuals m-2) at the mega-nourishment Figure 2.3 Macroinvertebrate species richness at a mega-nourishment across the intertidal region across the intertidal region grouped by A) location (North, Hook, South and Lagoon) and B) year (2010, grouped by A) location (North, Hook, South and Lagoon) and B) year (2010, 2012, 2013, 2014 and 2012, 2013, 2014 and 2015). The continuous variable ‘intertidal position’ ranges from 0 being equal to 2015). The continuous variable ‘’intertidal position’’ ranges from 0 being equal to the low water line the low water line (LWL) to 1 being equal to the high water line (HWL). Each dot represents the average (LWL) to 1 being equal to the high water line (HWL). Each dot represents the sum of all taxa within a of all transects within a location, grouped per year. Grey solid line shows the GAM estimate for the location, grouped per year. Grey solid lines show the GAM estimate for the overall fit, with grey dashed overall fit, with grey dashed lines indicating the 95% confidence interval. Spline: k = 5. lines indicating the 95% confidence interval. Spline: k = 5.

Mega-nourishment creates novel habitat 41

A A

B B

42 Chapter 2 the community clusters North, South and at the Hook of the mega-nourishment as wave- 2.4.2 Effect of nourishment type on the macroinvertebrate community exposed sandy beaches and the Lagoon as a sheltered beach (see Figure 2.4A). 2.4.2.1 Abundance and species richness

Macroinvertebrate abundance was similar between beaches subject to regular nourishment A and no nourishment (t=-0.7, p=0.5), while abundance was significantly lower at the mega- nourishment (t=-5.4, p<0.001; Figure 2.6A). Overall, macroinvertebrate abundance varied

significantly with intertidal position (F=8.9, df=3.1, p<0.001), with higher abundances in the mid and low intertidal positions (120 ± 5 against 25 ± 8 individuals m-2 at LWL and HWL, respectively; Figure 2.6A).

Macroinvertebrate species richness was significantly lower at the unnourished beaches than

at beaches subject to regular nourishment and the mega-nourishment (F=3.5, df=2, p=0.03). Macroinvertebrate species richness varied significantly with intertidal position (F=18.6, df=1, p<0.001), with a higher species richness close to the low water line (5.6 ± 3.5 against 3.0 ± 3.6

species at HWL, respectively, Figure 2.6B).

Figure 2.5 NMDS ordination of the intertidal macroinvertebrate community at all locations at the Figure 2.4 NMDS ordination of the intertidal macroinvertebrate community at all locations at the mega-nourishment indicating taxa by code names. For readability, 63% of all code names are plotted mega-nourishment grouped by A) location (North, Hook, South and Lagoon) and B) year (2010, 2012, due to the high number of taxa (see Appendix section 2.6.5 for a legend of code names of plotted taxa). 2013, 2014 and 2015). Group means are shown as centroids based on the average group rank and a Open dots indicate each individual taxon and crosses indicate each individual sample. Stress = 0.12, k 95% confidence interval. Points indicate the individual samples. Stress = 0.12, k = 3. = 3.

Mega-nourishment creates novel habitat 43 the community clusters North, South and at the Hook of the mega-nourishment as wave- 2.4.2 Effect of nourishment type on the macroinvertebrate community exposed sandy beaches and the Lagoon as a sheltered beach (see Figure 2.4A). 2.4.2.1 Abundance and species richness

Macroinvertebrate species richness was significantly lower at the unnourished beaches than

species at HWL, respectively, Figure 2.6B).

44 Chapter 2

A A

B B

Figure 2.6 Macroinvertebrate abundance (log-transformed) (A) and richness (B) across the intertidal region at three different nourishment types (Mega = mega-nourishment, Beach = regular beach nourishment and Unnourished = unnourished beaches). The continuous variable ‘intertidal position’ Figure 2.7 NMDS ordination of the intertidal macroinvertebrate community across three nourishment ranges from 0 being equal to the low water line (LWL) to 1 being equal to the high water line (HWL). types (Mega = mega-nourishment, Beach = regular beach nourishment and Unnourished = Each dot represents the average (abundance) or sum of taxa (richness) of all transects within a location unnourished beaches) showing group centroids (A) or indicating taxa (B). Group means are shown as (mega-nourishment) or beach (regular beach nourishment and no nourishment) at each position, centroids based on the average group rank and a 95% confidence interval. For both plots, stress = 0.13, grouped per year. Grey lines show the GAM estimate for the overall fit, while grey dashed lines indicate k = 3. Crosses, plusses and triangles indicate the individual samples assigned to each of the three the 95% confidence interval. Spline: k = 5. nourishment types. For readability, 88% of all code names are plotted due to the high number of taxa (see Appendix section 2.6.5 for a legend of code names of plotted taxa).

Mega-nourishment creates novel habitat 45

A A

B B

46 Chapter 2

2.4.2.1 Community composition related goals coinciding with the applied sand nourishment. Through its differences in shape, size and frequency of nourishing, a mega-nourishment changes the environment in a different The macroinvertebrate communities at beaches subjected to regular nourishment and no way compared to regular beach nourishments even though e.g. sediment characteristics are nourishment were most similar in composition with a high overlap in group means (Figure not intended to be fundamentally different. These differences result in an altered intertidal 2.7A). The community composition at the wave-exposed beach locations within the mega- macroinvertebrate community with potential cascading effects within the sandy beach food nourishment was most distinct with no overlap in group means with unnourished beaches and web. a slight overlap with beaches subject to regular beach nourishment (Figure 2.7A). The macroinvertebrate community composition and variation showed significant differences 2.5.1 Dispersal is not strongly limiting after a mega-nourishment between nourishment types (R=0.08, p=0.002). Unnourished beaches harboured the greatest As expected, intertidal macroinvertebrate species common for wave-exposed sandy beaches variation in community composition as indicated by a larger group centroid (Figure 2.7A). were already encountered one year after establishment of the mega-nourishment. These In unnourished beaches, the community composition was driven by the presence of common species included the polychaete worm S. squamata, the amphipods H. arenarius and carnivorous species, such as the crab Carcinus maenas (Figure 2.7B). Species that were shared B. pilosa and the isopod E. pulchra (Van Hoey et al. 2004). These findings are in accordance among the three nourishment types included the polychaete worm Scolelepis squamata and with Leewis et al. (2012). This rapid colonisation of the bare sand associated with the hook of the amphipod Haustorius arenarius (Figure 2.7B). At the mega-nourishment, the mega-nourishment was especially successfully executed by S. squamata which reached macroinvertebrate community composition was strongly related to the presence of the the highest abundance of all taxa encountered at the mega-nourishment (data not shown). In amphipod Bathyporeia elegans and members of the crab family Portunidae, but also by the the years following mega-nourishment, these common species were still present. These polychaete worm Spio martinensis (Figure 2.7B). findings show that common intertidal macroinvertebrates successfully colonised the mega- nourishment, emphasising their great dispersal ability (e.g. Speybroeck et al. 2007; Grantham 2.5 Discussion et al. 2003). We found that a mega-nourishment can locally enhance intertidal macroinvertebrate species When comparing years after nourishment, both intertidal macroinvertebrate abundance and richness by enhancing habitat relief through variations in sandy beach morphology at species richness were lower in 2014 compared to other post-nourishment years. It is not landscape level. In particular, a mega-nourishment provides a new beach habitat along the uncommon to find large differences in macroinvertebrate composition between individual main coast in the form of a sheltered lagoon, which was inhabited by a distinct intertidal years due to the highly dynamic environment of the sandy beach (Turner et al. 1995) for macroinvertebrate community that is commonly encountered on beach types with among example causing local changes in mud content and chlorophyll-a (Ysebaert and Herman 2002). others finer sands and a higher organic matter content (see McLachlan and Brown 2006, Also, there may be years in which the reproductive output of certain species is lower or when Beukema et al. 1999). In addition, intertidal macroinvertebrate species richness and mortality is higher, which is related to the relatively long life-span of certain species and abundance were higher south of the mega-nourishment compared to the other locations, discontinuous reproduction throughout the year (which is e.g. the case for S. squamata which may again be related to the shape of the mega-nourishment. (Speybroeck et al. 2007)). In the years after establishment, the intertidal macroinvertebrate Our study also shows that a mega-nourishment has both positive and negative effects on the community showed greater spatial variability in composition compared to the community intertidal macroinvertebrate community when compared to beaches subject to regular beach encountered before the mega-nourishment was applied. Although this can again be attributed or no nourishment. While macroinvertebrate species richness was higher at both the mega- to between-year differences, the further development of the lagoon over the years likely had nourishment and beaches subject to regular beach nourishment than at unnourished beaches, the greatest effect on the increased variability in intertidal macroinvertebrate community macroinvertebrate abundance was lower at the mega-nourishment. This suggests that composition. intertidal macroinvertebrate species are able to establish on these sandy beaches, but a 2.5.2 Spatial variation by design facilitates macroinvertebrate species variety of abiotic non-optimal habitat characteristics and/or biotic factors, such as post- settlement competition and predation, limit the abundance of these species (Todd 1998). Secondly, we hypothesised that the enhanced habitat relief in beach morphology within the Furthermore, the wave-exposed beaches of a mega-nourishment harboured a different mega-nourishment would result in a sheltered beach that attracts other macroinvertebrate intertidal macroinvertebrate community compared to the species composition encountered species than those commonly encountered on wave-exposed sandy beaches, which was on beaches subject to regular beach and no nourishment. A mega-nourishment thus does not indeed observed. A distinct intertidal macroinvertebrate community composition was result in a similar intertidal macroinvertebrate community as was found on unnourished encountered in the lagoon, which included the amphipod C. volutator and the polychaete beaches. Whether this should be regarded as a problem or not depends on the specific nature- worms H. filiformis, C. capitata and P. elegans, which are species commonly encountered on

Mega-nourishment creates novel habitat 47

48 Chapter 2 intertidal mudflats (Beukema et al. 1999). The species P. elegans and H. filiformis are and no nourishment, which is in contrast to our third hypothesis. Directly after construction characteristic for intermediate and late successional stages of mudflats, respectively (Van of the mega-nourishment, the average median grain size was only slightly higher than at the Colen et al. 2008), indicating that assembly of a mudflat macroinvertebrate community original beach before construction (Huisman et al. 2014), which was expected to facilitate occurred in the lagoon. Where dredged material is used for the creation of a mudflat, macroinvertebrate colonisation. However, the sediment at the mega-nourishment became colonisation by typical mudflat species (including C. volutator and C. capitata) occurs within a generally coarser over time (Huisman et al. 2014), which likely had an effect on year (Bolam and Whomersley 2005), which is in accordance to our study. The mega- macroinvertebrate community composition. In addition, a mega-nourishment may give rise nourishment therefore represents a connection between sandy beach ecology and tidal flat to a range of other environmental changes (i.e. variability in hydrodynamic forces, beach ecology. The presence of this intertidal macroinvertebrate community coincides with the slope) which influence the prevalence of certain intertidal macroinvertebrate species. The sediment composition of the lagoon which accumulates organic matter (Wijsman 2016), as taxa that drive the intertidal macroinvertebrate community composition at the mega- organic particles precipitate and benthic primary production prospers in this benign nourishment, such as B. elegans, Portunidae, S. martinensis and P. ciliata, were less common hydrodynamic environment (Hartwig 1978). This community type is rarely encountered along but still part of several transitional intertidal macroinvertebrate communities related to the the Dutch coast which is dominated by wave-exposed sandy beaches subject to high Eurydice pulchra - Scolelepis squamata community (Van Hoey et al. 2004). hydrodynamic forces. Mudflats are present in the upper north (the Wadden sea) and the As to our final hypothesis, unnourished beaches did have the most dissimilar lower south (the Zeeland delta) of the Netherlands. The mega-nourishment thus locally gives macroinvertebrate community composition as compared to beaches subject to sand rise to a habitat that attracts a different intertidal macroinvertebrate community. nourishment practices. The intertidal macroinvertebrate communities can further develop in

the largely undisturbed unnourished beaches. For example, intertidal macroinvertebrate Interestingly, both macroinvertebrate abundance and richness were higher south of the communities at beaches that received no nourishment included the carnivorous crab species mega-nourishment compared to the other locations within the mega-nourishment. This C. maenas. These are attracted to beaches where sufficient prey species, consisting of primary finding may be related to the sea currents that move from south to north along this part of consumers, are present (Wong and Dowd 2013). Also, these beaches did not receive any sand the Dutch coast and hence influence migration patterns of intertidal macroinvertebrate nourishment because they are non-erosive. Unnourished beaches are therefore expected to species. Many intertidal macroinvertebrate species have a planktonic period in their life cycle have a lower temporal variability in beach slope and mean grain size, which may have affected and depend on hydrodynamic forces for dispersal to establish on new beaches, either in their the macroinvertebrate community composition (Brazeiro 2001). Nevertheless, there may be planktonic phase or as an adult (Grantham et al. 2003). As a result, the base of the sand hook many underlying and interrelated factors causing these differences in community patterns potentially acts as a sink for migrating intertidal macroinvertebrate species, which may lead which will be difficult to quantify in future studies. to an accumulation of a high number of macroinvertebrates but also of more species. Moreover, the environmental conditions differ, e.g. in sediment characteristics and variation Furthermore, intertidal macroinvertebrate abundance was lower at the mega-nourishment in dry and wet beach (micro-habitats), and may explain the higher intertidal compared to beaches subject to regular and no nourishment, which potentially has cascading macroinvertebrate abundance and richness south of the mega-nourishment. For example, effects on fish, crabs and shore birds that use these species as prey (McLachlan and Brown Huisman et al. (2014) found that at the outer hook of the mega-nourishment the sediment 2006). For example, birds have been shown to choose their foraging sites based on prey was 20 to 30% coarser compared to other parts of the mega-nourishment. Coarse sediment is density at the landscape scale along a sandy beach (Schlacher et al. 2014). These effects have known to be associated to low macroinvertebrate abundance and richness (Speybroeck et al. not been explored in the current set-up. Therefore, it remains unknown whether this has 2006). In addition, the beach south of the mega-nourishment could be more dissipative, which significant consequences for higher trophic levels when compared to other nourishment is associated with finer sands and a higher macroinvertebrate abundance and richness types. (McLachlan and Brown 2006). This suggests that intertidal macroinvertebrate colonisation of In our study, zonation patterns for intertidal macroinvertebrate abundance and richness were less common species may depend on suitable environmental conditions around the mega- similar across locations within a mega-nourishment and over a five-year period. Both the nourishment. mega-nourishment and the beaches subject to regular beach nourishment had similar

zonation patterns as unnourished beaches. Abundance and richness were higher close to the 2.5.3 Comparing the post-recovery intertidal macroinvertebrate community to other types of low water line with abundance being more variable, which is in accordance to conceptual nourishment models proposed by McLachlan and Brown (2006). This suggests that the zonation of the The intertidal macroinvertebrate community composition of wave-exposed beaches at the macroinvertebrate community regarding abundance and richness was not disproportionally mega-nourishment were to a small degree dissimilar from beaches subject to regular beach

Mega-nourishment creates novel habitat 49 intertidal mudflats (Beukema et al. 1999). The species P. elegans and H. filiformis are and no nourishment, which is in contrast to our third hypothesis. Directly after construction characteristic for intermediate and late successional stages of mudflats, respectively (Van of the mega-nourishment, the average median grain size was only slightly higher than at the Colen et al. 2008), indicating that assembly of a mudflat macroinvertebrate community original beach before construction (Huisman et al. 2014), which was expected to facilitate occurred in the lagoon. Where dredged material is used for the creation of a mudflat, macroinvertebrate colonisation. However, the sediment at the mega-nourishment became colonisation by typical mudflat species (including C. volutator and C. capitata) occurs within a generally coarser over time (Huisman et al. 2014), which likely had an effect on year (Bolam and Whomersley 2005), which is in accordance to our study. The mega- macroinvertebrate community composition. In addition, a mega-nourishment may give rise nourishment therefore represents a connection between sandy beach ecology and tidal flat to a range of other environmental changes (i.e. variability in hydrodynamic forces, beach ecology. The presence of this intertidal macroinvertebrate community coincides with the slope) which influence the prevalence of certain intertidal macroinvertebrate species. The sediment composition of the lagoon which accumulates organic matter (Wijsman 2016), as taxa that drive the intertidal macroinvertebrate community composition at the mega- organic particles precipitate and benthic primary production prospers in this benign nourishment, such as B. elegans, Portunidae, S. martinensis and P. ciliata, were less common hydrodynamic environment (Hartwig 1978). This community type is rarely encountered along but still part of several transitional intertidal macroinvertebrate communities related to the the Dutch coast which is dominated by wave-exposed sandy beaches subject to high Eurydice pulchra - Scolelepis squamata community (Van Hoey et al. 2004). hydrodynamic forces. Mudflats are present in the upper north (the Wadden sea) and the As to our final hypothesis, unnourished beaches did have the most dissimilar lower south (the Zeeland delta) of the Netherlands. The mega-nourishment thus locally gives macroinvertebrate community composition as compared to beaches subject to sand rise to a habitat that attracts a different intertidal macroinvertebrate community. nourishment practices. The intertidal macroinvertebrate communities can further develop in

50 Chapter 2 influenced by (different) environmental factors altering zonation patterns (Degraer et al. (Vanden Eede et al. 2014, Peterson et al. 2006). We recommend that further research includes 2003). the effects of changes in intertidal macroinvertebrate community composition on higher trophic levels to obtain a more complete overview on the ecological effects of sand It is finally important to note that we used three data sets with different experimental set-ups, nourishment practices. Finally, an in-depth analysis of the underlying abiotic and biotic factors which may have put constraints on the comparisons and interpretations we could make. For causing differences in the intertidal macroinvertebrate community between sand example, the intertidal macroinvertebrate community composition showed equal variability nourishment practices would yield critical information to facilitate future sand nourishment for the mega-nourishment at the wave-exposed locations as for beaches subject to regular designs. beach nourishment. Drawing a conclusion from this finding is, however, difficult as the variability in community composition is obtained from within one beach for the mega- 2.5.5 Conclusions nourishment (North, Hook, South and Lagoon) but several beaches for both regular and no The Sand Motor mega-nourishment was constructed as a long-term management alternative nourishment. The mega-nourishment data therefore probably display α-diversity, while the for coastal protection of sandy shores and is the first large-scale experiment of its kind. Local other beaches give an indication of β-diversity for the intertidal macroinvertebrate disturbance to ecological communities is reduced providing new, temporary habitat for nature community. Moreover, we needed to combine transects that were up to 1000 m apart at the development. We conclude that a mega-nourishment creates novel habitat for intertidal mega-nourishment to have replicate values within each location at the mega-nourishment, macroinvertebrates by enhancing habitat relief of the sandy beach. While coastal protection while sampling on all other beaches was concentrated on a much smaller beach part (25 m). is the primary goal in the management of most Dutch sandy shores, well designed mega- Finally, there was great variability in time of collection as samples were collected between nourishments seem to be a promising coastal defence strategy in terms of the 2002 and 2015. In addition, only at the mega-nourishment samples were collected as a small macroinvertebrate community of the intertidal sandy beach. time series, generating several data points for the same beach. Despite these limitations to our combined data set, we believe this study provides interesting and robust results on a novel sand nourishment strategy and its impact on the intertidal macroinvertebrate community compared to regular beach nourishments.

2.5.4 Implications for coastal management

We have shown that macroinvertebrate biodiversity can be temporally enhanced by creating a hook-shaped mega-nourishment. The shape is crucial, as it creates a lagoon sheltered from incoming waves, resulting in large-scale heterogeneity of the sandy beach morphology in terms of wave-exposure and accumulation of organic matter. Enhancing habitat relief attracts a wider variety of species and new communities can be assembled (Stein et al. 2014, Tamme et al. 2010). Although depending on the exact ecological goals of a sand nourishment to be implemented, biodiversity is a widely valued and easy to measure characteristic within coastal management which supports the sandy beach food web and gives rise to a variety of ecosystem functions, such as production and nutrient cycling (Schlacher et al. 2007). This suggests that a mega-nourishment may constitute an attractive design for creating diverse intertidal macroinvertebrate communities. Continuous monitoring of the development of the Sand Motor mega-nourishment and the intertidal macroinvertebrate community patterns over time will provide insight in the long-term dynamics. This is especially interesting as the mega-nourishment was designed to be completely incorporated with the original coast in twenty years (Stive et al. 2013), making the lagoon and its intertidal macroinvertebrate community a transient beach feature. On the other hand, intertidal macroinvertebrate abundance was overall lower at the mega-nourishment compared to beaches subject to regular beach and no nourishment. A lower intertidal macroinvertebrate abundance means a lower prey availability, with potentially cascading effects on the sandy beach food web

Mega-nourishment creates novel habitat 51 influenced by (different) environmental factors altering zonation patterns (Degraer et al. (Vanden Eede et al. 2014, Peterson et al. 2006). We recommend that further research includes 2003). the effects of changes in intertidal macroinvertebrate community composition on higher trophic levels to obtain a more complete overview on the ecological effects of sand It is finally important to note that we used three data sets with different experimental set-ups, nourishment practices. Finally, an in-depth analysis of the underlying abiotic and biotic factors which may have put constraints on the comparisons and interpretations we could make. For causing differences in the intertidal macroinvertebrate community between sand example, the intertidal macroinvertebrate community composition showed equal variability nourishment practices would yield critical information to facilitate future sand nourishment for the mega-nourishment at the wave-exposed locations as for beaches subject to regular designs. beach nourishment. Drawing a conclusion from this finding is, however, difficult as the variability in community composition is obtained from within one beach for the mega- 2.5.5 Conclusions nourishment (North, Hook, South and Lagoon) but several beaches for both regular and no The Sand Motor mega-nourishment was constructed as a long-term management alternative nourishment. The mega-nourishment data therefore probably display α-diversity, while the for coastal protection of sandy shores and is the first large-scale experiment of its kind. Local other beaches give an indication of β-diversity for the intertidal macroinvertebrate disturbance to ecological communities is reduced providing new, temporary habitat for nature community. Moreover, we needed to combine transects that were up to 1000 m apart at the development. We conclude that a mega-nourishment creates novel habitat for intertidal mega-nourishment to have replicate values within each location at the mega-nourishment, macroinvertebrates by enhancing habitat relief of the sandy beach. While coastal protection while sampling on all other beaches was concentrated on a much smaller beach part (25 m). is the primary goal in the management of most Dutch sandy shores, well designed mega- Finally, there was great variability in time of collection as samples were collected between nourishments seem to be a promising coastal defence strategy in terms of the 2002 and 2015. In addition, only at the mega-nourishment samples were collected as a small macroinvertebrate community of the intertidal sandy beach. time series, generating several data points for the same beach. Despite these limitations to our combined data set, we believe this study provides interesting and robust results on a novel sand nourishment strategy and its impact on the intertidal macroinvertebrate community compared to regular beach nourishments.

2.5.4 Implications for coastal management

52 Chapter 2

2.6 Appendix 2.6.2 Median grain size distribution between nourishment types 2.6.1 Median grain size distribution within a mega-nourishment There was a significant difference in median grain size between nourishment types (ANOVA, df=2, F=7.4, p<0.001) but not between intertidal positions (ANOVA, df=1, F=0.0, p=0.88) and Median grain size differed significantly between locations (ANOVA, df=3, F=13.9, p<0.001) but there was no significant interaction effect between nourishment type and intertidal position not between intertidal positions (ANOVA, df=1, F=0.3, p=0.62) and there was no significant (ANOVA, df=2, F=0.7, p=0.51) (Figure A2.2). interaction between location and intertidal position (ANOVA, df=3, F=1.2, p=0.31) (Figure A2.1). Median grain size differed significantly between years (ANOVA, df=3, F=4.6, p<0.01) but not between intertidal positions (ANOVA, df=1, F=0.2, p=0.67) and there was no significant interaction between location and intertidal position (ANOVA, df=3, F=0.37, p=0.78) (Figure A2.1).

Figure A2.2 Boxplots showing the median grain size between nourishment types (Mega = mega- nourishment, Beach = regular beach nourishment and Unnourished = beaches subject to no B nourishment) for separate intertidal positions. 2.6.3 Effect of median grain size on abundance and richness within a mega-nourishment Between locations at the mega-nourishment, there was no significant effect of median grain size on abundance (GAM, df=1, F=0.5, p=0.47), but there was a significant effect on richness

(GAM, df=1, F=7.6, p<0.01). Between years at the mega-nourishment, there was no significant effect of median grain size on either abundance (GAM, df=1, F=1.8, p=0.18) or richness (GAM, df=1, F=0.5, p=0.48).

When removing an outlier from the data, which had both the highest reported median grain

size (546) and the highest richness (top right in Figure A2.3), median grain size did not have any significant effect between locations on abundance (GAM, df=1, F=0.3, p=0.59) or richness (GAM, df=1, F=2.9, p=0.09), or between years on abundance (GAM, df=1, F=2.2, p=0.15) or

richness (GAM, df=1, F=3.9, p>0.05).

2.6.4 Effect of median grain size on abundance and richness between nourishment types Figure A2.1 Boxplots showing the median grain size between A) locations and B) years for separate intertidal positions at the Sand Motor mega-nourishment. Between nourishment types, there was no significant effect of median grain size on abundance (GAM, df=1, F=0.0, p=0.98) or richness (GAM, df=1, F=0.0, p=0.98).

Mega-nourishment creates novel habitat 53

When removing an outlier from the data, which had both the highest reported median grain

richness (GAM, df=1, F=3.9, p>0.05).

54 Chapter 2

Figure A2.3 Scatterplot between median grain size and richness. Symbols and colours indicate locations within the mega-nourishment. 2.6.5 Legend of code names for taxa plotted in the NMDS ordinations

Legend of code names of taxa plotted in Figure 2.5, in alphabetical order: Ali.suc = Alitta succinea, Ano.sp = Anoplodactylus sp., Bat.ele = Bathyporeia elegans, Bat.pel = Bathyporeia pelagica, Bat.pil = Bathyporeia pilosa, Cap.cap = Capitella capitata, Cap.sp = Capitella sp., Car = Cardiinae, Cha = Chaetognatha, Cor = Corophiidae, Cor.sp = Corophium sp., Cor.vol = Corophium volutator, Dio.pug = Diogenes pugilator, Ete = Eteoninae, Ete.sp = Eteone sp., Eur.pul = Eurydice pulchra, Gas.spi = Gastrosaccus spinifer, Gra.sp = Grania sp., Hau.are = Haustorius arenarius, Het.fil = Heteromastus filiformis, Jae.alb = Jaera albifrons, Lim.bal = Limecola balthica, Mar.vir = Marenzelleria viridis, Mon.ach = Monocorophium acherusicum, Mya.are = Mya arenaria, Myt.edu = Mytilus edulis, Nep.sp = Nepthys sp., Nep.cae = Nepthys caeca, Oli = Oligochaeta, Pal = Palaemonidae, Par.ful = Paraonis fulgens, Per.ulv = Peringia ulvae, Phy.muc = Phyllodoce mucosa, Pol = Polychaeta, Pol.cor = Polydora cornuta, Pol.cil = Polydora ciliata, Pon.alt = Pontocrates altamarinus, Por = Portunidae, Por.lat = Portumnus latipes, Pyg.ele = Pygospio elegans, Sca.sp = Scatella sp., Sco.squ = Scolelepis squamata, Sco.sp = Scolelepis sp., Spi.bom = Spiophanes bombyx, Spi.mar = Spio martinensis, Xan.ran = Xanthocanace ranula. In Figure 2.7, taxa names in addition to those mentioned for Figure 2.5 include, in alphabetical order: Ann = Annelida, Amp1 = Amphipoda nr. 1 (unidentified), Amp2 = Amphipoda nr. 2 (unidentified), Car.sp = Carcinus sp., Cra.cra = Crangon crangon, Dec = Decapoda, Ido.bal = Idotea baltica, Meg = Megalopa, Nep.cir = Nephtys cirrosa, Owe.fus = Owenia fusiformis, Pon.are = Pontocrates arenarius, Spi.sub = Spisula subtruncata.

Figure A2.3 Scatterplot between median grain size and richness. Symbols and colours indicate locations within the mega-nourishment. 2.6.5 Legend of code names for taxa plotted in the NMDS ordinations

Chapter 3 Chapter 3

Non-additive effects of consumption in an intertidal macroinvertebrate community are independent of food availability Non-additive effects of consumption in an intertidal macroinvertebrate community are independent of food availability but driven by complementarity effects but driven by complementarity effects

Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Matty P. Berg and Rien Aerts Matty P. Berg and Rien Aerts

This chapter has been published in: Ecology and Evolution This chapter has been published in: (2018), 8: 3086-3097 Ecology and Evolution doi: 10.1002/ece3.3841 (2018), 8: 3086-3097 doi: 10.1002/ece3.3841

Chapter 3 Chapter 3

58 Chapter 3

3.1 Abstract composition that cannot simply be explained by expectations based on the species’ monoculture responses (Chapin III et al. 2000; Loreau et al. 2001). For example, Cardinale et Suboptimal environmental conditions are ubiquitous in nature and commonly drive the outcome of biological interactions in community processes. Despite the importance of al. (2002) showed in a mesocosm experiment that by adding more caddisfly larvae species to biological interactions for community processes, knowledge on how species interactions are a community, facilitative interactions increased, leading to non-additive effects of resource affected by a limiting resource, for example, low food availability, remains limited. Here, we consumption (i.e. a positive net diversity effect). Two classes of non-additive effects can be tested whether variation in food supply causes non-additive consumption patterns, using the distinguished and may operate simultaneously: complementarity and selection effects (Tilman macroinvertebrate community of intertidal sandy beaches as a model system. We quantified et al. 1997, Huston 1997). Complementarity, selection and net diversity effects can each be isotopically labelled diatom consumption by three macroinvertebrate species (Bathyporeia either positive, negative or zero (Loreau and Hector 2001). A positive complementarity effect pilosa, Haustorius arenarius and Scolelepis squamata) kept in mesocosms in either is driven by niche-partitioning or facilitation (e.g. Spehn et al. 2005, Tilman et al. 2014), while monoculture or a three-species community at a range of diatom densities. Our results show a negative complementarity effect results from physical or chemical interference. The that B. pilosa was the most successful competitor in terms of consumption at both high and selection effect measures whether differences in species performance in community are non- low diatom density, while H. arenarius and especially S. squamata consumed less in a randomly related to the performance in monoculture (e.g. Polley et al. 2003). Thus, a positive community than in their respective monocultures. Non-additive effects of consumption in this selection effect occurs when a species with a high monoculture performance is dominant in macroinvertebrate community were present and larger than mere additive effects, and similar the community. Complementarity and selection effects together contribute to the net across diatom densities. The underlying species interactions, however, did change with diatom diversity effect. A positive net diversity effect indicates an increased performance of the density. Complementarity effects related to niche-partitioning were the main driver of the net community, based on the expectation of the monocultures, while a negative effect indicates diversity effect of consumption, with a slightly increasing contribution of selection effects the opposite. By allocating observed non-additive effects to these two classes, more insight is related to competition with decreasing diatom density. For the first time, we showed that gained in which species interactions are involved in, and to what extent they contribute to, a non-additive effects of consumption are independent of food availability in a macroinvertebrate community. This suggests that, in communities with functionally different, particular community process (Loreau and Hector 2001). By disentangling whether and thus complementary, species, non-additive effects can arise even when food availability complementarity or selection effects drive non-additive consumption in a community, is low. Hence, at a range of environmental conditions, species interactions hold an important predictions of the effect of changes in community composition on related ecosystem functions potential to alter ecosystem functioning. can be improved. This makes it a useful tool to assess differences in species interactions within a community under varying environmental conditions. 3.2 Introduction Laboratory studies of non-additive effects on community and ecosystem processes have Although community assembly is in part directly driven by environmental factors, biological traditionally been conducted under optimal conditions (e.g. Cardinale et al. 2002, Vos et al. interactions are a crucial driver of final community composition (Diamond 1975, Götzenberger 2013), with light, nutrients, temperature and other factors optimized to the needs of the et al. 2012, Valladares et al. 2015). Therefore, the full dynamics and consequences of biological species in the experiment. However, in nature, conditions are rarely optimal and species will interactions for communities as a whole should be considered, especially in the light of have to adapt to survive and maintain in a given community (Berg et al. 2010). Indeed, many environmental change. Changes in environmental conditions affect the interactions between studies have shown that environmental stress can significantly impact community and species, and hence final community composition (Tylianakis et al. 2008, Griffiths et al. 2015). ecosystem processes with a change in species diversity and concomitant changes in ecosystem When these species and their interactions are subjected to different environmental functioning (e.g. Mulder et al. 2001, Steudel et al. 2012). The impact of different conditions, a specific set of species is selected for, which results in a final community environmental conditions makes it difficult to predict how the outcome of species interactions composition which may differ between environmental conditions (Ozinga et al. 2005). As affects the community as a whole (Loreau 2000). For example, in a marine benthic food web, species composition affects community processes (such as consumption), and ultimately the presence of primary and/or secondary consumers led to a change in the trophic cascade, ecosystem processes (such as decomposition, primary production and nutrient cycling), which caused either a positive or negative effect on algal biomass depending on nutrient levels understanding the effects of species interactions on community and ecosystem-level being ambient or enriched (O’Conner and Donohue 2013). As optimal conditions are processes along an environmental gradient is key (Tilman et al. 1997). uncommon in nature, it is not sufficient to test the effect of non-additivity on community Functional differences between species are important determinants of the outcome of their processes purely under optimal conditions. So far, however, few studies have evaluated how species interactions, resulting in either coexistence or competitive exclusion of species within non-additive effects of consumption change under non-optimal environmental conditions a community (Chesson 2000, Valladares et al. 2015). Interactions among organisms may such as resource availability in a controlled setting. therefore often lead to non-additive effects of community processes, or effects of species

Non-additive effects of consumption 59

60 Chapter 3

In this study, we tested how diatom density as a limiting resource impacts community 3.3 Methods processes using the intertidal macroinvertebrate community of sandy beach ecosystems as a 3.3.1 Experimental design model system. We chose sandy beaches for three main reasons. First, the sandy beach food web is controlled primarily from the bottom-up and relies heavily on external resource inputs To investigate the effect of diatom density on consumption by the three macroinvertebrate in the form of organic matter (Schlacher and Hartwig 2013). The intertidal macroinvertebrate species both in monoculture and in community, we performed a mesocosm experiment in a community mainly consists of filter and deposit feeders, which depend on microalgae and fully-controlled climate room in which diatom density was manipulated. We used four diatom particulate organic matter (POM) in the water column which enter the beach at high tide or densities ranging from no diatoms to a high and ad libitum density of diatoms, where in level on benthic microalgae attached to sand grains (McLachlan and Brown 2006). Secondly, at the 0 no diatoms were added, in level 1 and 2 respectively 10% and 50% of the highest diatom sandy beach, food availability is temporally and spatially heterogeneous (Olabarria et al. density level were added and in level 3 100% of the highest density level was added. Diatoms 2007), e.g. due to variable hydrodynamic forces (Rosenberg 1995, Menge 2000). This suggests were offered as a four-species mixture to ensure a variety of diatoms were available in case that species will show responses to those different conditions. Finally, the intertidal zone at a the macroinvertebrates would have strong food preferences. Due to practical limitations we sandy beach harbours a macroinvertebrate community with a relatively low complexity, performed our climate-room experiment in two parts over time (two weeks in-between consisting of a limited number of species (Janssen and Mulder 2005). This allows us to parts), in which all conditions could be kept equal due to the strict environmental controls in assemble a simple but representative experimental community with results that can be more the climate room. In both parts, the climate chamber had a 12:12 h light/dark regime (light readily translated to natural field conditions. intensity: 250 ± 30 µmol m-2 s-1, lamp type: Philips Master HPI-T Plus spectral scheme 50) and a 12:12 h temperature cycle (20 °C during the day and 15 °C during the night), ensuring similar The aims of this study were to unravel 1) diatom consumption patterns in a macroinvertebrate environmental conditions. These conditions mimic spring/summer conditions in the community compared to consumption in species’ monocultures upon variation in diatom Netherlands. density supply and 2) if observed differences in diatom consumption at different diatom densities resulted from selection or complementarity effects. To this end, we performed an The first experimental part (60 mesocosms in total) contained only monocultures of each experiment with isotopically labelled diatoms that were fed to a community, assembled with macroinvertebrate species to determine diatom consumption at four diatom density levels in three macroinvertebrate species commonly found in high abundances within the intertidal the absence of other macroinvertebrate species (Table 3.1). The second experimental part (35 community of Dutch beaches (Janssen and Mulder 2005, Leewis et al. 2012): Bathyporeia mesocosms in total) mainly contained communities, consisting of the combination of the pilosa and Haustorius arenarius (both amphipods) and Scolelepis squamata (a polychaete three species together, to investigate the effect of diatom density on consumption (Table 3.1). For this purpose, 20 out of these 35 mesocosms contained communities at four diatom density worm). These species are sand-dwelling filter and deposit feeders, but differ slightly in feeding levels. The remaining 15 mesocosms acted as a control. In both experimental parts, there were strategy making them functionally distinct. Haustorius arenarius and S. squamata collect any five replicates for each treatment combination. To confirm there were no differences in floating particles of organic matter in the water column (Dennell 1933, Dauer 1983), while B. macroinvertebrate survival or diatom consumption between both experimental parts (e.g. pilosa mainly scrapes organic material from sand grains (Nicolaisen and Kanneworff 1969). We due to potential differences in environmental conditions or field collection of focused on three-species combinations to understand how a simple community of macroinvertebrates), we included monocultures with the highest diatom density level as a macroinvertebrates would respond to changes in food availability as compared to individual control in the second part. We only duplicated the highest diatom density level to ensure species’ monocultures. We expected that at high diatom density, interspecific interactions in survival and consumption were not affected or limited by a low food availability when the macroinvertebrate community would alter consumption compared to the species’ including lower diatom densities than ad libitum. There were no significant differences in monocultures, because they use the same pool of food (diatoms) and partially overlap in either survival or diatom consumption per mesocosm for macroinvertebrate monocultures at feeding strategy. More specifically, we expected that the individual macroinvertebrate species the highest diatom density level between both parts (Wilcoxon rank-sum test, W=84.5, in monoculture would consume a different amount of diatoms when compared with their p=0.22; and W=160, p>0.05, respectively), indicating animal survival and diatom consumption consumption in a community. Further, we hypothesised that if environmental conditions did not depend on the experimental part itself. This allowed us to take both experimental become harsher (when less food in the form of diatoms is available), intertidal parts together and create one combined dataset for further analysis. Each experimental part macroinvertebrate species with a lower competitive ability would consume less in community lasted seven days. This time period is sufficient to study short term consumption dynamics compared to that species’ monoculture. As a consequence, selection effects should increase between these species, as related to the aim of this study. Mesocosms were constructed of a as diatom density decreases. We expected that positive non-additive effects would occur in 30 cm high PVC tube with a diameter of 11.8 cm, with the lower side closed with a sheet of PVC. A sediment column was constructed in each mesocosm consisting of a layer of 15 cm our study system, mainly due to niche-partitioning between the three macroinvertebrate inert quartz sand (median grain size: 280 µm), followed by a column of 10 cm of artificial species, promoting co-existence.

Non-additive effects of consumption 61

62 Chapter 3

Table 3.1 Summary of the experimental design indicating the mesocosms included in each Table 3.2 Summary of characteristics for the four diatom species used in diatom mixtures, including experimental part. B = B. pilosa, H = H. arenarius and S = S. squamata. life stage, cell size (average ± standard deviation) and isotopic enrichment for both 13C and 15N (average ± standard deviation). Not for each species a duplicate sample could be taken for δ15N analysis in each Experimental part Monoculture or Community Species Diatom density n Total n experimental part, therefore lacking a standard deviation. Symbols indicate the following: # Scholz and 1 Monoculture B 0% 5 Liebezeit (2012); $ average of four species, Scholz and Liebezeit (2012); % average of two strains, 10% 5 Balzano et al. (2011), * Laws et al. (2013). 50% 5 Experimental part 1 Experimental part 2 100% 5 Cell size as H 0% 5 δ13C δ15N δ13C δ15N 10% 5 Species Life stage length x width 50% 5 (‰) (‰) (‰) (‰) (µm) 100% 5 S 0% 5 Navicula Benthic 15.6 ± 4.9 6123 ± 19 2888 ± 6 6786 ± 71 3497 perminuta x 2.8 ± 1.6 10% 5 # 50% 5 Amphora sp. Benthic 76.5 x 17.1 4769 ± 49 3087 ± 11 8000 ± 283 3689 100% 5 $ 60 Skeletonema Planktonic 9.6 x 8.75 9344 ± 127 3075 9483 ± 111 3353 2 Community BHS 0% 5 costatum % Thalassiosira sp. Planktonic 21 x 17 6273 ± 123 2927 ± 25 6395 ± 89 3847 ± 3 10% 5 * 50% 5 100% 5 North Sea (Rousseau et al. 2002, Ehrenhauss et al. 2004, Scholz and Liebezeit 2012). Diatom Monoculture B 100% 5 cultures were started based upon 20 mL diatom strains within seven days upon arrival of these H 100% 5 strains in separate 500 mL glass flasks and placed in a climate chamber under optimal S 100% 5 conditions. These diatom cultures were tended for approximately six months until the start of 35 the experiment to have sufficient diatom culture (2.5-3 L per diatom species in total) available

to perform the experiment. Every four to five weeks, each diatom culture was sub cultured sea water (30‰ salt content; Instant Ocean, Aquarium Systems, Inc., Mentor, OH, USA) and, with fresh L1-medium based on artificial sea water (30‰ salt content) by adding culture to finally, a 5 cm column of air. During the experiment, all mesocosms were aerated with medium in a ratio of 1:10 based on volume (medium protocol obtained from SCCAP). compressed air via an aeration stone and loosely covered at the top with cling film to limit 13 15 water evaporation but allowing air exchange (see Figure A3.1). This mesocosm set-up mimics Diatoms were labelled with the stable isotopes C and N to track consumption by the 13 13 the intertidal beach at high tide, which is when the macroinvertebrate species actively forage macroinvertebrate species. For C enrichment, an average of 0.06 g NaH CO3 (98% enriched) on the inundated sand surface and in the water column. In each experimental part, treatments was added as stock solution per L diatom culture in the last four months prior to the 13 were randomly distributed over the mesocosms and randomly allocated within the climate experiment in regular intervals. After each C addition, culture flasks were closed, gently chamber. shaken and left for 4-5 hours to incubate. Flasks were then taken to another room and the air within the flasks was flushed with compressed air for 15 minutes to remove surplus 13C. For 3.3.2 Diatom cultures and stable isotope labelling 15 -1 N diatom enrichment, 0.049 g 100 mL of the N-source in the regular L1-medium, NaNO3 -1 15 15 13 15 Four diatom species covering a range in cell size and life stage (Table 3.2) were used in the (7.5 g 100 mL ), was replaced by NH4 NO3 (98% enriched). Final C and N diatom diatom mixture to account for potential feeding preferences of the macroinvertebrates: enrichment differed between diatom species and both experimental parts (Table 3.2). For 13 15 Navicula perminuta (strain CCAP 1050/15) obtained from the Culture Collection of Algae and further calculations based on C and N diatom enrichment, the average of the four diatom Protozoa (CCAP, Scottish Marine Institute, United Kingdom), and Thalassiosira sp. (strain species was taken as we offered diatoms in mixture, with a separate value for each SCCAP K-1435), Amphora sp. (strain SCCAP K-1250) and Skeletonema costatum (strain SCCAP experimental part. K-0669) obtained from the Scandinavian Culture Collection of Algae and Protozoa (SCCAP, Upon diatom harvest, the culture medium was replaced by fresh artificial sea water to remove University of Copenhagen, Denmark). All four diatom species are commonly found in the non-incorporated stable isotopes. Biomass concentrations were determined by filtering a 50

Non-additive effects of consumption 63

64 Chapter 3 mL subsample over a 0.45 µm cellulose nitrate filter, oven-drying (72 hours at 40°C) and measured macroinvertebrate biomass at harvest was used in the calculations on diatom weighing the remaining diatoms. To prepare diatom mixtures, the volume needed from each consumption. diatom culture to obtain a 1:1:1:1 dry mass diatom species distribution was taken for each 3.3.4 Measurements mesocosm according to four diatom density levels. Four diatom density levels were offered to the macroinvertebrates, with the highest diatom density level considered to be ad libitum. In After seven days of incubation, all animals were harvested and survival was determined. level 0 no diatoms were added (50 mL artificial sea water was added as control) and was Animals were retrieved from the mesocosms at harvest and survival was on average 84% ± considered as a control for isotopic background levels in the macroinvertebrates, level 1 19% across all mesocosms, independent of treatment (data not shown). Animals were gently contained 10% of the highest diatom density level (0.0022 g diatoms 50 mL-1), level 2 dried with a tissue to remove adherent water and weighed for fresh biomass (to the nearest contained 50% of the highest diatom density level (0.011 g diatoms 50 mL-1) and level 3 μg), directly followed by killing the animals by moving them to a vial filled with liquid nitrogen contained 100% of the highest density level (0.022 g diatoms 50 mL-1). Level 3 corresponded and storing at -80 °C until further processing. All individuals per species from one mesocosm to two times the average macroinvertebrate biomass of diatoms added per mesocosm (0.010 were pooled together to have sufficient material for chemical analysis, freeze-dried for 48 h g animal ash free dry weight). All diatom mixtures were stored cool (5 °C) in the dark until the and ground to obtain a homogenised powder. Between 1.0 and 1.5 mg of each sample was 13 15 start of the experiment 48 hours later. weighed in a tin cup for dual ( C and N) stable isotope analysis. Stable isotope enrichment for both diatoms and animals is expressed as a δ value (Fry 2006). To determine the relative 3.3.3 Macroinvertebrate collection isotope enrichment of the samples, we used Vienna PeeDee Belemnite (VPDB) as the 13 15 Three common macroinvertebrate species from the Dutch intertidal beach (Leewis et al. 2012) international reference standard for C and nitrogen in the air for N (Fry 2006). The stable were used: Bathyporeia pilosa Lindström, 1855 (Amphipoda: Bathyporeiidae), Haustorius isotopes were measured using an elemental analyser (NC2500; ThermoQuest Italia, Rodana, arenarius Slabber, 1769 (Amphipoda: Haustoriidae) and Scolelepis squamata Müller, 1806 Italy) coupled with an isotope ratio mass spectrometer (Delta Plus; Thermo-Quest Finnigan, (Polychaeta: Spionidae). Scolelepis squamata and H. arenarius were collected at the beach Bremen, Germany). For calibration of natural isotope abundance samples, USGS 40 and USGS 13 15 near Bloemendaal aan Zee (52.42 N, 4.55 E), the Netherlands, and B. pilosa was collected from 41 were used. The reproducibility of the δ C and δ N analysis as determined by repeated the Paulinaschor near Terneuzen (51.35 N, 3.74 E), the Netherlands. A fresh batch of animals analysis of an internal standard (Bovine liver, NIST 1577c) was within 0.15 ‰ (n = 3). For 15 13 was collected in the field in May 2014, no more than 11 days before the start of each enriched samples, IAEA 305B, IAEA 311(δ N) and IAEA 309B (δ C) were used. experimental part, by sieving small quantities of hand-collected sand over a 1 mm-sieve and 13 15 To determine initial C and N enrichment in the diatoms, two 50 mL subsamples per species storing animals in pots containing natural sea water from the collection sites. Collected were taken and centrifuged at 1000 rpm for 10 minutes. Each sample was washed two times macroinvertebrates were kept alive in aquaria filled with a 15 cm layer of inert quartz sand with artificial sea water (30‰ salt content) to remove non-incorporated stable isotopes and artificial sea water in the climate chamber. Aquaria were aerated with air stones and present in the medium and dried in the oven (60°C for 72 h). Diatoms were ground to powder animals were kept under optimal conditions until the start of the experiment. Of the surviving and analysed for 13C and 15N with stable isotope analysis. To determine N and C animals that were collected in the field, healthy and active individuals were selected to be concentrations, powdered diatom samples were washed with demi water to remove salt and randomly divided over the macroinvertebrate treatments. Animals were starved for 24 hours then measured by dry combustion with a Flash EA1112 elemental analyser (Thermo Scientific, prior to the start of the experiment. Rodana, Italy).

Total macroinvertebrate biomass was kept equal at 0.010 g ash free dry weight in each 3.3.5 Analysis of diatom consumption mesocosm, which was based on macroinvertebrate community biomass as found on natural sandy beaches in the Netherlands (personal observation). By dividing by the average dry As a measure of diatom consumption, we used the stable isotope enrichment measured in the biomass per individual for each species (adapted from Degraer et al. 1999 and Speybroeck et macroinvertebrates. We determined the isotopic background for both δ13C and δ15N for each al. 2008b), the number of individuals per mesocosm was calculated. Densities used in the macroinvertebrate species in both monoculture and community at the end of the experiment experiment were within the natural range observed at Dutch sandy beaches (Leewis et al. from the individuals that had been subject to food level 0 (control), where diatoms were 2012). To obtain similar biomass in all treatments before the start of the experiment, absent and thus no isotopic enrichment (i.e. consumption) occurred. The use of species- macroinvertebrate monocultures consisted of nine animals for B. pilosa and H. arenarius and specific background δ13 C and δ15 N accounted for the potential effects of trophic fractionation seven animals for S. squamata, whereas the three-species communities consisted of three B. on stable isotope ratios. In further analysis, we omitted results for 0% diatom density. The pilosa individuals, three H. arenarius individuals and two S. squamata individuals. The difference in δ13C and δ15N between macroinvertebrates from the other diatom density treatments and the background δ13C and δ15N provided the assimilated δ13C and δ15N. In

Non-additive effects of consumption 65 mL subsample over a 0.45 µm cellulose nitrate filter, oven-drying (72 hours at 40°C) and measured macroinvertebrate biomass at harvest was used in the calculations on diatom weighing the remaining diatoms. To prepare diatom mixtures, the volume needed from each consumption. diatom culture to obtain a 1:1:1:1 dry mass diatom species distribution was taken for each 3.3.4 Measurements mesocosm according to four diatom density levels. Four diatom density levels were offered to the macroinvertebrates, with the highest diatom density level considered to be ad libitum. In After seven days of incubation, all animals were harvested and survival was determined. level 0 no diatoms were added (50 mL artificial sea water was added as control) and was Animals were retrieved from the mesocosms at harvest and survival was on average 84% ± considered as a control for isotopic background levels in the macroinvertebrates, level 1 19% across all mesocosms, independent of treatment (data not shown). Animals were gently contained 10% of the highest diatom density level (0.0022 g diatoms 50 mL-1), level 2 dried with a tissue to remove adherent water and weighed for fresh biomass (to the nearest contained 50% of the highest diatom density level (0.011 g diatoms 50 mL-1) and level 3 μg), directly followed by killing the animals by moving them to a vial filled with liquid nitrogen contained 100% of the highest density level (0.022 g diatoms 50 mL-1). Level 3 corresponded and storing at -80 °C until further processing. All individuals per species from one mesocosm to two times the average macroinvertebrate biomass of diatoms added per mesocosm (0.010 were pooled together to have sufficient material for chemical analysis, freeze-dried for 48 h g animal ash free dry weight). All diatom mixtures were stored cool (5 °C) in the dark until the and ground to obtain a homogenised powder. Between 1.0 and 1.5 mg of each sample was 13 15 start of the experiment 48 hours later. weighed in a tin cup for dual ( C and N) stable isotope analysis. Stable isotope enrichment for both diatoms and animals is expressed as a δ value (Fry 2006). To determine the relative 3.3.3 Macroinvertebrate collection isotope enrichment of the samples, we used Vienna PeeDee Belemnite (VPDB) as the 13 15 Three common macroinvertebrate species from the Dutch intertidal beach (Leewis et al. 2012) international reference standard for C and nitrogen in the air for N (Fry 2006). The stable were used: Bathyporeia pilosa Lindström, 1855 (Amphipoda: Bathyporeiidae), Haustorius isotopes were measured using an elemental analyser (NC2500; ThermoQuest Italia, Rodana, arenarius Slabber, 1769 (Amphipoda: Haustoriidae) and Scolelepis squamata Müller, 1806 Italy) coupled with an isotope ratio mass spectrometer (Delta Plus; Thermo-Quest Finnigan, (Polychaeta: Spionidae). Scolelepis squamata and H. arenarius were collected at the beach Bremen, Germany). For calibration of natural isotope abundance samples, USGS 40 and USGS 13 15 near Bloemendaal aan Zee (52.42 N, 4.55 E), the Netherlands, and B. pilosa was collected from 41 were used. The reproducibility of the δ C and δ N analysis as determined by repeated the Paulinaschor near Terneuzen (51.35 N, 3.74 E), the Netherlands. A fresh batch of animals analysis of an internal standard (Bovine liver, NIST 1577c) was within 0.15 ‰ (n = 3). For 15 13 was collected in the field in May 2014, no more than 11 days before the start of each enriched samples, IAEA 305B, IAEA 311(δ N) and IAEA 309B (δ C) were used. experimental part, by sieving small quantities of hand-collected sand over a 1 mm-sieve and 13 15 To determine initial C and N enrichment in the diatoms, two 50 mL subsamples per species storing animals in pots containing natural sea water from the collection sites. Collected were taken and centrifuged at 1000 rpm for 10 minutes. Each sample was washed two times macroinvertebrates were kept alive in aquaria filled with a 15 cm layer of inert quartz sand with artificial sea water (30‰ salt content) to remove non-incorporated stable isotopes and artificial sea water in the climate chamber. Aquaria were aerated with air stones and present in the medium and dried in the oven (60°C for 72 h). Diatoms were ground to powder animals were kept under optimal conditions until the start of the experiment. Of the surviving and analysed for 13C and 15N with stable isotope analysis. To determine N and C animals that were collected in the field, healthy and active individuals were selected to be concentrations, powdered diatom samples were washed with demi water to remove salt and randomly divided over the macroinvertebrate treatments. Animals were starved for 24 hours then measured by dry combustion with a Flash EA1112 elemental analyser (Thermo Scientific, prior to the start of the experiment. Rodana, Italy).

66 Chapter 3 combination with the average freeze-dry biomass per animal in the mesocosms at harvest, of 0.017. Differences in macroinvertebrate composition effect were analysed with a one-way the total assimilation of 13C and 15N was calculated (in mg individual-1). The amount of 13C and ANOVA for net diversity effect, complementarity effect and selection effect separately and 15N present on average in the diatoms (in mg mg diatom-1) was finally used to calculate what diatom density as a factor. ANOVAs were followed up with Tukey’s post hoc tests, which diatom mass the macroinvertebrates must have minimally consumed to reach their calculated correct for multiple comparisons. There was one outlier in the data; in one mesocosm 13C and 15N assimilation (in mg diatom mg animal-1). This was calculated by dividing the consumption was very high for B. pilosa in community at 50% diatom density, which could not amount of 13C and 15N in the animals (in mg animal-1) by the amount of 13C and 15N in the be rejected on any grounds. However, performing the same analyses for both consumption diatoms (in mg diatom-1) and finally correcting for the mass per individual (in mg animal-1) as and diversity effects without this outlier resulted in no changes in accepting or rejecting the diatom consumption. Differences in assimilation efficiency among species may have affected tested statistical hypotheses (results not shown). Prior to analysis, all data were tested for these estimates, but these differences are considered to be generally small (Vander Zanden homogeneity of variances and a normal distribution. If these assumptions were not met, a and Rasmussen 2001). The relatively short experiment does not allow for quantification of square root transformation was performed on the original data (for the three-way ANOVA, for stable isotope accumulation within the species’ tissue as full tissue turnover for these species the two-way ANOVAs at 10 and 50% food availability, for net diversity effect and for is expected to occur over a longer time period (see e.g. McLeod et al. 2013, Hentschel 1998). complementarity effect). P-values were considered to be significant at α = 0.05. All data were Instead, the experiment provided a snap shot of the isotopic dynamics within the animal body analysed with the statistical program R, version 3.1.2 (R Core Team 2015). between consumption, accumulation and excretion. Given that this was done for each species 3.4 Results after the same incubation period, we expect this to be of only minor influence on the interpretation of the results. 3.4.1 Overall effects of diatom consumption

3.3.6 Calculation of diversity effects Diatom consumption by the three macroinvertebrate species over the experimental period varied strongly (maximum consumption was 0.24, 0.14 and 0.10 mg diatom mg animal-1 for B. The net diversity effect of macroinvertebrate species on consumption was calculated by pilosa, S. squamata and H. arenarius, respectively) with diatom density and differed between subtracting the expected consumption in community from the observed consumption in the monocultures and communities (Figure 3.1). The overall analysis showed that diatom density, community at each level of diatom density, for each species separately. The expected diatom macroinvertebrate species and community composition all had significant effects on diatom consumption for a macroinvertebrate species in community was its consumption in consumption. Moreover, all two-way interactions and the three-way interaction were monoculture, adjusted for mass. Under the null hypothesis, the expected and observed significant (see three-way ANOVA results in Table 3.3). Below an in-depth analysis is given by diatom consumption are equal and no selection or complementarity effects occur. To identify separate comparisons for each level of diatom density. the extent to which deviations from this null hypothesis can be attributed to selection or 3.4.2 Diatom consumption at high diatom density complementarity effects, we used the equation provided by Loreau and Hector (2001). The net diversity effect (ΔY) was the sum of the complementarity effect ( ) and the Both macroinvertebrate species (two-way ANOVA, df=2, F=14.1, p<0.001) and community selection effect ( ), with N as the number of macroinvertebrate species in the composition (two-way ANOVA, df=1, F=10.6, p<0.01) had a significant effect on diatom 𝑁𝑁𝑁𝑁∆RY 𝑀𝑀𝑀𝑀 community, as the difference in relative observed and expected diatom consumption, consumption at high diatom density (Figure 3.1; Table 3.4). In addition, there was a significant 𝑁𝑁𝑁𝑁푁푁푁푁푁𝑁푁 M) and as observed diatom consumption in the monoculture. For we used the average of interaction effect between these factors, indicating that macroinvertebrate species consumed ΔRY all mesocosms for each species and food availability combination (n = 5), to have a differently in the monocultures and in the community (two-way ANOVA, df=2, F=17.1, 𝑀𝑀𝑀𝑀 𝑀𝑀𝑀𝑀 representative indicator of performance in the mesocosms. p<0.001). In the monocultures, S. squamata had the highest diatom consumption with 0.11 ± 0.02 mg diatom mg animal-1, followed by B. pilosa (0.058 ± 0.039 mg diatom mg animal-1; 3.3.7 Statistical analysis -1 Tukey’s post hoc, p=0.02) and H. arenarius (0.021 ± 0.018 mg diatom mg animal ; Tukey’s post We performed a three-way ANOVA to analyse the overall effect of macroinvertebrate species hoc, p<0.001), of which the last two had a similar diatom consumption (Tukey’s post hoc, (three levels), diatom density availability (three levels) and macroinvertebrate community p=0.16). Single species consumption changed when the three macroinvertebrate species were composition (two levels) on diatom consumption. To proceed, and to interpret the placed together in a community (Figure 3.1). The average diatom consumption of S. squamata -1 interactions found, we performed three separate two-way ANOVA (one for each diatom dropped sharply by 89% to 0.012 ± 0.008 mg diatom mg animal as compared to its density level) to test for the effects of macroinvertebrate species and macroinvertebrate monoculture (Tukey’s post hoc, p<0.001). In contrast, both H. arenarius and B. pilosa community composition on diatom consumption. For each of the two-way ANOVAs, p-values consumed a similar amount of diatoms in both the monoculture and community (Tukey’s post were corrected for multiple comparisons with the Bonferroni correction, resulting in a pcritical

Non-additive effects of consumption 67 combination with the average freeze-dry biomass per animal in the mesocosms at harvest, of 0.017. Differences in macroinvertebrate composition effect were analysed with a one-way the total assimilation of 13C and 15N was calculated (in mg individual-1). The amount of 13C and ANOVA for net diversity effect, complementarity effect and selection effect separately and 15N present on average in the diatoms (in mg mg diatom-1) was finally used to calculate what diatom density as a factor. ANOVAs were followed up with Tukey’s post hoc tests, which diatom mass the macroinvertebrates must have minimally consumed to reach their calculated correct for multiple comparisons. There was one outlier in the data; in one mesocosm 13C and 15N assimilation (in mg diatom mg animal-1). This was calculated by dividing the consumption was very high for B. pilosa in community at 50% diatom density, which could not amount of 13C and 15N in the animals (in mg animal-1) by the amount of 13C and 15N in the be rejected on any grounds. However, performing the same analyses for both consumption diatoms (in mg diatom-1) and finally correcting for the mass per individual (in mg animal-1) as and diversity effects without this outlier resulted in no changes in accepting or rejecting the diatom consumption. Differences in assimilation efficiency among species may have affected tested statistical hypotheses (results not shown). Prior to analysis, all data were tested for these estimates, but these differences are considered to be generally small (Vander Zanden homogeneity of variances and a normal distribution. If these assumptions were not met, a and Rasmussen 2001). The relatively short experiment does not allow for quantification of square root transformation was performed on the original data (for the three-way ANOVA, for stable isotope accumulation within the species’ tissue as full tissue turnover for these species the two-way ANOVAs at 10 and 50% food availability, for net diversity effect and for is expected to occur over a longer time period (see e.g. McLeod et al. 2013, Hentschel 1998). complementarity effect). P-values were considered to be significant at α = 0.05. All data were Instead, the experiment provided a snap shot of the isotopic dynamics within the animal body analysed with the statistical program R, version 3.1.2 (R Core Team 2015). between consumption, accumulation and excretion. Given that this was done for each species 3.4 Results after the same incubation period, we expect this to be of only minor influence on the interpretation of the results. 3.4.1 Overall effects of diatom consumption

68 Chapter 3

Table 3.3 Overview of the three-way ANOVA results on the effect of diatom density, macroinvertebrate monoculture and community. In the community, B. pilosa had a higher diatom consumption species and community composition on diatom consumption. Asterisks indicate statistically significant compared to H. arenarius (Tukey’s post hoc, p<0.01) and S. squamata (Tukey’s post hoc, p-values at α=0.05. p<0.001). Regardless of community composition, B. pilosa was the only species that df F p significantly affected diatom consumption at 10% diatom density, while H. arenarius and S. Species 2 31.6 <0.001 * squamata showed little response in terms of consumption (ANOVA, df=2, F=22.2, p<0.001) Diatom density 2 39.3 <0.001 * (Figure 3.1, Table 3.4). The amount of diatoms consumed by B. pilosa was not different Community composition 1 6.6 0.012 * between its monocultures and in community at 10% diatom density (Tukey’s post hoc, Species * Diatom density 4 4.4 <0.01 * p=0.37). Species * Community composition 2 18.7 <0.001 * 3.4.4 Net diversity effect of macroinvertebrate diversity and its components Diatom density * Community composition 2 3.9 0.025 * Species * Diatom density * Community composition 4 3.9 <0.01 * The net diversity effect on consumption was positive and similar across diatom densities (one- way ANOVA, df=2, F=1.5, p=0.27) and was mainly driven by complementarity effects. This is Table 3.4 Overview of the two-way ANOVA results on the effect of macroinvertebrate species and clearly shown by the more positive complementarity effect compared to the selection effect, community composition on diatom consumption, for each diatom density level separately. For each of which was closer to zero or negative (Figure 3.2). Differences in diatom consumption between the two-way ANOVAs, p-values are corrected with the Bonferroni correction at α=0.05, resulting in a what we expected from the species’ monocultures and observed in the community were thus pcritical of 0.017. Asterisks indicate statistically significant p-values at pcritical=0.017. negligible between high and low diatom densities. The complementarity effect did not df F p significantly change with diatom density (one-way ANOVA, df=2, F=1.4, p=0.29). However, the 10% diatom density Species 2 22.2 <0.001 * selection effect did change from predominantly negative at 100% diatom density to mildly Community composition 1 1.0 0.324 positive when fewer diatoms were available (one-way ANOVA, df=2, F=7.2, p<0.01). Thus, Species * Community composition 2 1.5 0.237 selection effects contributed more to the overall net diversity effect with decreasing diatom 50% diatom density Species 2 10.3 <0.001 * Community composition 1 2.6 0.117 Species * Community composition 2 7.9 <0.01 * 100% diatom density Species 2 14.1 <0.001 * Community composition 1 10.6 <0.01 * Species * Community composition 2 17.1 <0.001 * hoc, p=0.99 and p=0.72, respectively), with B. pilosa having a higher diatom consumption than H. arenarius in community (0.079 ± 0.031 against 0.013 ± 0.013 mg diatom mg animal-1, respectively; Tukey’s post hoc, p<0.01).

3.4.3 Diatom consumption at low diatom densities

Diatom consumption by the three macroinvertebrate species was altered considerably at low diatom densities compared to high diatom densities (Figure 3.1, Table 3.4). At 50% diatom density, macroinvertebrate species differed significantly in diatom consumption (two-way ANOVA, df=2, F=10.3, p<0.001) and there was a significant interaction effect between species and community composition (two-way ANOVA, df=2, F=7.9, p<0.01). Interestingly, each macroinvertebrate species consumed a similar amount of diatoms in the community and its respective monoculture (Tukey’s post hoc, B. pilosa: p=0.23; H. arenarius: p=0.14 and S. squamata: p=0.15), even though H. arenarius and S. squamata appeared to have consumed Figure 3.1. Diatom consumption of three macroinvertebrate species (b = Bathyporeia pilosa, h = less in the community (see Figure 3.1). This non-significant difference is possibly due to the Haustorius arenarius, s = Scolelepis squamata) at three different diatom densities (percentage dilution large variation observed in diatom consumption for B. pilosa and H. arenarius, both in of ad libitum diatom supply) in either monoculture (Mono) or in a three-species community (Com). Error bars indicate the standard error of the mean.

Non-additive effects of consumption 69

3.4.3 Diatom consumption at low diatom densities

70 Chapter 3

functionally different, and thus complementing species in terms of feeding strategy, non- additive effects can arise even when food availability is low.

3.5.1 High diatom densities: B. pilosa is the most successful consumer

As expected, diatom consumption at high diatom density was altered in community as compared with the species’ monocultures, with B. pilosa having highest consumption in the community, while S. squamata consumed most in monoculture. One explanation is that B. pilosa is ‘released’ from intraspecific competition in the community as it is surrounded by fewer conspecifics, potentially making it a more successful competitor with other species. Bathyporeia pilosa has a preference for benthic microalgae (Maria et al. 2011) and feeds by scraping the organic material from sand grains (Nicolaisen and Kanneworff 1969). In contrast, H. arenarius and S. squamata both have a less distinguished preference for food particles (Dennell 1933, Dauer 1983). Assuming that B. pilosa, as a specialist, is more efficient in consuming its preferred food source (Büchi and Vuilleumier 2014), e.g. by lower handling times or higher ingestion rates, it will reduce food availability for the other species in the community.

In general, the specialist B. pilosa is most successful in community, but not the most successful species in monoculture at high food conditions, which is the generalist S. squamata. These Figure 3.2. Net diversity effect, complementarity effect and selection effect as function of diatom density (percentage dilution of ad libitum diatom supply), expressed as the amount of diatoms findings are in accordance to theory (Büchi and Vuilleumier 2014), stating that specialists consumed (mg per mg animal). Each dot represents one mesocosm containing a three-species outcompete generalists in their optimal habitat (here: high benthic diatom density at 100% community. diatom density) and that heterogeneity of food together with the absence of strong competing species (here: in monoculture) favours generalists. A shift from a single species density. For the net diversity effect, the selection effect finally was canceled out by a slightly assemblage to a community thus coincides with a change in total consumption by the higher complementarity effect at high diatom density (Figure 3.2). individual macroinvertebrate species when food availability is high and heterogeneous.

3.5 Discussion 3.5.2 Low diatom densities: B. pilosa remains the most successful consumer

In this study, we document a strong influence of diatom density on diatom consumption by The species with the lowest competitive ability in this experiment, S. squamata, consumed intertidal macroinvertebrate species, both for single species and in species mixtures. These slightly less in community when diatom density decreased. Although the effect is relatively macroinvertebrate species showed a different consumption pattern when diatom densities small, it does support our hypothesis. At lower diatom densities, we found that B. pilosa decreased. Diatom consumption was obviously lower when food was scarce, but importantly, remained the most successful species in terms of consumption, with a higher consumption the nature of macroinvertebrate species interactions changed as well. Even though the three than S. squamata and H. arenarius in community. At 50% diatom density, the three species macroinvertebrate species responded differently under varying diatom densities, the net consumed similar amounts of diatoms in monoculture. Both H. arenarius and S. squamata diversity effect on consumption was positive and similar across all diatom densities. A positive consumed less in community compared to their respective monocultures, but the difference net diversity effect indicates an increased performance of the community based on the in consumption is slightly smaller for H. arenarius. The main feeding strategy of H. arenarius expectation of the monocultures. Complementarity in consumption was the main driver of is to move the water with its maxillae and filter very small organic particles from this (Dennell the net diversity effect, with an increasing contribution of selection effects with decreasing 1933). In contrast, S. squamata feeds primarily on larger particles (Dauer 1983). Haustorius diatom densities. Hence, the non-additive effects on consumption observed in this intertidal arenarius therefore appears better capable of using smaller food particles than S. squamata, macroinvertebrate community were independent from diatom density and concomitant potentially explaining its slightly higher consumption than S. squamata in community. At 10% changes in macroinvertebrate species interactions. This suggests that in communities with diatom density, only B. pilosa was able to feed on diatoms. Haustorius arenarius and S. squamata were unable to consume at this low diatom density, even in the absence of other

Non-additive effects of consumption 71

functionally different, and thus complementing species in terms of feeding strategy, non- additive effects can arise even when food availability is low.

3.5.1 High diatom densities: B. pilosa is the most successful consumer

3.5 Discussion 3.5.2 Low diatom densities: B. pilosa remains the most successful consumer

72 Chapter 3 macroinvertebrate species. In monoculture, these two macroinvertebrate species possibly response variable as individuals may reach satisfaction on a shorter time scale than e.g. for a had difficulty discovering the food as there were few food particles available, resulting in no variable as biomass production. Indeed, the highest food level in our experiment was consumption. Bathyporeia pilosa consumed a similar amount of diatoms in community as in considered to be ad libitum, thus an excessive food supply does not necessarily lead to monoculture, providing another piece of evidence that interspecific competition did not affect increased consumption. Consequently, positive complementarity effects do not necessarily its consumption when food was scarce. The patterns found in diatom consumption coincide increase with an increase in resource availability. If the enhanced total consumption in with macroinvertebrate occurrences within the tidal regimes of sandy beaches. Bathyporeia community is however maintained over a longer time period, this could lead to a higher pilosa resides mostly in the higher part of the intertidal zone where food supply is low (Fish intertidal macroinvertebrate biomass and promote the flow of nutrients in the intertidal sandy and Preece 1970, Van Tomme et al. 2012), while H. arenarius and S. squamata are generally beach ecosystem. found in the mid-tidal part of the intertidal zone (Leewis et al. 2012) where food availability may locally be enhanced by sea water containing microalgae (McLachlan and Brown 2006). 3.5.3.2 Selection effects

Thus, in this experiment the specialist B. pilosa remained the better competitor at low diatom We hypothesised that selection effects would increase with declining diatom densities, which densities. This is slightly unexpected, because a specialist is predicted to show lower we indeed observed. Selection effects were mainly negative at high diatom density and mildly consumption when preferred food is encountered on a less predictable basis (Büchi and positive at low diatom density, which is in accordance with theoretical expectations (Loreau Vuilleumier 2014), although specialists are also expected to be more efficient consumers of 2000). When less food is available, there appears to be a slightly higher impact of competition the (low amounts of) food available. As a consequence, consumption patterns across the between macroinvertebrate species on consumption when they have to use the same food species did not change when food availability is low. source and when their niches are not fully partitioned. At low diatom densities, relative fitness differences, for example due to different resource requirements, become more important and 3.5.3 A consistent non-additive effect, but shifts between selection and complementarity influence competitive interactions (HilleRisLambers et al. 2012). However, it seems unlikely effects that a cascading effect of potential differences in relative fitness on total consumption occurred, as consumption was similar between monocultures and the community. 3.5.3.1 Complementarity effects 3.5.3.3 Total net biodiversity effect In accordance to our expectation, we found a large and dominant positive complementarity effect across diatom densities, indicating that functionally distinct species can increase total The net diversity effect on consumption was positive and similar across diatom densities and consumption. Functionally different species may be better able to coexist due to stabilizing was mainly driven by complementarity effects. Although we found that at 10 and 50% diatom niche differences, such as niche-partitioning, when these effects are greater than relative density the contribution of the less successful species H. arenarius and S. squamata to the fitness differences (Tilman et al. 1997, HilleRisLambers et al. 2012, Valladares et al. 2015), total consumption in community was limited, consumption was always greater in the making niche-partitioning a probable mechanism of enhancing total diatom consumption in community as compared with the expectation based on the species’ monocultures. This shows this study system. The different feeding strategies of these co-occurring macroinvertebrate that the range of functions across macroinvertebrate species was large enough to observe species in the intertidal beach make them functionally different in terms of consumption. This non-additive effects for consumption and therefore increase resource use efficiency. difference accounted for part of the variation in consumption observed in this study. Bathyporeia pilosa contributed most to the total net biodiversity effect of consumption and Facilitation is another aspect of complementarity, but in intertidal communities the main was also the species with the lowest average biomass (1.38 ± 0.23 mg dry biomass against facilitation mechanism appears to be the amelioration of physical stress (e.g. temporal 5.69 ± 0.86 mg and 7.58 ± 2.83 mg for H. arenarius and S. squamata respectively). However, drought and reworking of soft sediments) (Bulleri 2009). This is not directly linked to food it is expected that species with a high biomass exert the largest effect on consumer availability and biological interactions, and is in general unlikely to occur in this mesocosm set performance and related community processes (Reiss et al. 2011), and this discrepancy may up with identical physical environments. Therefore, niche-partitioning appears to be the most be due to a higher mass-specific metabolic rate of small-bodied organisms such as B. pilosa. probable mechanism explaining observed positive complementarity effects in our experiment 3.5.4 Implications for community ecology (Finke and Snyder 2008). Although previous studies reported an increase in the positive complementarity effect for ecosystem functioning with an increase in resource availability The differences in consumption between macroinvertebrate species within a community, as (Fridley 2002, Boyer et al. 2009), we did not find this pattern. Given the short time period of found here, could eventually lead to changes in community composition. In turn, this altered our study, we used consumption as the response variable, which is a more constrained community may influence food availability via consumption. This touches upon the central

Non-additive effects of consumption 73 macroinvertebrate species. In monoculture, these two macroinvertebrate species possibly response variable as individuals may reach satisfaction on a shorter time scale than e.g. for a had difficulty discovering the food as there were few food particles available, resulting in no variable as biomass production. Indeed, the highest food level in our experiment was consumption. Bathyporeia pilosa consumed a similar amount of diatoms in community as in considered to be ad libitum, thus an excessive food supply does not necessarily lead to monoculture, providing another piece of evidence that interspecific competition did not affect increased consumption. Consequently, positive complementarity effects do not necessarily its consumption when food was scarce. The patterns found in diatom consumption coincide increase with an increase in resource availability. If the enhanced total consumption in with macroinvertebrate occurrences within the tidal regimes of sandy beaches. Bathyporeia community is however maintained over a longer time period, this could lead to a higher pilosa resides mostly in the higher part of the intertidal zone where food supply is low (Fish intertidal macroinvertebrate biomass and promote the flow of nutrients in the intertidal sandy and Preece 1970, Van Tomme et al. 2012), while H. arenarius and S. squamata are generally beach ecosystem. found in the mid-tidal part of the intertidal zone (Leewis et al. 2012) where food availability may locally be enhanced by sea water containing microalgae (McLachlan and Brown 2006). 3.5.3.2 Selection effects

74 Chapter 3 question of whether species diversity is a consequence of (response) or a cause of (effect) 3.6 Appendix resource availability, and these effects have been shown to be able to occur simultaneously A B (Cardinale et al. 2006). However, we only tested for the former aspect. Following community dynamics over time and tracking both resource density and consumer composition may help to clarify how these are linked (and intertwined). Finally, when translating our findings to field conditions, the impacts of differences in environmental conditions need to be accounted for.

Diatom density is a direct result of marine primary production which is an important ecosystem function. Diatom production can be enhanced, for example, by an increase of anthropogenic nutrient input which is currently wide spread in marine systems (Allgeier et al. 2011) or reduced by over-consumption (e.g. Schlacher and Hartwig 2013). Wave and current strength subsequently may affect diatom supply to the beach, creating resource heterogeneity that influences the relation between species composition and community and C ecosystem processes (Dyson et al. 2007), while hydrodynamics may as well directly affect consumption patterns. Despite these limitations to our current set-up, we predict that higher macroinvertebrate functional dissimilarity results in a higher total consumption by the community. In a bottom-up controlled ecosystem, high consumer dissimilarity thus aids in making nutrients available from primary production to higher trophic levels.

3.5.5 Conclusions

In the context of community responses to differences in environment, we showed that variation in food availability consistently leads to positive non-additive effects of consumption by a macroinvertebrate community. This suggests that in communities with functionally Figure A3.1. Three pictures showing the mesocosms used in the experiment: A) a helicopter-view of different, and thus complementing, species, non-additive effects can arise even when food an open mesocosm (plastic foil removed) filled with sand and water, with aeration of the water column availability is low. This finding is especially relevant in ecosystems (such as coastal or tundra in action, B) side view of a mesocosm and C) an overview of the mesocosms as placed in the climate ecosystems) where food supply is limited or variable, either because of temporal or spatial room during the experiment. variability, and the ecosystem is primarily bottom-up controlled.

Non-additive effects of consumption 75 question of whether species diversity is a consequence of (response) or a cause of (effect) 3.6 Appendix resource availability, and these effects have been shown to be able to occur simultaneously A B (Cardinale et al. 2006). However, we only tested for the former aspect. Following community dynamics over time and tracking both resource density and consumer composition may help to clarify how these are linked (and intertwined). Finally, when translating our findings to field conditions, the impacts of differences in environmental conditions need to be accounted for.

3.5.5 Conclusions

Chapter 4

Strong seasonal and macroinvertebrate community effects on nutrient mineralisation in wrack on sandy beaches

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman and Rien Aerts

This chapter has been submitted for publication

Chapter 4

Strong seasonal and macroinvertebrate community effects on nutrient mineralisation in wrack on sandy beaches

Emily M. van Egmond, Peter M. van Bodegom, Matty P. Berg, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman and Rien Aerts

This chapter has been submitted for publication

78 Chapter 4

4.1 Abstract water levels (Hammann and Zimmer 2014). Drift lines mainly consist of stranded sea grasses and sea weeds (collectively termed wrack) but may also include other organic components, Sandy beaches play a significant role in nutrient cycling on the land-ocean interface, and such as carrion and faeces or man-made debris (Colombini and Chelazzi 2003). Young drift decomposition of beach-cast macroalgae (i.e. wrack) is crucial to this connection. The lines are primarily composed of freshly deposited wrack and are formed around the high water decomposition and mineralisation of wrack is driven by a variety of abiotic and biotic line (Orr et al. 2005). When wrack is not resuspended back into the water by high sea water processes, but we currently lack an understanding of how these drivers may interact. levels, wrack may either remain in its current drift line or be blown further up-shore at high Therefore, we assessed the individual and combined effects of the macroinvertebrate wind speeds, until the material becomes buried in the sand, caught by other structures (e.g. community, season and drift line position on N and P mineralisation of wrack and of season plants) or has reached a wind-dead location (Hammann and Zimmer 2014). This older, more and drift line position on macroinvertebrate community composition, by performing a litter decayed wrack is generally present in drift lines above the high water line, both higher up the bag experiment on a sandy beach. We found a strong effect of season on both beach and closer to the dune foot than young drift lines consisting of fresh wrack (Rodil et al. macroinvertebrate community composition and N and P mineralisation. Drift line was not a 2008). driver of either macroinvertebrate community composition or N and P mineralisation, except that old drift lines have higher P mineralisation in spring while the opposite was the case in Wrack that remains on the beach decomposes through a variety of abiotic and biotic processes other seasons. Multiple linear regression analysis was used to test the combined effects on N (Colombini and Chelazzi 2003). Abiotic processes that work on deposited wrack include drying and P mineralisation, showing that season (87% on average) and macroinvertebrate and photodegradation by the sun, erosion of organic material by wind and coverage by a layer abundance (12% on average) together explained most of the variation in N and P of sand, while biotic processes include the decomposition of wrack by microbes and mineralisation. For P mineralisation, macroinvertebrate richness and diversity also had an macroinvertebrates (Colombini and Chelazzi 2003, Orr et al. 2005). The interaction between additional but small effect (3% and 2% on average, respectively). The independence of N and biotic and abiotic processes may, furthermore, depend on both spatial and temporal factors, P mineralisation from drift line position indicates that wrack decay is largely uncoupled from such as position across the beach (i.e. height above sea water level) and season, respectively the direct environment where decomposition occurs. Instead, the strong effects of both (McLachlan and McGwynne 1989, Colombini et al. 2000, Gonçalves and Marques 2011). season and macroinvertebrate abundance on nutrient cycling suggest that nutrient hot spots Macroinvertebrates directly affect wrack decomposition by feeding on wrack, and its may be formed on sandy beaches that accumulate wrack. Such hot spots likely support beach associated biofilm (Porri et al. 2011), thereby fragmenting the organic material (Ince et al. pioneer plant growth and enhance vegetation cover and diversity. In the light of coastal 2007, Salathé and Riera 2012). By decreasing wrack particle size and mixing bacteria with management, our study stresses the importance of leaving wrack undisturbed on sandy wrack through macroinvertebrate feeding activity, the surface area for microbial activity beaches, especially during the plant growing season. increases and decomposition is stimulated (Robertson and Mann 1980, Colombini and 4.2 Introduction Chelazzi 2003). Also, the burrowing activities of some macroinvertebrates incorporate wrack fragments within the sand, indirectly increasing decomposition due to improvement of abiotic Coastal ecosystems provide a dynamic interface linking terrestrial and marine ecosystems conditions (Inglis 1989), i.e. lower maximum temperatures and higher soil moisture content. (Heck et al. 2008) and perform a wide range of important ecosystem functions, such as coastal Wrack consumption can be high and supratidal macroinvertebrates have been estimated to protection by buffering of wave energy and nutrient cycling (McLachlan and Brown 2006). consume up to 80% (Griffiths and Stenton-Dozey 1981, Griffiths et al. 1983) and even 100% Sandy beaches, in particular, form a unique ecosystem of their own (McLachlan 1980), where (Lastra et al. 2015) of the organic matter input entering the sandy beach. Therefore, the terrestrial and marine habitats strongly interact. As sandy beaches receive large amounts of macroinvertebrate community can be a crucial driver of wrack decomposition, especially exogenous organic matter that has been produced by primary and secondary producers in the where abundances are locally high and/or consumption of wrack by individual ocean, they are considered to be primarily recipient ecosystems (Liebowitz et al. 2016). macroinvertebrates is significant (e.g. Lastra et al. 2015, Ruiz-Delgado et al. 2016). Ecological communities on sandy beaches depend heavily on this organic matter input for their functioning (Polis and Hurd 1996, Del Vecchio et al. 2013, Schlacher et al. 2017), The interactions between macroinvertebrate community composition and wrack especially as the internal primary production of sandy beaches is low and the ecosystem is decomposition change over time. After deposition on the beach, wrack is swiftly colonised by generally bottom-up controlled (Schlacher and Hartwig 2013). macroinvertebrates, marking the start of a succession of microbes and macroinvertebrate species associated with decay stages of wrack (Colombini and Chelazzi 2003, Olabarria et al. Organic material is deposited onto the beach in a drift line during retreating water. This 2007, Whitman et al. 2014, Ruiz-Delgado et al. 2016). In general, talitrids (such as the deposition is influenced by a combination of wind, waves and currents, usually forming several amphipod Talitrus saltator Montagu) and Diptera are the first colonisers of wrack, followed semi-continuous bands of organic material parallel to the coast line. On a tide-dominated by insects (mainly Coleoptera) and spiders (Lavoie 1985, Ruiz-Delgado et al. 2016). With an beach, multiple drift lines are formed with a shift from spring to neap tide as the water line increase in wrack age and stage of decay, changes in the macroinvertebrate abundance, keeps reaching lower levels on the beach, while on tide-independent beaches, a decrease in richness and community composition occur (Jędrzejczak 2002b, Olabarria et al. 2007, wind speed is primarily responsible for the formation of multiple drift lines by lowering sea

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80 Chapter 4

Olabarria et al. 2010). In turn, the macroinvertebrate community affects the decomposition To establish an environmental gradient perpendicular to the coast line, litter bags were placed of wrack, mainly via consumption of organic matter (Lastra et al. 2015). When a patch of wrack either within a recently established drift line (<48 h old) directly above the high water line has been largely decomposed, macroinvertebrates may move along to other, less (HWL) or an old drift line (> several days old) higher up the beach, with at least 10 m between decomposed wrack patches. Only species that can still feed on more decomposed wrack or both lines. While the number of drift lines was greatly variable in the field, both from day to use it for other purposes (e.g. habitat, egg deposition, secondary consumption) will remain day and between seasons (personal observation), the young drift line was always the one at (Ruiz-Delgado et al. 2016). Thus, there appears to be a tight, reciprocal interaction between HWL and the old drift line was higher up on the beach and the one closest to the dune foot. the macroinvertebrate community composition and wrack decomposition (Lastra et al. 2015). Young drift lines consisted of freshly deposited wrack which was generally still moist from the sea water, while old drift lines consisted of dry wrack that had been positioned on the beach The decomposition of wrack on sandy beaches results in the release of inorganic nitrogen (N) longer ago and was (partly) buried by sand. and phosphorus (P) to the environment (i.e. mineralisation) (Dugan et al. 2011, McLachlan and Brown 2006). This may lead to a nutrient flow to the water to support marine primary The experiment was performed in three seasons to study seasonal effects on N and P production, as nutrients leach from partly decomposed wrack around the high water line mineralisation: spring (May 2015), summer (August 2015) and autumn (October 2015). Litter (Colombini and Chelazzi 2003). This is supported by the suggestion that most eroding sandy bags consisted of freshly collected litter of Ulva lactuca Linnaeus, a common green macroalgae beaches flush its nutrients, together with beach sand, back to the water, thereby returning species found among wrack on Dutch and other European sandy beaches (e.g. Barreiro et al. the nutrients provided by the exogenous organic material (McLachlan and McGwynne 1989). 2011). Litter bags were incubated in the drift lines for approximately two weeks, after which At some conditions, nutrient hot spots may be created in the supratidal zone, locally they were harvested. This period was chosen as it was expected that U. lactuca would have supporting terrestrial primary (Hemminga and Nieuwenhuize 1990, Posey et al. 1999, Del been decomposed for more than 50% (Buchsbaum et al. 1991, Mews et al. 2006), which would Vecchio et al. 2013) and secondary production (Polis and Hurd 1996, Schlacher et al. 2017). allow wrack to be significantly decomposed and differences in wrack decay to have emerged. The fast decomposition was considered a major advantage of U. lactuca over e.g. the more While the individual components related to wrack dynamics on sandy beaches are known (as slowly decomposing macroalgae Fucus vesiculosus Linnaeus which is more common among discussed above), we lack an understanding on the interactions between season, wrack (Barreiro et al. 2011), as a shorter incubation period made the experiment less macroinvertebrates and position on the beach in determining wrack decomposition and vulnerable to disturbances. Thus, there were two treatments within this litter bag experiment: nutrient mineralisation. Identifying the main drivers of wrack decomposition and drift line position (young or old) and season (spring, summer or autumn). As it was expected mineralisation on sandy beaches is essential to understand nutrient cycling in the sandy beach that litter bags would be lost at the beach due to both natural (e.g. storms) and anthropogenic ecosystem and its connections to terrestrial and marine ecosystems. Therefore, in this study, (e.g. digging up of litter bags by humans or dogs) disturbances, we placed 30 litter bags for we aimed to assess whether 1) supratidal macroinvertebrate community composition, 2) each combination of treatments. This resulted in 60 litter bags placed on the beach per season season (temporal effect), and/or 3) placement in young or old drift lines (horizontal spatial and 180 litter bags in total for the entire experiment. effect) are drivers of N and P mineralisation of wrack. We hypothesised that 1) a higher macroinvertebrate abundance and a more diverse community have a positive effect on N and Prior to placement of a litter bag in the drift line, U. lactuca was rewetted by submerging the P mineralisation of wrack, 2) N and P mineralisation of wrack is dependent on season, with a litter bag in sea water at the site for 5 seconds. This was done to mimic the moisture content higher mineralisation in summer, and 3) N and P mineralisation of wrack is independent of of natural wrack when freshly deposited on the beach and to have similar initial moisture drift line position. Regarding the third hypothesis; by using the same fresh wrack in both young conditions in each litter bag. Litter bag margins were buried up to 3 cm deep, securing the and old drift lines, our research will allow to decouple the effects of wrack decay stage and edges under the sand but allowing the middle part of the bag (± 10 cm2) to be uncovered. In environment on decomposition and mineralisation. To study the effect of the supratidal each drift line, we marked ten positions that were each 10 m apart, resulting in 90 m of drift macroinvertebrate community, drift line and season on N and P mineralisation, we performed line parallel to the coast to place litter bags. At each position, three litter bags were placed a litter bag experiment on a sandy beach along the Dutch coast. together in a triangle no more than 50 cm from the drift line. To prevent removal of litter bags due to disturbance, a 23-cm iron pin was placed 30 cm deep in the sand at the center of each 4.3 Methods cluster of three litter bags, to which each of the litter bags was attached with a piece of sisal 4.3.1 Design of field experiment twine. All twines were buried in the sand. GPS coordinates were taken at each cluster of three litter bags for retrieval purposes. At the end of the entire experiment, 95 of the 180 litter bags The experiment was conducted near Scheveningen, the Netherlands (52.05 N, 4.19 E). The could be retrieved, however, and 64 litter bags had enough wrack material (≥1 g of wrack with Netherlands is subject to a temperate climate, with a mean annual temperature of 11.3 °C and remaining sand) left for chemical analysis. a mean annual rainfall of 891 mm recorded at Hoek van Holland, the closest weather station to the field site (Royal Netherlands Meteorological Institute (KNMI) 2015). Litter bags (for details: see below) were placed on a beach of approximately 200 m wide backed up by dunes.

Nutrients mineralisation in wrack 81

82 Chapter 4

4.3.2 Litter bag preparation Samples were then diluted with 4 ml demineralised water and total P content was measured colorimetrically (Murphy and Riley 1962). Ash free dry weight was determined by combusting We had access to a U. lactuca culture which provided for a steady supply of sea weed a homogenised subsample of 20 mg (10 mg for U. lactuca at t=0) for 5 h at 550 °C. All fresh throughout the year. For each season, a fresh batch of U. lactuca of approximately 5-6 kg wet and dry masses were determined up to the nearest 0.001 g. weight was collected from the cultures at The Netherlands Institute for Sea Research (NIOZ), at Texel, the Netherlands, 7-10 days before the start of the experiment. Ulva lactuca was air- 4.3.5 Data and statistical analysis dried by hanging it on plastic lines at 25 °C for at least 72 hours. From this air-dried material, Of the 64 retrieved litter bags, four litter bags that did not contain any macroinvertebrates 6 subsamples were dried in the oven at 70 °C for 72 hours to determine the relationship were excluded, resulting in 60 litter bags to be used in the data analysis. N and P mineralisation between air-dry and oven-dry U. lactuca, which was used to estimate the oven-dry weight added at the start of the experiment. Litter bags were made 15 x 20 cm in size and constructed (in mg per g initial wrack dry weight) was calculated as the absolute difference in total N or P of white nylon mesh, with a smaller mesh size on the lower (1 mm) than the upper (10 mm) content of wrack at harvest and at the start of the experiment per litter bag, which was divided side of the litter bag. This was done to prevent fragmented sea weed of falling through larger by the initial dry weight of wrack for standardisation. The total N and P content in wrack at openings upon harvest, but to allow larger macroinvertebrates to enter the litter bag, the start of the experiment was estimated using % N and % P of t=0 wrack material from each 10 respectively. After cleaning air-dried sea weed from dead animals and other organic respective season. Macroinvertebrate abundance (log -transformed), richness (number of contaminations with a pair of tweezers, 4.0 ± 0.1 g air-dry U. lactuca was added to each litter taxa) and Shannon’s diversity index (H’) were also calculated per litter bag. bag and sealed on the edges with hot glue. Prior to analysis, all data were tested for homogeneity of variances (Levene’s test) and normal 4.3.3 Macroinvertebrate collection distribution (Shapiro-Wilk test). When these assumptions were not met, a log (N At harvest, each retrieved litter bag was detached from the iron pin and gently placed in an mineralisation and macroinvertebrate abundance) or square root (macroinvertebrate empty plastic 1-L pot, avoiding animals to escape. Below each litter bag, a 20 x 20 x 15 cm richness and diversity) transformation was performed on the original data. First, we analysed volume of sand was collected using a stainless-steel rectangle corer with a small spade and whether macroinvertebrate community metrics were significantly affected by drift line (two sieved over a 10-mm sieve directly in the sea. Remaining animals were collected and stored in levels: young and old) and season (three levels: spring, summer and autumn) by running two- 70% ethanol. On the same day of harvest, material was transported to the laboratory and way ANOVAs. Secondly, we analysed how N and P mineralisation were affected by drift line intact litter bags with the remaining wrack were placed in a Tullgren extractor for at least one (two levels: young and old) and season (three levels: spring, summer and autumn) in two-way week, to extract all macroinvertebrates (van Straalen and Reijninks 1979). Care was taken to ANOVAs. Two-way ANOVAs were followed by Tukey post hoc tests where applicable. Finally, transfer only a limited amount of sand together with the litter bag into the Tullgren funnel to prevent clogging of the vials. Animals were collected in a vial with 70% ethanol, counted and macroinvertebrate abundance, richness or diversity were added to drift line and season in a identified to the lowest possible taxonomic level (Table A4.1). Air-dried litter bags with multiple regression analysis to determine whether macroinvertebrate community metrics remaining wrack were stored in 1-L plastic pots until further processing the week after. added predictive power to explaining variance of N and P mineralisation. Only the interaction between drift line and season was included in each multiple regression model, following the 4.3.4 Measurements on macroalgae results of the two-way ANOVAs. The relative importance of each of the factors in the multiple Remaining wrack was removed from the litter bags and gently washed with artificial sea water regression model was calculated by decomposing R2 into non-negative contributions that sum (30‰ salt content; Instant Ocean, Aquarium Systems, Inc., Mentor, OH, USA) to remove sand to the total of R2, taking care of the dependency of ordering within the regression model by and organic contaminants attached to the wrack. Wrack samples were dried at 70 °C for 72 averaging over all possible orderings of regressors, following Grömping (2006). All statistical hours, weighed for dry biomass (including remaining sand) and ground into a fine powder in analyses were done in R, version 3.2.3 (R Core Team 2015). a ball mill (MM400, Retsch, Haan, Germany) and homogenised by mixing the ground sample with a steel stirrer. Each sample was split into two: one part was used to determine ash free 4.4 Results dry weight and the other part was used for chemical analysis (total C, N and P content). Three U. lactuca samples taken at t=0 for each season were also analysed for total C, N and P content 4.4.1 Macroinvertebrate abundance, richness and diversity across drift line and season and ash free dry weight. Total C and N content of wrack were determined by weighing 8-12 mg (3-4 mg for U. lactuca at t=0) of ground sample in a tin cup, followed by dry combustion Macroinvertebrate abundance, richness and diversity did not differ between drift lines, but with a Flash EA1112 elemental analyser (Thermo Scientific, Rodana, Italy). For total P content, did significantly differ between seasons (Table 4.1). In autumn, macroinvertebrate abundance a 50 mg (100 mg for U. lactuca at t=0) subsample was digested in 1 ml of a 1:4 mixture of 37% was higher than in spring and summer (190 ± 130 ind. against 26 ± 45 and 75 ± 75 ind. litter bag-1, respectively; Tukey’s post hoc, t=5.4, p<0.001 and t=2.8, p=0.02, respectively; Figure (by volume) HCl and 65% (by volume) HNO3, in a closed Teflon cylinder for 6 h at 140 °C.

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84 Chapter 4

Table 4.1. Results of the two-way ANOVAs for macroinvertebrate abundance, richness and Shannon’s Table 4.3. Results of multiple linear regression analysis for the relationship between N and P diversity with drift line and season as factors. An asterix indicates a significant p-value (<0.05), while mineralisation and macroinvertebrate community (implemented as either abundance (log- an open circle indicates a trend (p<0.10). transformed), richness or Shannon’s diversity), drift line and season. N and P mineralisation were the dependent variables in these models (Y in the model Y ~ X). In each model, the interaction between

df F P drift line and season was included. An asterix indicates a significant p-value (<0.05), while an open Macroinvertebrate abundance circle indicates a trend (p<0.10). Drift line 1 0.5 0.50 % of model df F p Season 2 18.1 <0.001* explained

Drift line * Season 2 4.9 0.01* N mineralisation 2 Macroinvertebrate richness Abundance Overall fit: R =0.63, p <0.001* Abundance 1 29.4 <0.001* 11 Drift line 1 0.6 0.44 Drift line 1 0.5 0.47 <1 Season 2 18.0 <0.001* Season 2 37.6 <0.001* 88 Drift line * Season 2 0.4 0.66 Drift line * Season 2 0.7 0.49 1.2 2 Macroinvertebrate diversity Richness Overall fit: R =0.63, p <0.001* Richness 1 3.3 0.07 ° 1.2

Drift line 1 3.5 0.07 ° Drift line 1 0.1 0.82 <1 Season 2 50.1 <0.001* 98 Season 2 50.5 <0.001* Drift line * Season 2 0.4 0.65 <1 Drift line * Season 2 1.5 0.23 2 Diversity Overall fit: R =0.63, p <0.001* Diversity 1 3.5 0.07 ° 1.2

Drift line 1 0.0 0.97 <1 Table 4.2. Results of the two-way ANOVAs for N and P mineralisation with drift line and season as Season 2 50.0 <0.001* 98 factors. An asterix indicates a significant p-value (<0.05). Drift line * Season 2 0.4 0.66 <1

df F P P mineralisation 2 N mineralisation Abundance Overall fit: R =0.89, p <0.001* Abundance 1 168.6 <0.001* 13 Drift line 1 0.5 0.48 <1 Drift line 1 0.1 0.73 Season 2 159.1 <0.001* 85 Season 2 59.0 <0.001* Drift line * Season 2 5.0 <0.01* 2.0 Drift line * Season 2 0.7 0.50 2 Richness Overall fit: R =0.89, p <0.001* Richness 1 7.8 <0.01* 2.5 P mineralisation Drift line 1 0.0 0.93 <1 Drift line 1 0.07 0.79 Season 2 237.7 <0.001* 94

Season 2 227.7 <0.001* Drift line * Season 2 4.7 0.01* 1.9 Drift line * Season 2 5.4 <0.01* Diversity Overall fit: R2=0.89, p <0.001* Diversity 1 21.9 <0.001* 1.7 Drift line 1 0.5 0.47 <1 Season 2 237.6 <0.001* 96 4.1). In summer, macroinvertebrate richness was higher than in spring and autumn (3.2 ± 1.2 Drift line * Season 2 5.6 <0.01* 2.1 -1 taxa against 1.5 ± 1.1 and 1.4 ± 0.7 taxa litter bag respectively; Tukey’s post hoc, t=4.8, p<0.001 and t=-5.8, p<0.001, respectively; Figure 4.1). Macroinvertebrate diversity was higher 4.4.2 N and P mineralisation across drift line and season in summer than in spring and autumn (H’ = 0.8 ± 0.2 against 0.2 ± 0.3 and 0.02 ± 0.04, For N mineralisation, there was a significant effect of season only (Table 4.2). In spring, N respectively; Tukey’s post hoc, t=4.6, p<0.001 and t=-6.8, p<0.001, respectively; Figure 4.1). In mineralisation was lower (9.36 ± 0.89 mg g initial wrack-1) than in summer and autumn (14.78 addition, macroinvertebrate diversity was significantly different between spring and autumn ± 2.60 and 15.05 ± 2.57 mg g initial wrack-1, respectively; Tukey’s post hoc, t=8.0, p<0.001 and (Tukey’s post hoc, t=-2.4, p<0.05), with a higher macroinvertebrate diversity in spring. Only t=8.7, p<0.001, respectively; Figure 4.2). Also for P mineralisation, only the main effect of for macroinvertebrate abundance there was a significant interaction effect between drift line season was significant (Table 4.2). In spring, P mineralisation was lowest (1.14 ± 0.07 mg g and season (Table 4.1). In summer, the macroinvertebrate abundance was higher in old than -1 -1 -1 initial wrack ) while P mineralisation was highest in autumn (1.57 ± 0.07 mg g initial wrack ), in young drift lines (127 ± 77 ind. against 28 ± 32 ind. litter bag ; Tukey’s post hoc, t=3.3, with an intermediate P mineralisation in summer (1.30 ± 0.07 mg g initial wrack-1; Figure 4.2). p=0.02), while macroinvertebrate abundance in spring and autumn was similar between In contrast to N mineralisation, there was a significant interaction effect of drift line and young and old drift lines (Tukey’s post hoc, t=0.2, p=1.0 and t=-2.3, p=0.2 respectively). season for P mineralisation (Table 4.2). P mineralisation was slightly higher in old drift lines in spring (1.17 ± 0.06 against 1.10 ± 0.06 mg g initial wrack-1), while the opposite was the case

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for summer and autumn with a slightly higher P mineralisation in young drift lines (1.33 ± 0.07 A against 1.27 ± 0.08 mg g initial wrack-1 and 1.59 ± 0.07 against 1.55 ± 0.06 mg g initial wrack-1,

respectively; Figure 4.2).

4.4.3 Combined effect of the macroinvertebrate community, drift line and season on

mineralisation

combination with season (Table 4.3). In addition, macroinvertebrate abundance showed a significant positive effect on N mineralisation, while richness and diversity did not significantly affect N mineralisation. For P mineralisation, macroinvertebrate abundance, richness and

diversity all had a significant positive impact (Table 4.3). Season explained 85 to 98% of the B fitted model, while macroinvertebrate abundance, richness and diversity explained 11 to 13%, 1 to 3% and 1 to 2% respectively. Adding interaction terms between macroinvertebrate

abundance, richness or diversity and drift line and season respectively, did not change these patterns (see Appendix, Table A4.2 and A4.3).

A B

Figure 4.2. Means for A) N mineralisation and B) P mineralisation of wrack per drift line and season. Error bars indicate the standard error from the mean. 4.5 Discussion In this study we aimed to assess the individual and combined effects of the supratidal macroinvertebrate community, drift line position and season on N and P mineralisation of C wrack. We found a strong effect of season on both macroinvertebrate community composition and N and P mineralisation. Season explained most of the variation in N and P mineralisation. Drift line position only showed an effect on macroinvertebrate abundance and

P mineralisation in interaction with season. When adding macroinvertebrate abundance to the multiple regression model, the total explained variance remained the same, while both season and macroinvertebrate abundance affected N and P mineralisation, indicating that a

part of the seasonal dynamics in N and P mineralisation was explained by macroinvertebrate abundance. Moreover, P mineralisation was also explained by macroinvertebrate richness and diversity, but to a lesser extent than by macroinvertebrate abundance and season. Together,

this indicates that both season and macroinvertebrate community metrics, in particular Figure 4.1. Means for macroinvertebrate A) abundance, B) richness and C) Shannon’s diversity per drift abundance, played a crucial role in nutrient cycling on our sandy beach. line and season. Error bars indicate the standard error from the mean.

Nutrients mineralisation in wrack 87 for summer and autumn with a slightly higher P mineralisation in young drift lines (1.33 ± 0.07 A against 1.27 ± 0.08 mg g initial wrack-1 and 1.59 ± 0.07 against 1.55 ± 0.06 mg g initial wrack-1, respectively; Figure 4.2).

4.4.3 Combined effect of the macroinvertebrate community, drift line and season on mineralisation

Within the multiple linear regression models, the effects of drift line and season on N and P mineralisation were maintained, with a significant positive effect of season on both N and P mineralisation and only on P mineralisation a significant positive effect of drift line in combination with season (Table 4.3). In addition, macroinvertebrate abundance showed a significant positive effect on N mineralisation, while richness and diversity did not significantly affect N mineralisation. For P mineralisation, macroinvertebrate abundance, richness and diversity all had a significant positive impact (Table 4.3). Season explained 85 to 98% of the B fitted model, while macroinvertebrate abundance, richness and diversity explained 11 to 13%, 1 to 3% and 1 to 2% respectively. Adding interaction terms between macroinvertebrate abundance, richness or diversity and drift line and season respectively, did not change these patterns (see Appendix, Table A4.2 and A4.3).

A B

88 Chapter 4

decomposition and mineralisation through an increase in feeding, shredding and digging Importantly, there appears to be a critical, reciprocal relationship between the activities performed by these macroinvertebrates, and the subsequent positive effects on macroinvertebrate community and wrack mineralisation. Macroinvertebrate community microbial activity (Inglis 1989, Jędrzejczak 2002b, Ince et al. 2007, Lastra et al. 2008, Salathé composition associated with wrack has been indicated to influence wrack decomposition and and Riera 2012). Macroinvertebrate abundance was higher in autumn than in spring and mineralisation (Dugan et al. 2003, Lastra et al. 2008, Urban-Malinga et al. 2008, this study). In summer, which was mainly due to the presence of large numbers of Diptera larvae (mainly turn, factors such as wrack biomass, structure and nutritional quality all affect Fucellia sp. and Coelops sp., see Appendix, Table A4.1). Abundance of Diptera larvae on wrack macroinvertebrate community composition (Colombini and Chelazzi 2003, Dugan et al. 2003, typically peaks between one to two weeks of field incubation (Jędrzejczak 2002b), which Olabarria et al. 2007). These processes occur simultaneously in time and space, posing the coincides with the litter bag harvest after two weeks in this study. Abundances of the future research challenge to fully disentangle the relative importance of the reciprocal terrestrial amphipod Talitrus saltator were close to zero in this study, as T. saltator is an early processes occurring between wrack mineralisation and macroinvertebrate community succession species and its abundance on wrack peaks around four days (Jędrzejczak 2002b) composition, both at multiple temporal and spatial scales. up to seven days (Olabarria et al. 2007) after wrack is deposited on the beach. As we sampled the wrack after two weeks, we did not capture this species and our results reflect the 4.5.2 Season is a strong driver of wrack mineralisation cumulative effects across multiple macroinvertebrate community successional stages. Hence, we were unable to disentangle whether an early peak in T. saltator abundance or the later In accordance with our second hypothesis, N and P mineralisation of wrack was highly peak of Diptera larvae was responsible for part of the N and P mineralisation of wrack. As both dependent on season. N mineralisation was high in both summer and autumn, while P groups potentially have a strong effect on wrack decomposition (e.g. Stenton-Dozey and mineralisation was highest in autumn. Seasonal variation in mineralisation may be related to Griffiths 1980, Lastra et al. 2008, Salathé and Riera 2012, Lastra et al. 2015), the relative seasonal differences in weather conditions, such as temperature and moisture content. importance of individual supratidal macroinvertebrate species on wrack mineralisation thus Moderately high temperatures increase wrack decay rates on sandy beaches by stimulating requires further study. feeding rates of macroinvertebrates and microbial activity (Colombini and Chelazzi 2003, Lastra et al. 2015). At the same time, wrack has temperature insulating properties that help For P mineralisation, macroinvertebrate richness and diversity were additionally identified as maintain a more stable, moderate temperature within the patch of wrack compared to the significant predictors, although with a lower magnitude than macroinvertebrate abundance. overlaying air temperature (Coupland et al. 2007). A high precipitation coupled to low This may be related to a greater variety in nutritional requirements among evaporation, and increased moisture conditions e.g. due to burial by sand, stimulates macroinvertebrates when more or different macroinvertebrate species are present on wrack, microbial activity and results in releasing more nutrients from wrack via decay (Lavery et al. potentially influencing wrack mineralisation. As a clear macroinvertebrate succession occurs 2013, Coupland et al. 2007). During our study, both the mean temperature (18.6 °C) and mean on wrack (Olabarria et al. 2007, Whitman et al. 2014, Ruiz-Delgado et al. 2016), early- precipitation (131.3 mm) were highest in August (summer) compared to May (spring; 12.1 °C succession macroinvertebrate species, such as T. saltator, may indirectly facilitate late and 50.6 mm, respectively) and October (autumn; 10.4 °C and 34.5 mm, respectively) (Royal succession macroinvertebrate species, e.g. due to fragmentation of wrack to smaller particle Netherlands Meteorological Institute (KNMI) 2015). The higher temperatures in summer may size as a result of their feeding activities on wrack and its associated biofilm (e.g. Olabarria et have resulted in enhanced wrack N mineralisation, assuming that moisture was not limiting. al. 2007). Late-succession macroinvertebrate species may then be able to feed on wrack that While the net impacts of increased temperature (causing higher evaporation) and increased was previously not available to them in terms of particle size or nutritional quality (Heard precipitation on the moisture content of wrack in the field are not known, it appears likely 1994). This mechanism could also operate within a specific wrack successional stage, where that an additional driver was responsible for the high wrack mineralisation observed in large-sized macroinvertebrates may facilitate small-sized macroinvertebrates, as a greater autumn. As indicated above, macroinvertebrate abundance was strongly related to N and P variety in invertebrate body size is associated with higher mineralisation rates (Heemsbergen mineralisation, and the highest macroinvertebrate abundance was observed in autumn. This et al. 2004, Handa et al. 2014). Finally, niche-partitioning may occur among co-occurring suggests that a part of the seasonal dynamics in N and P mineralisation may be explained by macroinvertebrate species that are dependent on the same food source but have different macroinvertebrate abundance. temporal and spatial uses (Colombini et al. 2000, Jaramillo et al. 2003, Lastra et al. 2010, Bessa et al. 2014a). As a result, at a greater variety of supratidal macroinvertebrate species, more In addition to seasonal effects related to differences in weather conditions and wrack is utilised, resulting in a higher wrack mineralisation. It nevertheless remains unclear macroinvertebrate abundances, the initial quality of wrack used in the experiment may be

Nutrients mineralisation in wrack 89

4.5.1 Macroinvertebrate abundance is a strong driver of wrack mineralisation why this appears to hold for P mineralisation only. This difference between N and P mineralisation might be due to a different distribution of nitrogen- and phosphorus-rich As to our first hypothesis, we did find that macroinvertebrate abundance had a strong positive compounds within wrack: if organic compounds with a high P content have been made effect on both N and P mineralisation of wrack, but macroinvertebrate community richness available from wrack due to a richer and more diverse macroinvertebrate community, this and diversity were only for P mineralisation a significant explanatory variable (see also might have resulted in a higher P mineralisation without affecting N mineralisation. Appendix, Figure A4.1 and A4.2). A higher macroinvertebrate abundance may enhance wrack decomposition and mineralisation through an increase in feeding, shredding and digging Importantly, there appears to be a critical, reciprocal relationship between the activities performed by these macroinvertebrates, and the subsequent positive effects on macroinvertebrate community and wrack mineralisation. Macroinvertebrate community microbial activity (Inglis 1989, Jędrzejczak 2002b, Ince et al. 2007, Lastra et al. 2008, Salathé composition associated with wrack has been indicated to influence wrack decomposition and and Riera 2012). Macroinvertebrate abundance was higher in autumn than in spring and mineralisation (Dugan et al. 2003, Lastra et al. 2008, Urban-Malinga et al. 2008, this study). In summer, which was mainly due to the presence of large numbers of Diptera larvae (mainly turn, factors such as wrack biomass, structure and nutritional quality all affect Fucellia sp. and Coelops sp., see Appendix, Table A4.1). Abundance of Diptera larvae on wrack macroinvertebrate community composition (Colombini and Chelazzi 2003, Dugan et al. 2003, typically peaks between one to two weeks of field incubation (Jędrzejczak 2002b), which Olabarria et al. 2007). These processes occur simultaneously in time and space, posing the coincides with the litter bag harvest after two weeks in this study. Abundances of the future research challenge to fully disentangle the relative importance of the reciprocal terrestrial amphipod Talitrus saltator were close to zero in this study, as T. saltator is an early processes occurring between wrack mineralisation and macroinvertebrate community succession species and its abundance on wrack peaks around four days (Jędrzejczak 2002b) composition, both at multiple temporal and spatial scales. up to seven days (Olabarria et al. 2007) after wrack is deposited on the beach. As we sampled the wrack after two weeks, we did not capture this species and our results reflect the 4.5.2 Season is a strong driver of wrack mineralisation cumulative effects across multiple macroinvertebrate community successional stages. Hence, we were unable to disentangle whether an early peak in T. saltator abundance or the later In accordance with our second hypothesis, N and P mineralisation of wrack was highly peak of Diptera larvae was responsible for part of the N and P mineralisation of wrack. As both dependent on season. N mineralisation was high in both summer and autumn, while P groups potentially have a strong effect on wrack decomposition (e.g. Stenton-Dozey and mineralisation was highest in autumn. Seasonal variation in mineralisation may be related to Griffiths 1980, Lastra et al. 2008, Salathé and Riera 2012, Lastra et al. 2015), the relative seasonal differences in weather conditions, such as temperature and moisture content. importance of individual supratidal macroinvertebrate species on wrack mineralisation thus Moderately high temperatures increase wrack decay rates on sandy beaches by stimulating requires further study. feeding rates of macroinvertebrates and microbial activity (Colombini and Chelazzi 2003, Lastra et al. 2015). At the same time, wrack has temperature insulating properties that help For P mineralisation, macroinvertebrate richness and diversity were additionally identified as maintain a more stable, moderate temperature within the patch of wrack compared to the significant predictors, although with a lower magnitude than macroinvertebrate abundance. overlaying air temperature (Coupland et al. 2007). A high precipitation coupled to low This may be related to a greater variety in nutritional requirements among evaporation, and increased moisture conditions e.g. due to burial by sand, stimulates macroinvertebrates when more or different macroinvertebrate species are present on wrack, microbial activity and results in releasing more nutrients from wrack via decay (Lavery et al. potentially influencing wrack mineralisation. As a clear macroinvertebrate succession occurs 2013, Coupland et al. 2007). During our study, both the mean temperature (18.6 °C) and mean on wrack (Olabarria et al. 2007, Whitman et al. 2014, Ruiz-Delgado et al. 2016), early- precipitation (131.3 mm) were highest in August (summer) compared to May (spring; 12.1 °C succession macroinvertebrate species, such as T. saltator, may indirectly facilitate late and 50.6 mm, respectively) and October (autumn; 10.4 °C and 34.5 mm, respectively) (Royal succession macroinvertebrate species, e.g. due to fragmentation of wrack to smaller particle Netherlands Meteorological Institute (KNMI) 2015). The higher temperatures in summer may size as a result of their feeding activities on wrack and its associated biofilm (e.g. Olabarria et have resulted in enhanced wrack N mineralisation, assuming that moisture was not limiting. al. 2007). Late-succession macroinvertebrate species may then be able to feed on wrack that While the net impacts of increased temperature (causing higher evaporation) and increased was previously not available to them in terms of particle size or nutritional quality (Heard precipitation on the moisture content of wrack in the field are not known, it appears likely 1994). This mechanism could also operate within a specific wrack successional stage, where that an additional driver was responsible for the high wrack mineralisation observed in large-sized macroinvertebrates may facilitate small-sized macroinvertebrates, as a greater autumn. As indicated above, macroinvertebrate abundance was strongly related to N and P variety in invertebrate body size is associated with higher mineralisation rates (Heemsbergen mineralisation, and the highest macroinvertebrate abundance was observed in autumn. This et al. 2004, Handa et al. 2014). Finally, niche-partitioning may occur among co-occurring suggests that a part of the seasonal dynamics in N and P mineralisation may be explained by macroinvertebrate species that are dependent on the same food source but have different macroinvertebrate abundance. temporal and spatial uses (Colombini et al. 2000, Jaramillo et al. 2003, Lastra et al. 2010, Bessa et al. 2014a). As a result, at a greater variety of supratidal macroinvertebrate species, more In addition to seasonal effects related to differences in weather conditions and wrack is utilised, resulting in a higher wrack mineralisation. It nevertheless remains unclear macroinvertebrate abundances, the initial quality of wrack used in the experiment may be

90 Chapter 4

responsible for the strong effect of season on N and P mineralisation of wrack. The C/N ratio environmental gradient across the entire sandy beach, combining both the intertidal and of the wrack used varied between seasons. When adding the C/N ratio of wrack to the multiple supratidal zone (McLachlan and Jaramillo 1995, Wood and Bjorndal 2000), where the higher regression models, C/N ratio was a strong predictor of N and P mineralisation in addition to supratidal zone is relatively stable in terms of the abiotic environment compared to the season (for P mineralisation only) and macroinvertebrate community metrics (see Appendix, intertidal zone. Wrack in older drift lines higher up the beach has consistently higher Table A4.4). Indeed, the N content of wrack is one of the potential drivers of wrack decay on temperatures and lower moisture contents than fresh wrack in young drift lines around the sandy beaches (Jędrzejczak 2002a). In conclusion, N and P mineralisation of wrack was high water line (Ruiz-Delgado et al. 2015). Moreover, wrack (and its associated strongly determined by season, which was due to both seasonal differences in weather macroinvertebrate community) close to the dune foot is less prone to rewetting by tidal conditions and the initial wrack quality used. inundation, redistribution across the beach by waves and wind, and inundation of macroinvertebrate colonisers (Wood and Bjorndal 2000, Defeo and Gómez 2005, Coupland et Jędrzejczak (2002a) proposes that the order of importance for factors affecting wrack decay al. 2007). Despite these apparent environmental differences, our results suggest that instead rate are type of wrack (i.e. macroalgae species), temperature, internal N content of wrack and differences in wrack decay stage are the dominant driver of differences in wrack decomposer activity. Similarly, in terrestrial ecosystems, temperature and plant growth form decomposition between drift lines. Macroinvertebrate abundance was similar between drift composition are identified as most important drivers of decomposition, with a smaller role for lines, possibly because species are mobile, allowing them to easily migrate between wrack litter quality within species (e.g. Cornelissen et al. 2007). In addition, climate is considered to patches deposited across the sandy beach (Colombini et al. 2000). It thus seems that the stable be a dominant driver of decomposition over macrodetritivores (García-Palacios et al. 2013), macroinvertebrate community and a high degree of migration of supratidal which may be even more pronounced on sandy beaches as they are classically viewed as being macroinvertebrate species across the supratidal zone of the sandy beach may have caused dominated by the environment (McLachlan and Brown 2006). Our results indicate that season wrack mineralisation to be largely independent from drift line position. was the main driver of N and P mineralisation followed by macroinvertebrate abundance, 4.5.4 Implications for coastal management supporting the above hypothesis on the order of importance of factors influencing mineralisation of wrack. In light of coastal management, our study stresses the importance of leaving wrack undisturbed on sandy beaches, especially in summer. In summer, wrack mineralisation was 4.5.3 Wrack mineralisation is largely independent of drift line position moderate to high, macroinvertebrate abundance was intermediate and macroinvertebrate Finally, we hypothesised that N and P mineralisation of wrack was independent of drift line richness and diversity were both high. However, summer is also the season with a high horizontal spatial position, which is what we generally observed in this study. Only for P recreation pressure on sandy beaches (Kelly 2016). Recreation both has a strong direct and mineralisation there was an additional interaction effect between drift line and season, indirect impact on wrack and its associated macroinvertebrate community (e.g. Schlacher and indicating P mineralisation was higher in old drift lines in spring, while the opposite was the Thompson 2012, McLachlan et al. 2013). Therefore, an integrated approach for coastal case for summer and autumn with a higher P mineralisation in young drift lines. This management of sandy beaches is necessary to facilitate wrack mineralisation and support the interaction effect may be explained by variation in the distance of the chosen drift lines to the sandy beach ecosystem, by mitigating anthropogenic disturbance to wrack and its high water in this study across seasons, which was dependent on stochastic variation in drift macroinvertebrate communities on sandy beaches as much as possible. line formation within each season. Again, it then remains unclear why N and P mineralisation 4.5.5 Conclusion showed a different response. This cannot be related to the macroinvertebrate community: even though macroinvertebrate abundance showed an interaction between drift line and On sandy beaches that accumulate wrack, both season and the macroinvertebrate season, the pattern for macroinvertebrate abundance was dissimilar from that of P community, especially its abundance, were found to play a crucial role in nutrient cycling. This mineralisation. may result in nutrient hot spots on the sandy beach, supporting beach pioneer plant growth and enhanced vegetation cover and diversity (Del Vecchio et al. 2013, Del Vecchio et al. 2017). By using the same fresh wrack in both young and old drift lines, our research allowed to Our study also highlights that wrack decomposition and mineralisation on sandy beaches is a decouple the effects of wrack decay stage and environment on decomposition and complex process, with many interacting drivers. The fate of wrack and its reciprocal relation mineralisation. Previous studies focussed on naturally decomposing wrack across the sandy with the macroinvertebrate community composition in particular, therefore requires to be beach, where young and old wrack were directly compared with each other. For example, studied in more detail to support the sandy beach ecosystem and its management as a whole. Dugan et al. (2011) found that N and P concentrations in beach sand differed with position across the beach, with the highest concentration of nutrients observed around the high water line where fresh wrack accumulated. Until now it was, however, unclear whether this was due to wrack decay stage or environmental conditions. Even so, differences in wrack carbon and nutrient dynamics are commonly related to environmental conditions: there is a strong

Nutrients mineralisation in wrack 91 responsible for the strong effect of season on N and P mineralisation of wrack. The C/N ratio environmental gradient across the entire sandy beach, combining both the intertidal and of the wrack used varied between seasons. When adding the C/N ratio of wrack to the multiple supratidal zone (McLachlan and Jaramillo 1995, Wood and Bjorndal 2000), where the higher regression models, C/N ratio was a strong predictor of N and P mineralisation in addition to supratidal zone is relatively stable in terms of the abiotic environment compared to the season (for P mineralisation only) and macroinvertebrate community metrics (see Appendix, intertidal zone. Wrack in older drift lines higher up the beach has consistently higher Table A4.4). Indeed, the N content of wrack is one of the potential drivers of wrack decay on temperatures and lower moisture contents than fresh wrack in young drift lines around the sandy beaches (Jędrzejczak 2002a). In conclusion, N and P mineralisation of wrack was high water line (Ruiz-Delgado et al. 2015). Moreover, wrack (and its associated strongly determined by season, which was due to both seasonal differences in weather macroinvertebrate community) close to the dune foot is less prone to rewetting by tidal conditions and the initial wrack quality used. inundation, redistribution across the beach by waves and wind, and inundation of macroinvertebrate colonisers (Wood and Bjorndal 2000, Defeo and Gómez 2005, Coupland et Jędrzejczak (2002a) proposes that the order of importance for factors affecting wrack decay al. 2007). Despite these apparent environmental differences, our results suggest that instead rate are type of wrack (i.e. macroalgae species), temperature, internal N content of wrack and differences in wrack decay stage are the dominant driver of differences in wrack decomposer activity. Similarly, in terrestrial ecosystems, temperature and plant growth form decomposition between drift lines. Macroinvertebrate abundance was similar between drift composition are identified as most important drivers of decomposition, with a smaller role for lines, possibly because species are mobile, allowing them to easily migrate between wrack litter quality within species (e.g. Cornelissen et al. 2007). In addition, climate is considered to patches deposited across the sandy beach (Colombini et al. 2000). It thus seems that the stable be a dominant driver of decomposition over macrodetritivores (García-Palacios et al. 2013), macroinvertebrate community and a high degree of migration of supratidal which may be even more pronounced on sandy beaches as they are classically viewed as being macroinvertebrate species across the supratidal zone of the sandy beach may have caused dominated by the environment (McLachlan and Brown 2006). Our results indicate that season wrack mineralisation to be largely independent from drift line position. was the main driver of N and P mineralisation followed by macroinvertebrate abundance, 4.5.4 Implications for coastal management supporting the above hypothesis on the order of importance of factors influencing mineralisation of wrack. In light of coastal management, our study stresses the importance of leaving wrack undisturbed on sandy beaches, especially in summer. In summer, wrack mineralisation was 4.5.3 Wrack mineralisation is largely independent of drift line position moderate to high, macroinvertebrate abundance was intermediate and macroinvertebrate Finally, we hypothesised that N and P mineralisation of wrack was independent of drift line richness and diversity were both high. However, summer is also the season with a high horizontal spatial position, which is what we generally observed in this study. Only for P recreation pressure on sandy beaches (Kelly 2016). Recreation both has a strong direct and mineralisation there was an additional interaction effect between drift line and season, indirect impact on wrack and its associated macroinvertebrate community (e.g. Schlacher and indicating P mineralisation was higher in old drift lines in spring, while the opposite was the Thompson 2012, McLachlan et al. 2013). Therefore, an integrated approach for coastal case for summer and autumn with a higher P mineralisation in young drift lines. This management of sandy beaches is necessary to facilitate wrack mineralisation and support the interaction effect may be explained by variation in the distance of the chosen drift lines to the sandy beach ecosystem, by mitigating anthropogenic disturbance to wrack and its high water in this study across seasons, which was dependent on stochastic variation in drift macroinvertebrate communities on sandy beaches as much as possible. line formation within each season. Again, it then remains unclear why N and P mineralisation 4.5.5 Conclusion showed a different response. This cannot be related to the macroinvertebrate community: even though macroinvertebrate abundance showed an interaction between drift line and On sandy beaches that accumulate wrack, both season and the macroinvertebrate season, the pattern for macroinvertebrate abundance was dissimilar from that of P community, especially its abundance, were found to play a crucial role in nutrient cycling. This mineralisation. may result in nutrient hot spots on the sandy beach, supporting beach pioneer plant growth and enhanced vegetation cover and diversity (Del Vecchio et al. 2013, Del Vecchio et al. 2017). By using the same fresh wrack in both young and old drift lines, our research allowed to Our study also highlights that wrack decomposition and mineralisation on sandy beaches is a decouple the effects of wrack decay stage and environment on decomposition and complex process, with many interacting drivers. The fate of wrack and its reciprocal relation mineralisation. Previous studies focussed on naturally decomposing wrack across the sandy with the macroinvertebrate community composition in particular, therefore requires to be beach, where young and old wrack were directly compared with each other. For example, studied in more detail to support the sandy beach ecosystem and its management as a whole. Dugan et al. (2011) found that N and P concentrations in beach sand differed with position across the beach, with the highest concentration of nutrients observed around the high water line where fresh wrack accumulated. Until now it was, however, unclear whether this was due to wrack decay stage or environmental conditions. Even so, differences in wrack carbon and nutrient dynamics are commonly related to environmental conditions: there is a strong

92 Chapter 4

4.6 Appendix 4.6.2 Full multiple regression model 4.6.1 Macroinvertebrate species and counts A multiple regression model to test the effect of drift line, season and macroinvertebrate community metrics (abundance, richness and diversity) on N and P mineralisation of wrack Litter bags filled with Ulva lactuca Linnaeus were harvested after two weeks of incubation on was performed. When including all interactions within the multiple regression models, the a sandy beach and upon inspection, we found 18 macroinvertebrate taxa and 5777 same patterns were observed as when only the interaction effect of season and drift line was macroinvertebrate individuals in total (Table A4.1). The two most common taxonomic groups included (Table 4.3), except for an additional significant positive effect on P mineralisation by belonged to the Diptera, where Fucellia sp. larvae and Coelops sp. larvae were most abundant the interaction between abundance and drift line in the model including abundance (Table (4624 and 814 individuals, respectively), formed the largest part of the total number of A4.2 and A4.3). individuals (80.04 and 14.09 %, respectively) and they were widely present among the total number of litter bags (81.97 and 39.34 %, respectively; Table A4.1). 4.6.3 Dissecting the effect of season Table A4.1. Macroinvertebrate species and their total number of individuals, percentage of the total Large differences were recorded in C/N ratio between seasons (data not shown), but it was number of individuals and their presence across litter bags, for all litter bags combined. unclear whether season affected the C/N ratio of wrack at harvest via seasonal weather Taxonomic group Total number % of total number Present in x % of conditions or differences in initial wrack quality. When adding the C/N ratio of wrack at harvest of individuals of individuals the litter bags to the multiple regression model, the C/N ratio was significantly related in each model to N Crustacea and P mineralisation (Table A4.4). Season, however, only significantly affected P Talitrus saltator (Talitridae) 2 0.03 3.28 Table A4.2. Results of multiple regression analysis for the relationship between N mineralisation and macroinvertebrate community (implemented as either abundance (log-transformed), richness or Coleoptera Shannon’s diversity), drift line and season. N mineralisation was the dependent variables in these Dyschirius sp. (Carabidae) 18 0.31 14.75 models (Y in the model Y ~ X). In each model, all interactions were included. An asterix indicates a Bledius sp. (Staphylinidae) 18 0.31 16.39 significant p-value (<0.05). Staphylinidae 5 0.09 8.20 Scarabaeidae (most likely Aegialia arenaria) 1 0.02 1.64 df F p Coleoptera adult 2 0.03 3.28 Abundance Overall fit: R2=0.57, p <0.001 * Abundance 1 27.1 <0.001 * Coleoptera larvae 2 0.03 3.28 Drift line 1 0.4 0.51 Season 2 29.7 <0.001* Diptera Abundance * Drift line 1 0.3 0.60 Fucellia sp. larvae (Anthomyiidae) 4624 80.04 81.97 Abundance * Season 2 0.2 0.86 Coelops sp. larvae (Coelopidae) 814 14.09 39.34 Drift line * Season 2 0.5 0.63 Lonchaeidae larvae 3 0.05 1.64 Abundance * Drift line * Season 2 0.4 0.69 Diptera larvae undetermined 1 82 1.42 9.84 Richness Overall fit: R2=0.58, p <0.001 * Richness 1 2.2 0.14 Diptera larvae undetermined 2 186 3.22 11.48 Drift line 1 0.0 0.84 Scatophagidae 3 0.05 3.28 Season 2 43.4 <0.001* Canacidae 3 0.05 4.92 Richness * Drift line 1 1.2 0.28 Chironomidae 10 0.17 14.75 Richness * Season 2 0.4 0.70 Bibionidae 1 0.02 1.64 Drift line * Season 2 0.3 0.74

Hemiptera Richness * Drift line * Season 2 0.7 0.48 2 Aphididae 2 0.03 3.28 Diversity Overall fit: R =0.57, p <0.001 * Diversity 1 1.8 0.19 Drift line 1 0.0 0.94 Hymenoptera Season 2 42.7 <0.001* Formicidae (most likely Lasius psammophilus) 1 0.02 1.64 Diversity * Drift line 1 0.4 0.52 All taxa (18 taxa in total) 5777 Diversity * Season 2 0.5 0.62 Drift line * Season 2 0.3 0.77 Diversity * Drift line * Season 2 0.5 0.60

Nutrients mineralisation in wrack 93

94 Chapter 4

Table A4.3. Results of multiple regression analysis for the relationship between P mineralisation and Table A4.4. Results of multiple regression analysis for the relationship between N and P mineralisation macroinvertebrate community (implemented as either abundance (log-transformed), richness or and macroinvertebrate community (implemented as either abundance (log-transformed), richness or Shannon’s diversity), drift line and season. P mineralisation was the dependent variables in these Shannon’s diversity), C/N ratio, drift line and season. N and P mineralisation were the dependent models (Y in the model Y ~ X). In each model, all interactions were included. An asterix indicates a variables in these models (Y in the model Y ~ X). In each model, the interaction between drift line and significant p-value (<0.05). season was included. An asterix indicates a significant p-value (<0.05), while an open circle indicates a trend (p<0.10). df F p Abundance Overall fit: R2=0.89, p <0.001 * Abundance 1 171.0 <0.001 * df F p Drift line 1 0.4 0.56 N mineralisation Season 2 146.9 <0.001* Abundance Overall fit: R2=0.60, p <0.001* Abundance 1 28.9 <0.001 * Abundance * Drift line 1 4.8 0.03 * C/N ratio 1 59.3 <0.001 * Abundance * Season 2 1.5 0.24 Drift line 1 0.6 0.46 Drift line * Season 2 4.9 0.01 * Season 2 2.3 0.11 Abundance * Drift line * Season 2 0.1 0.89 Drift line * Season 2 0.5 0.58 Richness Overall fit: R2=0.88, p <0.001 * Richness 1 13.6 <0.001 * Richness Overall fit: R2=0.59, p <0.001* Richness 1 2.3 0.14 Drift line 1 0.0 0.96 C/N ratio 1 83.3 <0.001 * Season 2 202.9 <0.001* Drift line 1 0.5 0.48 Richness * Drift line 1 1.6 0.22 Season 2 2.9 0.06 ° Richness * Season 2 0.0 0.97 Drift line * Season 2 0.3 0.76 Drift line * Season 2 4.7 0.01 * Diversity Overall fit: R2=0.59, p <0.001* Diversity 1 1.9 0.18 Richness * Drift line * Season 2 0.3 0.72 C/N ratio 1 83.7 <0.001* Diversity Overall fit: R2=0.88, p <0.001 * Diversity 1 37.4 <0.001 * Drift line 1 0.6 0.45 Drift line 1 0.8 0.38 Season 2 2.9 0.06 ° Season 2 199.2 <0.001* Drift line * Season 2 0.3 0.77 Diversity * Drift line 1 1.2 0.28 P mineralisation Diversity * Season 2 0.7 0.49 Abundance Overall fit: R2=0.89, p <0.001* Abundance 1 167.5 <0.001 * Drift line * Season 2 5.5 <0.01 * C/N ratio 1 156.0 <0.001 * Diversity * Drift line * Season 2 0.2 0.82 Drift line 1 0.5 0.49 Season 2 67.9 <0.001 * mineralisation and with a much smaller magnitude than C/N ratio (Table A4.4). This suggests Drift line * Season 2 4.1 0.02 * that the strong effect of season (in the models without the C/N ratio, Table 4.3), originates Richness Overall fit: R2=0.89, p <0.001* Richness 1 14.5 <0.001 * from both seasonal weather conditions and initial differences in wrack quality. C/N ratio 1 326.1 <0.001 * Drift line 1 1.1 0.29

Season 2 54.3 <0.001 *

Drift line * Season 2 4.1 0.02 * Diversity Overall fit: R2=0.89, p <0.001* Diversity 1 39.2 <0.001 * C/N ratio 1 346.9 <0.001 * Drift line 1 5.3 0.02 * Season 2 35.1 <0.001 * Drift line * Season 2 4.7 0.01 *

Nutrients mineralisation in wrack 95

Season 2 54.3 <0.001 *

96 Chapter 4

4.6.4 Scatter plots of macroinvertebrate community metrics against N and P mineralisation A B

A B

C C

Figure A4.2. Scatterplot of A) abundance, B) richness and C) Shannon’s diversity against P mineralisation. Shapes of points indicate drift line and colours of points indicate season. Each point Figure A4.1. Scatterplot of A) abundance, B) richness and C) Shannon’s diversity against N represents one litter bag. mineralisation. Shapes of points indicate drift line and colours of points indicate season. Each point represents one litter bag.

Nutrients mineralisation in wrack 97

4.6.4 Scatter plots of macroinvertebrate community metrics against N and P mineralisation A B

A B

C C

Chapter 5

Growth of pioneer beach plants is strongly driven by buried macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman, Matty, P. Berg and Rien Aerts

Chapter 5

Growth of pioneer beach plants is strongly driven by buried macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman, Matty, P. Berg and Rien Aerts

This chapter has been submitted for publication

Chapter 5

Growth of pioneer beach plants is strongly driven by buried macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman, Matty, P. Berg and Rien Aerts

Chapter 5

Growth of pioneer beach plants is strongly driven by buried macroalgal wrack, while macroinvertebrates affected plant nutrient dynamics

Emily M. van Egmond, Peter M. van Bodegom, Jurgen R. van Hal, Richard S.P. van Logtestijn, Rob A. Broekman, Matty, P. Berg and Rien Aerts

This chapter has been submitted for publication

100 Chapter 5

5.1 Abstract and geomorphology (Orr et al. 2005). Moreover, the location of wrack on the beach, i.e. the distance to the mean sea level isocline, is strongly determined by tidal amplitudes which Sandy beaches depend heavily upon marine organic input, such as macroalgae, as internal change monthly to annually (e.g. Plag and Tsimplis 1999) resulting in several drift lines parallel organic matter productivity is low. The fate, however, of this marine organic material after to the water line. The initial quality of freshly deposited wrack depends on the identity of the being deposited onto the beach (termed wrack) and its impact on pioneer vegetation needs sea grass or sea weed species and their anatomical, physiological and chemical traits at the to be further elucidated. In particular, the effect of various drivers of wrack decomposition moment of detachment and transportation (Oldham et al. 2014), as well as on the relative and nutrient mineralisation on pioneer vegetation growth at sandy beaches are largely contribution of carrion in the wrack. This finally results in a spatiotemporal diverse drift line unknown. We studied the effect of wrack burial and macroinvertebrate presence on composition at the sandy beach. As the internal primary production of sandy beaches is very decomposition-driven nutrient availability and beach pioneer plant growth. To this end, we low and the ecosystem is generally bottom-up controlled (Schlacher and Hartwig 2013), the performed a mesocosm experiment manipulating Fucus vesiculosus wrack access to the input and subsequent pathway of wrack-bound energy and nutrients is crucial to the supratidal amphipod Talitrus saltator, and used Cakile maritima and Elytrigia juncea as functioning of the sandy beaches. Therefore, understanding the fate of marine-derived organic matter that enters the sandy beach is key for understanding its ecosystem functioning. phytometers to estimate wrack-derived nutrient supply. Buried wrack had a strong positive effect (2-3 times greater) on plant mass, N and P content of C. maritima compared to surface Once wrack is stranded on the beach, this material decays and decomposes through a variety wrack, while effects on E. juncea were largely absent. In addition, macroinvertebrate- of abiotic and biotic processes (Colombini and Chelazzi 2003). Abiotic processes that work on facilitated decomposition was important for increasing nutrient availability, but this did not freshly deposited wrack resulting in its degradation include photodegradation, erosion by result in an increase in plant growth. We conclude that the burial of wrack by a thin layer of wind-blown sand and coverage of wrack by a layer of sand. Over time, wrack in drift lines sand is a crucial driver of beach pioneer plant growth primarily due to an increase in sediment higher up the beach generally becomes buried by sand through aeolian transportation and moisture content. This supports the importance of management practices that allow other natural processes, where it locally enhances organic matter content and changes the deposited wrack to remain and be buried on the sandy beach for a long period of time, which physical structure of the sand, which is especially relevant in sandy beaches (Rossi and Underwood 2002). The aging and burial of wrack change the microclimate and habitat will have positive effects on beach pioneer plant growth and possibly embryo dune formation. properties for microbial decomposers and macroinvertebrates, making wrack an ephemeral 5.2 Introduction but stabilised habitat in terms of temperature and moisture content for supratidal macroinvertebrates (Ince et al. 2007, Ruiz-Delgado et al. 2015). An important biotic process Ecosystems are open entities, thus adjacent ecosystems typically exchange organic matter and influencing wrack decomposition is the swift colonisation of wrack by microbes and nutrients between them (Polis et al. 1997, Marcarelli et al. 2011). In low productive invertebrates, after which a succession of species starts (Olabarria et al. 2007). As the volume ecosystems, such as sandy beaches, exogenous dead organic matter and nutrients are and quality of wrack alter over time, changes in macroinvertebrate abundance, richness and transferred through detritus in the receiving ecosystem (Polis and Hurd 1996). In addition, community composition occur (Jędrzejczak 2002b, Olabarria et al. 2007). Macroinvertebrates ecosystem boundaries are continually crossed by organisms, where biologically possible that feed on wrack, and its associated biofilm (Porri et al. 2011), fragment the organic material (Nakano and Murakami 2001, Barrett et al. 2005). Coastal ecosystems are unique in the sense (Salathé and Riera 2012). By decreasing wrack particle size and mixing of bacteria and fungi that they provide an interface, linking terrestrial and marine ecosystems across the world with organic matter through feeding, the surface area for microbial activity increases and (Heck et al. 2008). These ecosystems perform a wide range of important ecosystem functions, decomposition is stimulated (Robertson and Mann 1980, Colombini and Chelazzi 2003). Also, such as nutrient cycling and the buffering of wave energy (McLachlan and Brown 2006). In the burrowing activities of some macroinvertebrates incorporate wrack fragments within the particular on sandy beaches, which form a unique ecosystem of its own (McLachlan 1980), sand, stimulating an increase in decomposition, due to enhanced activity of decomposers by terrestrial and marine habitats heavily interact. more favourable abiotic conditions (Inglis 1989). All these (a)biotic processes potentially affect Sandy beaches receive large amounts of marine exogenous organic matter that has been the decomposition of wrack and the release of organically-bound nutrients, but how these are produced by primary and secondary producers, and are therefore considered to be primarily interacting remains largely unknown. Specifically, the relationship between natural sand recipient ecosystems (Liebowitz et al. 2016). Sea grasses and sea weeds are important primary burial of wrack and macroinvertebrate-facilitated decomposition has not been previously producers that grow attached to a (rocky) substratum, but become detached as a result of studied. severe hydrodynamic conditions and are consequently deposited onto the beach (Suursaar et During and after the processing of organic material by detritivores, nutrients may flow back al. 2014). Drift lines mainly contain stranded sea grasses and sea weeds (collectively termed to the sea to support marine primary production (McLachlan 1980, Dugan et al. 2011) or wrack), but may also include other organic components, such as carrion or faeces (Colombini create nutrient hot spots and locally support terrestrial primary (Hemminga and and Chelazzi 2003). Wrack supply to the beach is highly variable in time and space and is driven Nieuwenhuize 1990, Del Vecchio et al. 2013) and secondary production (Polis and Hurd 1996, by, among others, the buoyancy capacity of the wrack, hydrodynamic forces and beach type Schlacher et al. 2017). As sandy beach communities are considered to depend more heavily

Growth of pioneer beach plants 101

102 Chapter 5 on marine subsidies than vice versa (Liebowitz et al. 2016), our focus in this study was on the the stipe, ± 2 cm above the holdfast and stored in a plastic bucket. Directly after collection, F. role of macroinvertebrate-facilitated decomposition of wrack on terrestrial plant growth. The vesiculosus was spread out on tables in the laboratory to dry at room temperature (20 °C) for supratidal zone provides adverse conditions for most plant species due to among others high three days and stored in a dry place until the start of the experiment. salinity, low moisture content and low nutrient availability of the sandy sediment (Pakeman 5.3.2 Animal collection and Lee 1991a). Wrack patches, however, are a unique micro-habitat for beach pioneer plants and an important nutrient and habitat source for animals within sandy beaches (Williams and The litter-feeding terrestrial amphipod Talitrus saltator is a common inhabitant of wrack on Feagin 2010, Del Vecchio et al. 2013). Indeed, beach pioneer plants benefit in terms of growth Dutch sandy beaches (see e.g. Van Colen et al. 2006). We collected T. saltator individuals from from a pulse in nutrient availability, especially nitrogen (Pakeman and Lee 1991b). However, the beach near Scheveningen, the Netherlands (52.05 N, 4.19 E) not more than two weeks the role of abiotic (burial by sand) and biotic (macroinvertebrate activity) factors, influencing before the start of the experiment. Animals were collected from bare sand in the intertidal wrack decomposition and nutrient availability, for beach pioneer plant growth needs to be zone with visible holes (entrance to burrows of T. saltator) and from fresh wrack patches further experimentally tested. deposited during receding tide. Sand was sieved over a 1 mm sieve and remaining animals were collected with a pair of soft tweezers. Fresh wrack was gently shaken above a 1 mm sieve Hence, the aims of this study were to test the effects of 1) wrack burial, 2) macroinvertebrate to stir the animals and those fallen onto the sieve were collected with a pair of soft tweezers. presence and 3) their interaction on decomposition-driven nutrient supply and beach pioneer Animals were transported to the laboratory in 1L plastic pots with a 10 cm layer of moist sand plant growth. We hypothesised that 1) buried wrack would have a more positive effect on from the collection site. Upon arrival in the laboratory the same day, collected animals were decomposition-driven nutrient supply and beach pioneer plant growth than wrack on the transferred to a terrarium filled with a 8-10 cm thick layer of quartz sand (Multiquartz, surface, as buried wrack has a higher moisture content and can more easily be decomposed. Lelystad, the Netherlands). Sand had a 0.25-0.40 mm grain size and was free from organic We further hypothesised that 2) macroinvertebrate presence would have a positive effect on matter by burning. The terrarium was finally covered with mesh (<0.5 mm mesh size) and decomposition-driven nutrient supply and beach pioneer plant growth. The common placed in a climate room (12:12 h light/dark regime, 20:15 °C day/night temperature regime terrestrial amphipod Talitrus saltator (Monatagu, 1808) used in this experiment was expected and an 85:75 % RH day/night air humidity). Freshly-cut F. vesiculosus sea weed was added ad to play an important role in decomposition by feeding on and thereby fragmenting the wrack libitum as a food source and ± 20 mL demi-water was sprayed every other day to keep the and by burrowing wrack fragments. As the wrack decomposes, more nutrients become environment moist. The last 24 h before the start of the experiment all sea weed was removed available in the sand below the wrack. This in turn is expected to enhance pioneer beach plant to starve the animals and to empty their guts. growth as nutrient-limitation for beach plant growth is removed when growing in a drift line. Finally, we hypothesised 3) there is an interaction effect between wrack burial and 5.3.3 Plant cultivation macroinvertebrate presence on decomposition-driven nutrient supply and beach pioneer We used two common pioneer plant species of Dutch sandy beaches: Cakile maritima and plant growth. We expected that wrack on the surface would be less palatable to T. saltator as Elytrigia juncea (see e.g. Speybroeck et al. 2008a, Doing 1995). Cakile maritima is an annual it holds less moisture (see Ruiz-Delgado et al. 2015) and a lower microbial biomass, hence forb that typically grows on buried wrack lines (Davy et al. 2006), while E. juncea is a perennial food, and thus negatively impacts the facilitation by macroinvertebrates of decomposition and grass that can be found at the dune foot and initiates embryo dune formation by capturing subsequent beach pioneer plant growth. sand, or within stabilised stands of C. maritima (Speybroeck et al. 2008a, Davy et al. 2006). 5.3 Methods Cakile maritima seeds were collected by hand at the beach near Scheveningen, the Netherlands (52.05 N, 4.19 E) in November 2014 and December 2015, after which they were To test the effect of macroinvertebrate presence and wrack burial on wrack decomposition stored cool (5 °C) and dark upon arrival in the laboratory until sowing commenced. We grew and beach pioneer plant growth, we conducted a climate room experiment for which we C. maritima plants from these seeds five weeks before the start of the experiment. Seeds were assembled mesocosms consisting of pots of sand with different combinations of wrack burial, removed from their fruits and, after soaking for 2 hours in demi-water, five seeds were macroinvertebrate presence and plant species. randomly placed in a Petri-dish lined with filter paper moistened with demi-water (5-10 mL) 5.3.1 Wrack collection and preparation until saturated. Petri-dishes were placed in a climate room (see above for conditions) and covered with plastic trays to allow germination in the dark. Every two days we gently We used the brown sea weed Fucus vesiculosus as wrack, as it is a major component of wrack transferred seedlings with a pair of soft tweezers to small pots (diameter 8 cm, height 7 cm) found upon Dutch sandy beaches (personal observation; see also Nienhuis 1970). It is a filled with a 6-cm layer of quartz sand (same sand as used as above), placed on a saucer preferential food source for the supratidal amphipod Talitrus saltator (Lastra et al. 2008), (diameter 12.5 cm, height 2 cm) to catch remaining water added to the pot. Seedlings were which is used in this experiment as macroinvertebrate species (see below). Fresh F. vesiculosus watered once a week with 50 mL half-strength Hoagland solution (3mM KNO , 2 mM Ca(NO ), was collected from the rocky pier near IJmuiden, the Netherlands (52.46 N, 4.55 E) during low 3 3 1 mM NH H PO , 0.5 mM MgSO , 25 µM H BO , 1 µM KCl, 2 µM MnSO , 2 µM ZnSO , 0.1 µM tide, two weeks prior to the experiment. Sea weeds were cut loose with a pair of scissors at 4 2 4 4 3 3 4 4

Growth of pioneer beach plants 103 on marine subsidies than vice versa (Liebowitz et al. 2016), our focus in this study was on the the stipe, ± 2 cm above the holdfast and stored in a plastic bucket. Directly after collection, F. role of macroinvertebrate-facilitated decomposition of wrack on terrestrial plant growth. The vesiculosus was spread out on tables in the laboratory to dry at room temperature (20 °C) for supratidal zone provides adverse conditions for most plant species due to among others high three days and stored in a dry place until the start of the experiment. salinity, low moisture content and low nutrient availability of the sandy sediment (Pakeman 5.3.2 Animal collection and Lee 1991a). Wrack patches, however, are a unique micro-habitat for beach pioneer plants and an important nutrient and habitat source for animals within sandy beaches (Williams and The litter-feeding terrestrial amphipod Talitrus saltator is a common inhabitant of wrack on Feagin 2010, Del Vecchio et al. 2013). Indeed, beach pioneer plants benefit in terms of growth Dutch sandy beaches (see e.g. Van Colen et al. 2006). We collected T. saltator individuals from from a pulse in nutrient availability, especially nitrogen (Pakeman and Lee 1991b). However, the beach near Scheveningen, the Netherlands (52.05 N, 4.19 E) not more than two weeks the role of abiotic (burial by sand) and biotic (macroinvertebrate activity) factors, influencing before the start of the experiment. Animals were collected from bare sand in the intertidal wrack decomposition and nutrient availability, for beach pioneer plant growth needs to be zone with visible holes (entrance to burrows of T. saltator) and from fresh wrack patches further experimentally tested. deposited during receding tide. Sand was sieved over a 1 mm sieve and remaining animals were collected with a pair of soft tweezers. Fresh wrack was gently shaken above a 1 mm sieve Hence, the aims of this study were to test the effects of 1) wrack burial, 2) macroinvertebrate to stir the animals and those fallen onto the sieve were collected with a pair of soft tweezers. presence and 3) their interaction on decomposition-driven nutrient supply and beach pioneer Animals were transported to the laboratory in 1L plastic pots with a 10 cm layer of moist sand plant growth. We hypothesised that 1) buried wrack would have a more positive effect on from the collection site. Upon arrival in the laboratory the same day, collected animals were decomposition-driven nutrient supply and beach pioneer plant growth than wrack on the transferred to a terrarium filled with a 8-10 cm thick layer of quartz sand (Multiquartz, surface, as buried wrack has a higher moisture content and can more easily be decomposed. Lelystad, the Netherlands). Sand had a 0.25-0.40 mm grain size and was free from organic We further hypothesised that 2) macroinvertebrate presence would have a positive effect on matter by burning. The terrarium was finally covered with mesh (<0.5 mm mesh size) and decomposition-driven nutrient supply and beach pioneer plant growth. The common placed in a climate room (12:12 h light/dark regime, 20:15 °C day/night temperature regime terrestrial amphipod Talitrus saltator (Monatagu, 1808) used in this experiment was expected and an 85:75 % RH day/night air humidity). Freshly-cut F. vesiculosus sea weed was added ad to play an important role in decomposition by feeding on and thereby fragmenting the wrack libitum as a food source and ± 20 mL demi-water was sprayed every other day to keep the and by burrowing wrack fragments. As the wrack decomposes, more nutrients become environment moist. The last 24 h before the start of the experiment all sea weed was removed available in the sand below the wrack. This in turn is expected to enhance pioneer beach plant to starve the animals and to empty their guts. growth as nutrient-limitation for beach plant growth is removed when growing in a drift line. Finally, we hypothesised 3) there is an interaction effect between wrack burial and 5.3.3 Plant cultivation macroinvertebrate presence on decomposition-driven nutrient supply and beach pioneer We used two common pioneer plant species of Dutch sandy beaches: Cakile maritima and plant growth. We expected that wrack on the surface would be less palatable to T. saltator as Elytrigia juncea (see e.g. Speybroeck et al. 2008a, Doing 1995). Cakile maritima is an annual it holds less moisture (see Ruiz-Delgado et al. 2015) and a lower microbial biomass, hence forb that typically grows on buried wrack lines (Davy et al. 2006), while E. juncea is a perennial food, and thus negatively impacts the facilitation by macroinvertebrates of decomposition and grass that can be found at the dune foot and initiates embryo dune formation by capturing subsequent beach pioneer plant growth. sand, or within stabilised stands of C. maritima (Speybroeck et al. 2008a, Davy et al. 2006). 5.3 Methods Cakile maritima seeds were collected by hand at the beach near Scheveningen, the Netherlands (52.05 N, 4.19 E) in November 2014 and December 2015, after which they were To test the effect of macroinvertebrate presence and wrack burial on wrack decomposition stored cool (5 °C) and dark upon arrival in the laboratory until sowing commenced. We grew and beach pioneer plant growth, we conducted a climate room experiment for which we C. maritima plants from these seeds five weeks before the start of the experiment. Seeds were assembled mesocosms consisting of pots of sand with different combinations of wrack burial, removed from their fruits and, after soaking for 2 hours in demi-water, five seeds were macroinvertebrate presence and plant species. randomly placed in a Petri-dish lined with filter paper moistened with demi-water (5-10 mL) 5.3.1 Wrack collection and preparation until saturated. Petri-dishes were placed in a climate room (see above for conditions) and covered with plastic trays to allow germination in the dark. Every two days we gently We used the brown sea weed Fucus vesiculosus as wrack, as it is a major component of wrack transferred seedlings with a pair of soft tweezers to small pots (diameter 8 cm, height 7 cm) found upon Dutch sandy beaches (personal observation; see also Nienhuis 1970). It is a filled with a 6-cm layer of quartz sand (same sand as used as above), placed on a saucer preferential food source for the supratidal amphipod Talitrus saltator (Lastra et al. 2008), (diameter 12.5 cm, height 2 cm) to catch remaining water added to the pot. Seedlings were which is used in this experiment as macroinvertebrate species (see below). Fresh F. vesiculosus watered once a week with 50 mL half-strength Hoagland solution (3mM KNO , 2 mM Ca(NO ), was collected from the rocky pier near IJmuiden, the Netherlands (52.46 N, 4.55 E) during low 3 3 1 mM NH H PO , 0.5 mM MgSO , 25 µM H BO , 1 µM KCl, 2 µM MnSO , 2 µM ZnSO , 0.1 µM tide, two weeks prior to the experiment. Sea weeds were cut loose with a pair of scissors at 4 2 4 4 3 3 4 4

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-2 CuSO4, 0.1 µM (NH4)6Mo7O24 and 10 µM Fe(Na)EDTA) and once a week with 50-100 mL demi- fresh biomass or 52 individuals m ) corresponding to field densities encountered in wrack (19 water, depending on the size of the plants, until the start of the experiment. ± 24 individuals m-2 (Bessa et al. 2014b); 91 ± 18 individuals m-2 (Ruiz-Delgado et al. 2016)). Females with brood sacks were omitted from the mesocosms. Animals were placed on top of As we were insufficiently successful in growing E. juncea seedlings from root stocks collected the sand, after which most of them started burying themselves into the sand. Each mesocosm in the field, we collected mature E. juncea plants (with a shoot length of at least 20 cm) instead contained either one C. maritima or E. juncea plant. All mesocosms were covered with a nylon and used these directly in the experiment. Approximately 100 E. juncea plants were collected mesh (mesh size 0.5 mm) secured by tape on the pot edges, with a hole (square of 1 cm2) to 7 days before the start of the experiment on the beach ‘De Hors’, Texel, the Netherlands allow the stem of the plant to pass while keeping the animals in the mesocosms. A piece of (53.00 N, 4.74 E) and were, upon arrival in the laboratory, placed in a plastic bucket (diameter white nylon wool (Pond Filter Wool, VT, Velda Group, the Netherlands) was wrapped around 34 cm, height 26 cm) with a layer of 30 cm quartz sand (same sand as used as above) in the the stem to protect it from the sharp edges of the plastic mesh, and to prevent animals from climate room. On the day of collection, 500 mL half-strength Hoagland solution was evenly escaping. All mesocosms were placed in a climate room with a 12:12 h light/dark regime (light added to the bucket containing all E. juncea plants. Sand was kept moist by adding 500 mL intensity: 500 µmol m-2 s-1; lamp type: Philips CDM-TMW 315 W/942), a 20:15 °C day/night demi-water every other day until the start of the experiment. As we collected more E. juncea temperature regime and an 85:75 % RH day/night air humidity. These circumstances plants than necessary, we randomly selected 47 individuals to be used in the experiment. correspond to late spring/early summer conditions in the Netherlands. The bottom of the 5.3.4 Experimental design mesocosms was lined with tightly woven plastic root canvas, which allowed water and solutes to pass but kept all other material inside the mesocosm. All mesocosms were placed on a We used a 2-way design to study the effect of wrack burial (surface or buried) and saucer to collect leaching water after watering mesocosms. macroinvertebrates (present or absent) on the growth of two individual beach pioneer plant species (C. maritima and E. juncea). For each treatment we had eight replicates, which were 5.3.5 Additions prior to and during the experiment divided over eight blocks (Table 5.1). In addition, we performed a nutrient addition test to The day before the start of the experiment, each mesocosm received 250 mL demi-water and determine if a potential positive effect of wrack addition on plant growth could be related to 50 mL 50 mM NaCl to ensure equal starting conditions in moisture and salt content. A low salt nutrient limitation. For this purpose, we used three treatments for both C. maritima and E. content has a positive effect on beach pioneer plant growth (Lee and Ignaciuk 1985, Debez et juncea: nutrient addition, inoculum addition and no nutrient addition (plant only). An al. 2004). Wrack inoculum was prepared by adding 3.7 kg of freshly collected Fucus vesiculosus inoculum addition treatment was included to account for the effect of indirectly adding extra wrack to 3.5 L demi-water. After 3 hours of soaking, the inoculum was strained to remove nutrients in treatments that received wrack and inoculum. For each of these three treatments larger wrack particles (>1mm). All main treatments and the inoculum treatment of the we had five replicates, which were divided over five blocks (Table 5.1). In a climate room, all nutrient addition treatments were given 200 mL demi-water and 50 mL inoculum at the start mesocosms were placed within combined blocks (eight in total). This finally resulted in five of the experiment, while the nutrient addition treatment without inoculum was given 250 mL blocks with fourteen mesocosms (combining main treatments and the nutrient addition test demi-water. All mesocosms received 125 mL demi-water twice a week during the experiment. treatments) and three blocks with eight mesocosms (remaining mesocosms of main The nutrient addition treatments that received nutrient solution instead were watered twice treatments). Blocks and mesocosms within blocks were moved around randomly twice a a week with 125 mL nutrient solution that contained 0.03 g N (0.43 mL of 5 M NH Cl stock week. In total, there were 94 mesocosms and each mesocosm was randomly assigned to one 4 solution) and 0.004 g P (0.13 mL of 1 M NaH2PO4 stock solution). In total, plants in these of the above treatments. treatments received 0.24 g N and 0.03 g P, which is in the same range as the amount of N and Each mesocosm (plastic pot, diameter 14 cm; height: 14 cm) was filled with a 9 cm layer of P available in the amount of wrack added in this experiment. The experiment was run for four quartz sand (same sand as used as above). Each mesocosm assigned to a wrack treatment weeks in June-July 2016. received 14 g of dry F. vesiculosus, which corresponds to a potential nutrient addition (if all nutrients would be released from wrack) of 0.37 g N and 0.05 g P (data not shown). In treatments with surface wrack, this resulted in a 2.5-3 cm thick layer of loosely packed wrack placed on top of the sand, covering the entire surface of the mesocosm. In treatments that contained buried wrack, this resulted in a layer of 2.5-3 cm loosely packed wrack placed on top of the sand and covered with approximately 150 g sand so that the top of the wrack was just visible, with only tiny parts of wrack peeking out at the sand surface (Figure 5.1). Before placing wrack in the mesocosm, 50 mL of wrack inoculum (see below) was added onto the wrack to account for wrack-associated decomposer microorganisms and as food source for Figure 5.1. Graphical representation of the wrack burial treatments in the main experiment, indicating macrodetritivores which may have died-off while air-drying. For those treatments with the depth and material of the layers. macroinvertebrates present, we randomly added eight individuals of T. saltator (± 0.3 g total

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Table 5.1. Summary of the experimental design indicating the mesocosms included for both testing 6 h at 140 °C. Samples were then diluted with 4 ml demineralised water and total P content the main treatments and the nutrient addition test. Within brackets it is indicated how many was measured colorimetrically (Murphy and Riley 1962). To correct for sand trapped between mesocosms were included in the subset excluding mesocosms where no animals were retrieved upon plant roots, a homogenised root subsample was combusted at 550 °C to obtain mass loss on harvest. ignition. Total N concentration was used to determine the total N content of the plants which Main treatments Wrack burial Macroinvertebrates Plant species n Total n can be considered as a measure of total N uptake. Finally, the N/P ratio based on dry mass Surface Present C. maritima 8 (6) upon harvest was calculated to have a measure for the type of nutrient limitation in the plant E. juncea 8 (6) and its organs (see Appendix for results on the N/P ratio). Absent C. maritima 8 (8) E. juncea 8 (8) 5.3.7 Data and statistical analysis Deep Present C. maritima 8 (3) E. juncea 8 (3) First, we analysed the mortality of T. saltator individuals to determine whether observed Absent C. maritima 8 (8) mortality was related to treatments. To test the effect of both wrack (two levels: surface or E. juncea 8 (8) buried) and plant species (two levels: C. maritima and E. juncea) on mortality, a two-way 64 (50) ANOVA was performed. Mortality was higher in buried (90 ± 16%) than in shallow (70 ± 28%) Nutrient addition test Addition Plant species n Total n wrack treatments (ANOVA, df = 1, F = 6.1, p = 0.02). No differences in mortality were found Nutrients C. maritima 5 between plant species (ANOVA, df = 1, F = 1.6, p = 0.21) and there were no interactions E. juncea 5 Inoculum C. maritima 5 between wrack burial and plant species (ANOVA, df = 1, F = 1.2, p = 0.29). Given the large E. juncea 5 number of non-retrieved individuals and the unknown contribution of them to the processes None C. maritima 5 measured (while individuals found dead will at least have contributed to wrack decomposition (control) E. juncea 5 and mineralisation for part of the experimental period), we decided to include only those 30 mesocosms in which macroinvertebrates were retrieved upon harvest, either dead or alive, in further analysis. Exclusion of mesocosms without retrieved animals upon harvest resulted in 5.3.6 Measured variables 18 mesocosms remaining for the macroinvertebrate treatment (n=6 for shallow buried wrack and n=3 for deep buried wrack, for each of the two plant species, see Table 5.1). For a subset of specimens (n=10), we collected the fresh and dry mass (to the nearest 0.001 g) at t=0 for the roots, shoot (E. juncea only), stem (C. maritima only) and leaves (C. maritima We chose to present the absolute final mass, nutrient content and N/P ratio of the different only). We determined the fresh mass of the total plant for all individual plants at the start of plant organs as plants grew large quickly: the relative increase of total plant biomass was on the experiment and we measured fresh weight of wrack for all mesocosms. Upon harvest, we average 317% (± 278%) and 70% (± 101%) for C. maritima and E. juncea, respectively. Biomass collected the fresh and dry mass of the roots, shoot (E. juncea only), stem (C. maritima only), at t=0 was therefore considered small relative to the biomass increase and focussing on the flowering heads (C. maritima only), green leaves (C. maritima only) and (shedded) brown absolute final biomass simplifies both the analysis and interpretation of the results. Prior to leaves (C. maritima only). In addition, we determined the fresh and dry mass of remaining analysis, all data were tested for homogeneity of variances (Levene’s test) and normal wrack and the numbers of T. saltator found dead or alive. For wrack, the moisture content (%) distribution (Shapiro-Wilk test). When these assumptions were not met (main treatments: dry mass (total shoot), P content (total plant, total shoot and roots), N/P ratio (total plant, total at harvest was calculated. Talitrus saltator individuals were considered dead either when we shoot and roots) of C. maritima; dry mass (total plant, total shoot and roots), N content (total found the body of a non-moving individual or did not retrieve the body at all upon harvest, plant, total shoot and roots), P (total shoot), N/P ratio (total plant and roots) of E. juncea; which were taken together to calculate the presumed mortality. Total shoot mass of C. nutrient addition treatments: N content (total shoot) of E. juncea), a log transformation was maritima consisted of the stem, green and brown leaves and flowering head combined. This performed on the original data. To test the effect of both wrack (two levels: surface or buried) distinction was not made for E. juncea plants, which were all in the vegetative stage and and macroinvertebrates (two levels: present or absent) on each of the variables plant mass, N without entire leaves browning. Upon harvest, samples were oven-dried for 72 h at 70 °C. and P content and N/P ratio, a two-way ANOVA was performed for each plant organ (total Dried samples were ground into a fine powder in a ball mill (MM400, Retsch, Haan, Germany) plant, total shoot and roots) and for each plant species (C. maritima and E. juncea), separately. and homogenised by mixing the ground sample with a steel stirrer. Total N concentration of We performed a Kruskal-Wallis test to test the effect of macroinvertebrates (two levels: plant parts were determined by dry combustion with a Flash EA1112 elemental analyser presence or absence) and plant species (two levels: C. maritima and E. juncea) on wrack (Thermo Scientific, Rodana, Italy). For P content, a 50 mg subsample was digested in 1 ml of a moisture percentage separately. To evaluate the nutrient addition treatments (three levels:

1:4 mixture of 37% (by volume) HCl and 65% (by volume) HNO3, in a closed Teflon cylinder for nutrient addition, inoculum addition and plant only) on each of the variables plant dry mass,

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1:4 mixture of 37% (by volume) HCl and 65% (by volume) HNO3, in a closed Teflon cylinder for nutrient addition, inoculum addition and plant only) on each of the variables plant dry mass,

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N and P content and N/P ratio, we performed a one-way ANOVA for each plant organ (total and the total shoot was higher in the presence of macroinvertebrates, while the opposite was plant, total shoot and roots) and for each species, separately. The results of the nutrient the case when wrack was placed on the surface. In the presence of macroinvertebrates, P addition treatments can be found in the Appendix. ANOVAs were followed up with Tukey’s content of C. maritima was 3.1 ± 1.4 mg P against 0.9 ± 0.5 mg P for the total plant, 3.1 ± 1.4 post hoc tests if relevant. All statistical analyses were done in R, version 3.2.3 (R Core Team P mg against 0.9 ± 0.5 mg P for the total shoot and 0.3 ± 0.1 mg P against 0.1 ± 0.1 mg P for 2015). the roots, when wrack was buried or placed on the surface, respectively. In the absence of

5.4 Results 5.4.1 Wrack moisture content Surface-facing wrack had a lower moisture content than buried wrack (61.3 ± 6.4 % and 81.7 A ± 3.3 %, respectively; Kruskal-Wallis test, df = 1, χ2 = 47.3, p < 0.001). There were no significant differences in wrack moisture content between plant species (Kruskal-Wallis test, df = 1, χ2 = 0.27, p = 0.60) or macroinvertebrate treatments (Kruskal-Wallis test, df = 1, χ2 < 0.1, p = 0.98). 5.4.2 Plant biomass For Cakile maritima, wrack burial resulted in a strong and significant increase in the dry mass of the total plant, total shoot and roots (Table 5.2, Figure 5.2). Dry mass was 3.4 ± 1.2 g against

1.7 ± 0.5 g for the total plant, 2.9 ± 1.0 g against 1.5 ± 0.4 g for the total shoot and 0.6 ± 0.2 g against 0.2 ± 0.2 g for the roots, for buried and surface wrack, respectively. Thus, plant dry mass was approximately two times as high when wrack was buried as opposed to surface wrack. No significant effects were found for macroinvertebrate presence on the dry mass of the total plant, total shoot or roots. For Elytrigia juncea, there were no significant differences of either wrack burial or macroinvertebrate presence on the dry mass of either the total plant, total shoot or roots (Table 5.2, Figure 5.2).

5.4.3 Plant nitrogen content B The overall pattern for N content, for both plant species and all plant organs, was highly similar to the pattern of dry mass (Table 5.3, Figure 5.3), except that for C. maritima there was a significant negative effect of macroinvertebrate presence on the N content of the total plant.

This similarity suggests that the biomass increase of C. maritima in the buried wrack treatment was strongly coupled to increased N availability in the soil. When macroinvertebrates were present, the N content of the total plant was lower than when macroinvertebrates were absent, both for buried and surface wrack (buried: 64.2 ± 22.5 mg N against 72.7 ± 12.6 mg N, surface: 24.4 ± 7.5 mg N against 25.2 ± 8.2 mg N, respectively). Moreover, when wrack was buried or placed on the surface, N content of C. maritima was 39.3 ± 9.1 mg N against 14.0 ±

4.2 mg N for the total shoot and 19.5 ± 5.6 mg N against 5.7 ± 3.5 mg N for the roots, respectively. Thus, the N content was approximately three times as high when wrack was buried as opposed to surface wrack.

5.4.4 Plant phosphorus content Figure 5.2. Dry mass of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) The overall pattern for P content, for both plant species and all plant organs, was also highly Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack and similar compared to the pattern of dry mass (Table 5.4, Figure 5.4), except there was an in the presence or absence of the amphipod Talitrus saltator. For buried wrack n=3, while n=6 for interaction effect between wrack burial and macroinvertebrate presence for both the P surface-exposed wrack in the presence of T. saltator. For all other treatment combinations n=8. Error content of the total plant and the total shoot: if wrack was buried, P content of the total plant bars indicate the standard error from the mean.

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110 Chapter 5 macroinvertebrates, P content of C. maritima was 2.1 ± 0.7 mg P against 1.1 ± 0.4 mg P for the total plant, 1.6 ± 0.5 P mg against 1.0 ± 0.4 mg P for the total shoot and 0.4 ± 0.2 mg P against

0.1 ± 0.1 mg P for the roots, when wrack was buried deep or placed on the surface, A respectively. Thus, the P content was approximately two to three times as high when wrack was buried as opposed to surface wrack.

Figure 5.4. P content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack and in the presence or absence of the amphipod Talitrus saltator. For buried wrack n=3, while n=6 for surface-exposed wrack in the presence of T. saltator. For all other treatment combinations n=8. Error bars indicate the standard error from the mean.

Figure 5.3. N content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack and in the presence or absence of the amphipod Talitrus saltator. For buried wrack n=3, while n=6 for surface-exposed wrack in the presence of T. saltator. For all other treatment combinations n=8. Error bars indicate the standard error from the mean.

Growth of pioneer beach plants 111 macroinvertebrates, P content of C. maritima was 2.1 ± 0.7 mg P against 1.1 ± 0.4 mg P for the total plant, 1.6 ± 0.5 P mg against 1.0 ± 0.4 mg P for the total shoot and 0.4 ± 0.2 mg P against

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Table 5.2. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and Table 5.3. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and macroinvertebrate presence or absence (Macroinvertebrates) on plant dry mass, for two species macroinvertebrate presence or absence (Macroinvertebrates) on N content, for two species (Cakile (Cakile maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p- maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value value (<0.05). (<0.05), while an open circle indicates a trend (p<0.10).

df F p df F p C. maritima C. maritima Total plant Wrack 1 20.2 <0.001 * Total plant Wrack 1 88.2 <0.001 * Macroinvertebrates 1 1.8 0.19 Macroinvertebrates 1 5.3 0.03 * Wrack * Macroinvertebrates 1 0.0 0.87 Wrack * Macroinvertebrates 1 0.6 0.46 Total shoot Wrack 1 17.8 <0.001 * Total shoot Wrack 1 78.1 <0.001 * Macroinvertebrates 1 2.2 0.15 Macroinvertebrates 1 3.7 0.07 ° Wrack * Macroinvertebrates 1 0.0 0.98 Wrack * Macroinvertebrates 1 0.6 0.45 Roots Wrack 1 21.7 <0.001 * Roots Wrack 1 52.6 <0.001 * Macroinvertebrates 1 0.3 0.60 Macroinvertebrates 1 1.6 0.21 Wrack * Macroinvertebrates 1 0.5 0.47 Wrack * Macroinvertebrates 1 0.8 0.37 E. juncea E. juncea Total plant Wrack 1 0.1 0.74 Total plant Wrack 1 0.7 0.43 Macroinvertebrates 1 0.1 0.74 Macroinvertebrates 1 0.2 0.69 Wrack * Macroinvertebrates 1 1.3 0.26 Wrack * Macroinvertebrates 1 0.1 0.76 Total shoot Wrack 1 0.3 0.61 Total shoot Wrack 1 1.4 0.26 Macroinvertebrates 1 0.5 0.48 Macroinvertebrates 1 1.1 0.30 Wrack * Macroinvertebrates 1 2.0 0.18 Wrack * Macroinvertebrates 1 0.2 0.67 Roots Wrack 1 0.0 0.98 Roots Wrack 1 0.1 0.71 Macroinvertebrates 1 0.5 0.50 Macroinvertebrates 1 0.4 0.56 Wrack * Macroinvertebrates 1 0.0 0.93 Wrack * Macroinvertebrates 1 0.0 0.94

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Table 5.4. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and 5.5.1 Buried wrack is a strong driver of Cakile maritima growth macroinvertebrate presence or absence (Macroinvertebrates) on P content, for two species (Cakile maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value As to our first hypothesis, buried wrack had indeed a strong positive effect on beach pioneer (<0.05). plant growth, but only for C. maritima. Elytrigia juncea plants, on the other hand, did not respond to wrack presence, irrespective of burial depth. For C. maritima, dry mass and P df F p content were two times, and N content three times as high when wrack was buried as opposed C. maritima to surface wrack. Thus, C. maritima plants not only accumulated more nutrients both in the Total plant Wrack 1 27.9 <0.001 * total shoot and roots, but also grew larger when wrack was buried. It is expected that the Macroinvertebrates 1 0.1 0.71 differences in plant growth between C. maritima and E. juncea are mainly species-specific and Wrack * Macroinvertebrates 1 4.5 <0.05 * related to differences in growth and habitat requirements. Cakile maritima is an annual herb, Total shoot Wrack 1 18.5 <0.001 * and annual plant species are known to exhibit higher and faster plant growth of both the shoot Macroinvertebrates 1 1.6 0.22 and roots than perennial species (Gross et al. 1992). In contrast, Elytrigia juncea is a perennial Wrack * Macroinvertebrates 1 8.8 <0.001 * grass (Hanlon and Mesgaran 2014) and may thus exhibit lower plant growth as opposed to C. Roots Wrack 1 20.4 <0.001 * maritima. As C. maritima is typically associated with drift lines (Davy et al. 2006), while E. Macroinvertebrates 1 2.5 0.13 juncea can be found at the dune foot or in stabilised stands with C. maritima (Speybroeck et Wrack * Macroinvertebrates 1 0.2 0.63 al. 2008a, Davy et al. 2006), this may also be related to their, only partly overlapping, habitat E. juncea needs. Buried wrack may thus promote the growth of some plant species more profoundly Total plant Wrack 1 0.7 0.41 than other species on the beach, which ultimately may result in an altered plant community Macroinvertebrates 1 0.0 0.84 structure on sandy beaches. Wrack * Macroinvertebrates 1 0.6 0.43 Total shoot Wrack 1 0.0 0.96 Our findings suggest that the positive effect of buried wrack on C. maritima growth is primarily Macroinvertebrates 1 0.5 0.50 due to an increase in sediment moisture content rather than an increase in nutrient Wrack * Macroinvertebrates 1 0.5 0.48 availability. To discriminate between the moisture and nutrient effect of wrack on plant Roots Wrack 1 2.3 0.14 growth, we included nutrient addition treatments. These treatments showed that in general Macroinvertebrates 1 0.6 0.46 beach pioneer plants accumulated more N and P when a nutrient solution was added than Wrack * Macroinvertebrates 1 0.7 0.40 when plants were grown without nutrient additions, indicating that C. maritima benefited from additional N and P in terms of nutrient accumulation (see Appendix, Figure A5.3-S5.5 5.5 Discussion and Table A5.2). The additional nutrients did, however, not directly translate into an increase in plant growth (Table A5.2, Figure A5.1). This indicates that nutrients are not a limiting factor In this study, we focused on the effect of wrack burial and macroinvertebrate presence on for plant growth. Indeed, plant species that are adapted to low nutrient conditions have a low decomposition and nutrient availability for beach pioneer plant growth. We found a growth rate, even if nutrient availability is increased (Chapin III et al. 1990). Only when buried differential effect of wrack burial on plant growth. While burial of wrack had a strong positive wrack was added as opposed to solely nutrients in solution, the increased accumulation of N effect on the growth of Cakile maritima, no significant effect was found for Elytrigia juncea. and P did result in higher plant growth, suggesting that buried wrack had an additive positive For C. maritima, the N content of the total plant was lower in the presence of effect. In our study, buried wrack had a higher moisture content than surface-facing wrack. macroinvertebrates. For buried wrack, P content was higher for both the total plant and total Buried wrack remains moist as it is protected from severe desiccation by a layer of sand. shoot in the presence of macroinvertebrates. Differences in N and P content of plants due to Higher soil moisture contents are therefore an important wrack-mediated factor, positively macroinvertebrate presence did however not result in differences in plant dry mass. Together, influencing C. maritima plant growth. The decay of wrack is greater when the material is fresh this suggests that macroinvertebrates enhance decomposition of wrack, but that released and moist (Coûteaux et al. 1995), thereby releasing more dissolved organic carbon and inorganic N is taken up by the microbial community or is forming complexes with phenolic increasing microbial activity (Coupland et al. 2007, Lavery et al. 2013). The higher the microbial compounds, resulting in immobilisation of N for plants. Excess P on the other hand was activity, the faster remineralisation by bacteria occurs and nutrients become available for incorporated in C. maritima. We conclude that the burial of wrack is of paramount importance plant uptake (Colombini and Chelazzi 2003). In this study, this seems particularly true for the for C. maritima growth in support of embryo dune formation and possibly further ecological release of P. Moreover, by retaining moisture, wrack forms an organic band of easy-to-reach development of the sandy beach and dune ecosystems. moisture in the sand column (Adair et al. 1990), which benefits beach pioneer plant growth (Del Vecchio et al. 2013), most likely by lifting moisture limitation and promoting N and P transport and uptake (Aerts and Chapin III 1999). This is opposed to rain water entering the

Growth of pioneer beach plants 115

116 Chapter 5 sand and quickly moving downwards beyond the reach of the roots, as sand has a low competed more strongly with the microbial community for P than N, resulting in a higher P moisture holding capacity (Pakeman and Lee 1991a). We conclude that burial of wrack has a content and lower N/P ratio (12.5 ± 4.3; Figure A5.1, Table A5.1) when macroinvertebrates positive effect on C. maritima plant growth mainly through enhancement of sediment were present and nutrient availability was enhanced. In contrast, C. maritima was limited by moisture content. N and not P in other experiments (Pakeman and Lee 1991a, Pakeman and Lee 1991b), although the interactive effects between wrack, moisture, nutrients, the microbial community 5.5.2 Macroinvertebrate presence affects plant nutrient content, but not plant growth and the macroinvertebrate community were not taken into account in those studies. The final Macroinvertebrate presence had an effect on N and P content in plant tissue but not on beach uptake of N and P by C. maritima plants thus may potentially be influenced by the competitive pioneer plant growth, which is in contrast to our second hypothesis. In addition, we found ability of both the microbial community and the individual plant for these nutrients. Neither some interactive effects between wrack burial and macroinvertebrate presence for N and P for N or P though, an effect of macroinvertebrate presence was found on plant dry mass. This content in plant tissue only, which is partly in line with our final hypothesis. Thus, suggests that lifting P limitation is not sufficient to result in an increase in plant growth, even macroinvertebrates were important in decomposition-driven nutrient availability. Previous though total moisture content in the sediment increased when wrack was buried. Moisture studies on the effect of supratidal macroinvertebrates on wrack decomposition reported was either still limiting or an additional factor had been limiting plant growth (e.g. salt, mixed results, ranging from large positive (Lastra et al. 2008, Salathé and Riera 2012) to small micronutrients). Therefore, our study highlights the complexity of macroinvertebrate- or no effects (Inglis 1989, Jędrzejczak 2002b, Catenazzi and Donnelly 2007) and our findings mediated processes that result in the degradation of wrack and subsequent uptake of are in agreement to the former studies. nutrients by beach pioneer plants. For C. maritima, a negative effect of macroinvertebrate presence on the N content of the total It should be noted that the effects of biotic factors were likely underestimated in our plant was observed, which appears to be in contrast to our second hypothesis. In other experiment due to the considerable mortality of T. saltator. The effects of macroinvertebrate nutrient-poor ecosystems, such as northern peatlands, high decomposing activities however presence were even smaller when mesocosms in which no macroinvertebrates were retrieved result in an initial immobilisation of N by the microbial community (Dorrepaal et al. 2007). upon harvest were included in the analysis (see Appendix, Figure A5.6-A5.9 and Table A5.3- Macroinvertebrates enhance decomposition via fragmentation of wrack (Ince et al. 2007, A5.6). Although we had used a representative T. saltator density in this experiment, the effect Salathé and Riera 2012, Lastra et al. 2015), but the additionally released N may initially be of T. saltator on decomposition-driven nutrient availability may be larger in the field where T. incorporated in microbial instead of plant biomass (Dorrepaal et al. 2007). In addition, saltator densities can locally become very high (up to 3500 individuals m-2 (Van Colen et al. phenolic compounds, which are present in high amounts in Fucus sp. (Targett et al. 1992), may 2006) or even 7900 individuals m-2 (Ruiz-Delgado et al. 2016)). The effect of macroinvertebrate be released during decomposition. This released carbon may have acted as a carbon source presence on decomposition-driven nutrient availability may thus be amplified when more for the microbial community, enhancing its activity (Lavery et al. 2013) and consequently N individuals are present and active. Nevertheless, this will likely not result in an increase in immobilisation (Michelsen et al. 1995). Released phenolic compounds may however also bind plant growth as other factors appear to limit plant growth. to inorganic N thereby forming insoluble complexes and causing chemical immobilisation of N Together this suggests that wrack burial and consumption by macroinvertebrates are both (Hättenschwiler and Vitousek 2000). On the other hand, P content was higher for both the drivers of decomposition-driven nutrient availability and subsequently change the nutrient total plant and total shoot in the presence of macroinvertebrates when wrack was buried, dynamics of beach pioneer plants. As only wrack burial resulted in a higher plant growth, it while the opposite was the case in the presence of macroinvertebrates when wrack was appears that beach pioneer plants are limited by moisture rather than nutrients. placed on the surface. Macroinvertebrates thus had a positive effect on decomposition-driven Macroinvertebrates may have a positive effect on plant growth when decomposition and nutrient availability, supporting a higher P content in C. maritima plants, but only when nutrient release, due to macroinvertebrate feeding activity, exceed the nutritional needs of moisture was not limiting. Differences in N and P content of C. maritima were only observed the microbial community, or in the long term when nutrients are finally released from the when wrack was buried and sand moisture content was increased, which is likely due to an microbial community via remineralisation. increase in microbial activity (Coupland et al. 2007, Lavery et al. 2013) as opposed to drier surface-facing wrack. In addition, moist wrack was probably more palatable to T. saltator 5.5.3 Conclusions resulting in a higher consumption (see Ruiz-Delgado et al. 2015). The findings for P further We conclude that wrack burial enhances nutrient availability and stimulates the growth of suggest that the microbial community associated with wrack may be principally N (or C) some beach pioneer plants, especially C. maritima. Beach pioneer plants appeared to be limited and less limited by P (e.g. Heuck et al. 2015), resulting in an increased uptake of N mainly limited by moisture rather than nutrients. Decomposition of wrack by when this became available during wrack decomposition. Plants appeared to be P limited in macroinvertebrates appears to be an additional factor that increased nutrient availability, but the absence of macroinvertebrates when wrack was buried, as the N/P ratio of C. maritima this does not result in an increase in plant growth. Leaving wrack on the beach and allowing it shoots was relatively high (27.7 ± 12.1; Figure A5.1, Table A5.1) and well above a N/P ratio of to be covered by sand and subsequently decomposed, provides a moisture and nutrient hot 16 which indicates a P limitation (Aerts and Chapin III 1999). Plants may in that case have spot for beach pioneer plants on sandy beaches. Buried wrack can provide preferable

Growth of pioneer beach plants 117 sand and quickly moving downwards beyond the reach of the roots, as sand has a low competed more strongly with the microbial community for P than N, resulting in a higher P moisture holding capacity (Pakeman and Lee 1991a). We conclude that burial of wrack has a content and lower N/P ratio (12.5 ± 4.3; Figure A5.1, Table A5.1) when macroinvertebrates positive effect on C. maritima plant growth mainly through enhancement of sediment were present and nutrient availability was enhanced. In contrast, C. maritima was limited by moisture content. N and not P in other experiments (Pakeman and Lee 1991a, Pakeman and Lee 1991b), although the interactive effects between wrack, moisture, nutrients, the microbial community 5.5.2 Macroinvertebrate presence affects plant nutrient content, but not plant growth and the macroinvertebrate community were not taken into account in those studies. The final Macroinvertebrate presence had an effect on N and P content in plant tissue but not on beach uptake of N and P by C. maritima plants thus may potentially be influenced by the competitive pioneer plant growth, which is in contrast to our second hypothesis. In addition, we found ability of both the microbial community and the individual plant for these nutrients. Neither some interactive effects between wrack burial and macroinvertebrate presence for N and P for N or P though, an effect of macroinvertebrate presence was found on plant dry mass. This content in plant tissue only, which is partly in line with our final hypothesis. Thus, suggests that lifting P limitation is not sufficient to result in an increase in plant growth, even macroinvertebrates were important in decomposition-driven nutrient availability. Previous though total moisture content in the sediment increased when wrack was buried. Moisture studies on the effect of supratidal macroinvertebrates on wrack decomposition reported was either still limiting or an additional factor had been limiting plant growth (e.g. salt, mixed results, ranging from large positive (Lastra et al. 2008, Salathé and Riera 2012) to small micronutrients). Therefore, our study highlights the complexity of macroinvertebrate- or no effects (Inglis 1989, Jędrzejczak 2002b, Catenazzi and Donnelly 2007) and our findings mediated processes that result in the degradation of wrack and subsequent uptake of are in agreement to the former studies. nutrients by beach pioneer plants. For C. maritima, a negative effect of macroinvertebrate presence on the N content of the total It should be noted that the effects of biotic factors were likely underestimated in our plant was observed, which appears to be in contrast to our second hypothesis. In other experiment due to the considerable mortality of T. saltator. The effects of macroinvertebrate nutrient-poor ecosystems, such as northern peatlands, high decomposing activities however presence were even smaller when mesocosms in which no macroinvertebrates were retrieved result in an initial immobilisation of N by the microbial community (Dorrepaal et al. 2007). upon harvest were included in the analysis (see Appendix, Figure A5.6-A5.9 and Table A5.3- Macroinvertebrates enhance decomposition via fragmentation of wrack (Ince et al. 2007, A5.6). Although we had used a representative T. saltator density in this experiment, the effect Salathé and Riera 2012, Lastra et al. 2015), but the additionally released N may initially be of T. saltator on decomposition-driven nutrient availability may be larger in the field where T. incorporated in microbial instead of plant biomass (Dorrepaal et al. 2007). In addition, saltator densities can locally become very high (up to 3500 individuals m-2 (Van Colen et al. phenolic compounds, which are present in high amounts in Fucus sp. (Targett et al. 1992), may 2006) or even 7900 individuals m-2 (Ruiz-Delgado et al. 2016)). The effect of macroinvertebrate be released during decomposition. This released carbon may have acted as a carbon source presence on decomposition-driven nutrient availability may thus be amplified when more for the microbial community, enhancing its activity (Lavery et al. 2013) and consequently N individuals are present and active. Nevertheless, this will likely not result in an increase in immobilisation (Michelsen et al. 1995). Released phenolic compounds may however also bind plant growth as other factors appear to limit plant growth. to inorganic N thereby forming insoluble complexes and causing chemical immobilisation of N Together this suggests that wrack burial and consumption by macroinvertebrates are both (Hättenschwiler and Vitousek 2000). On the other hand, P content was higher for both the drivers of decomposition-driven nutrient availability and subsequently change the nutrient total plant and total shoot in the presence of macroinvertebrates when wrack was buried, dynamics of beach pioneer plants. As only wrack burial resulted in a higher plant growth, it while the opposite was the case in the presence of macroinvertebrates when wrack was appears that beach pioneer plants are limited by moisture rather than nutrients. placed on the surface. Macroinvertebrates thus had a positive effect on decomposition-driven Macroinvertebrates may have a positive effect on plant growth when decomposition and nutrient availability, supporting a higher P content in C. maritima plants, but only when nutrient release, due to macroinvertebrate feeding activity, exceed the nutritional needs of moisture was not limiting. Differences in N and P content of C. maritima were only observed the microbial community, or in the long term when nutrients are finally released from the when wrack was buried and sand moisture content was increased, which is likely due to an microbial community via remineralisation. increase in microbial activity (Coupland et al. 2007, Lavery et al. 2013) as opposed to drier surface-facing wrack. In addition, moist wrack was probably more palatable to T. saltator 5.5.3 Conclusions resulting in a higher consumption (see Ruiz-Delgado et al. 2015). The findings for P further We conclude that wrack burial enhances nutrient availability and stimulates the growth of suggest that the microbial community associated with wrack may be principally N (or C) some beach pioneer plants, especially C. maritima. Beach pioneer plants appeared to be limited and less limited by P (e.g. Heuck et al. 2015), resulting in an increased uptake of N mainly limited by moisture rather than nutrients. Decomposition of wrack by when this became available during wrack decomposition. Plants appeared to be P limited in macroinvertebrates appears to be an additional factor that increased nutrient availability, but the absence of macroinvertebrates when wrack was buried, as the N/P ratio of C. maritima this does not result in an increase in plant growth. Leaving wrack on the beach and allowing it shoots was relatively high (27.7 ± 12.1; Figure A5.1, Table A5.1) and well above a N/P ratio of to be covered by sand and subsequently decomposed, provides a moisture and nutrient hot 16 which indicates a P limitation (Aerts and Chapin III 1999). Plants may in that case have spot for beach pioneer plants on sandy beaches. Buried wrack can provide preferable

118 Chapter 5 microclimate conditions for plant growth and possibly support embryo dune formation, e.g. 5.6 Appendix for C. maritima (Davy et al. 2006), while also having a positive effect on dune vegetation in 5.6.1 N/P ratio for the main treatments terms of plant diversity (Del Vecchio et al. 2017). It is therefore recommended to allow wrack to be deposited and buried on the sandy beach to promote the sandy beach ecosystem in For C. maritima, there was a significant effect of wrack burial and a significant interaction future coastal management strategies. effect between wrack burial and macroinvertebrate presence for both N/P ratio of the total plant and the total shoot (Table A5.1, Figure A5.1). For buried wrack, the N/P ratio of the total plant was higher in the absence (N/P = 37.5 ± 11.7) than in the presence (N/P = 21.5 ± 4.4) of macroinvertebrates. The opposite was the case for surface-facing wrack, where total plant N/P ratio was higher in the presence (N/P = 27.8 ± 7.7) than in the absence (N/P = 23.4 ± 5.0) of macroinvertebrates. Similar to the total plant, the N/P ratio of the total shoot was higher in the absence (N/P = 27.7 ± 12.1) than in the presence (N/P = 12.5 ± 4.3) of macroinvertebrates when wrack was buried. The opposite was observed with surface-facing wrack, where the N/P ratio of the total shoot was higher in the presence (N/P = 17.6 ± 4.9) than in the absence (N/P = 14.2 ± 3.7) of macroinvertebrates. There were no significant interaction effects on the N/P ratio of the roots, but the N/P ratio of the roots (N/P = 64.8 ± 34.0) was three times higher than in the total shoot (N/P = 18.0 ± 10.2). For E. juncea, there were no significant differences of wrack position or macroinvertebrate presence on the N/P ratio of either the total plant, total shoot or roots (Table A5.1, Figure A5.1).

Table A5.1. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and macroinvertebrate presence or absence (Macroinvertebrates) on N/P ratio, for two species (Cakile maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value (<0.05).

df F p

C. maritima Total plant Wrack 1 4.6 <0.05 * Macroinvertebrates 1 1.9 0.18 Wrack * Macroinvertebrates 1 9.8 <0.01 * Total shoot Wrack 1 4.7 0.04 * Macroinvertebrates 1 2.5 0.13 Wrack * Macroinvertebrates 1 11.2 <0.01 * Roots Wrack 1 0.5 0.48 Macroinvertebrates 1 0.8 0.37 Wrack * Macroinvertebrates 1 0.0 0.89 E. juncea Total plant Wrack 1 0.1 0.73 Macroinvertebrates 1 0.1 0.79 Wrack * Macroinvertebrates 1 0.3 0.61 Total shoot Wrack 1 2.4 0.14 Macroinvertebrates 1 0.6 0.45 Wrack * Macroinvertebrates 1 0.5 0.51 Roots Wrack 1 0.5 0.50 Macroinvertebrates 1 0.0 0.97 Wrack * Macroinvertebrates 1 0.6 0.45

Growth of pioneer beach plants 119 microclimate conditions for plant growth and possibly support embryo dune formation, e.g. 5.6 Appendix for C. maritima (Davy et al. 2006), while also having a positive effect on dune vegetation in 5.6.1 N/P ratio for the main treatments terms of plant diversity (Del Vecchio et al. 2017). It is therefore recommended to allow wrack to be deposited and buried on the sandy beach to promote the sandy beach ecosystem in For C. maritima, there was a significant effect of wrack burial and a significant interaction future coastal management strategies. effect between wrack burial and macroinvertebrate presence for both N/P ratio of the total plant and the total shoot (Table A5.1, Figure A5.1). For buried wrack, the N/P ratio of the total plant was higher in the absence (N/P = 37.5 ± 11.7) than in the presence (N/P = 21.5 ± 4.4) of macroinvertebrates. The opposite was the case for surface-facing wrack, where total plant N/P ratio was higher in the presence (N/P = 27.8 ± 7.7) than in the absence (N/P = 23.4 ± 5.0) of macroinvertebrates. Similar to the total plant, the N/P ratio of the total shoot was higher in the absence (N/P = 27.7 ± 12.1) than in the presence (N/P = 12.5 ± 4.3) of macroinvertebrates when wrack was buried. The opposite was observed with surface-facing wrack, where the N/P ratio of the total shoot was higher in the presence (N/P = 17.6 ± 4.9) than in the absence (N/P = 14.2 ± 3.7) of macroinvertebrates. There were no significant interaction effects on the N/P ratio of the roots, but the N/P ratio of the roots (N/P = 64.8 ± 34.0) was three times higher than in the total shoot (N/P = 18.0 ± 10.2). For E. juncea, there were no significant differences of wrack position or macroinvertebrate presence on the N/P ratio of either the total plant, total shoot or roots (Table A5.1, Figure A5.1).

df F p

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5.6.2 Results nutrient addition test additions (total plant: 7.5 ± 1.2 mg N, p=0.001; total shoot: 4.3 ± 0.6 mg N, p<0.001; Table A5.2, Figure A5.3). For E. juncea, N content was significantly higher in plants that received a For shoot, root and total plant dry mass, no significant differences among the nutrient nutrient solution (total plant: 14.7 ± 6.5 mg N, total shoot: 10.9 ± 5.1 mg N) compared to plants treatments were found for either Cakile maritima or Elytrigia juncea (Table A5.2, Figure A5.2). grown with inoculum (total plant: 6.9 ± 2.1 mg N, p=0.03; total shoot: 5.2 ± 1.6 mg N, p=0.04), The N content was significantly higher in C. maritima that received a nutrient solution (total while plants that received a nutrient solution only showed a trend towards a higher N content plant: 17.7 ± 4.3 mg N, total shoot: 14.8 ± 3.5 mg N) than plants grown with inoculum (total than plants grown without nutrient additions (total plant: 8.6 ± 2.7 mg N, p=0.09; total shoot: plant: 9.4 ± 3.8 mg N, p=0.006; total shoot: 5.2 ± 2.0 mg N; p<0.001) or without nutrient

A A

B B

Figure A5.1. N/P ratio of the total plant (roots and shoot), total shoot (stem and leaves) and roots of Figure A5.2. Absolute dry mass of the total plant (roots and shoot), total shoot (stem and leaves) and A) Cakile maritima and B) Elytrigia juncea shown for both buried or surface-exposed wrack and in the roots of A) Cakile maritima and B) Elytrigia juncea at harvest shown for the three treatments in the presence or absence of the amphipod Talitrus saltator. For buried wrack n=3, while n=6 for surface- nutrient addition test: plant only, added nutrient solution equivalent to 100% wrack in trial (Nutrients) exposed wrack in the presence of T. saltator. For all other treatment combinations n=8. Error bars and added inoculum based on fresh wrack (Inoculum). For all treatments n=5. Error bars indicate the indicate the standard error from the mean. standard error from the mean.

Growth of pioneer beach plants 121

A A

B B

122 Chapter 5

5.9 ± 1.2 mg N, p=0.06; Table A5.2, Figure A5.3). Thus, for both plant species, the N content The P content was the only measured variable that was significantly different in the roots was approximately two to three times higher when plants received a nutrient solution as (Table A5.2, Figure A5.4). For C. maritima, the P content was significantly higher in plants that opposed to plants receiving either inoculum or no nutrient additions. received a nutrient solution (total plant: 1.7 ± 0.4 mg P, total shoot: 1.6 ± 0.2 mg P, roots: 0.2 ± 0.1 mg P) compared to plants grown with inoculum (total plant: 0.9 ± 0.3 mg P, p=0.004;

total shoot: 0.9 ± 0.3 mg P, p=0.005; roots: 0.1 ± 0.0 mg P, p=0.02) or without nutrient

A additions (total plant: 0.8 ± 0.3 mg P, p=0.002; total shoot: 0.8 ± 0.3 mg P, p=0.001; roots: 0.1

Figure A5.3. N content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) Cakile maritima and B) Elytrigia juncea at harvest shown for the three treatments in the nutrient addition test: plant only, added nutrient solution equivalent to 100% wrack in trial (Nutrients) and added inoculum based on fresh wrack (Inoculum). For all treatments n=5. Error bars indicate the Figure A5.4. P content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of standard error from the mean. A) Cakile maritima and B) Elytrigia juncea shown for the three treatments in the nutrient addition test: plant only, added nutrient solution equivalent to 100% wrack in trial (Nutrients) and added inoculum based on fresh wrack (Inoculum). For all treatments n=5. Error bars indicate the standard error from the mean.

Growth of pioneer beach plants 123

total shoot: 0.9 ± 0.3 mg P, p=0.005; roots: 0.1 ± 0.0 mg P, p=0.02) or without nutrient

A additions (total plant: 0.8 ± 0.3 mg P, p=0.002; total shoot: 0.8 ± 0.3 mg P, p=0.001; roots: 0.1

124 Chapter 5

± 0.1 mg P, p=0.03). For E. juncea, the P content was only significantly higher in the roots of Table A5.2. Overview of the one-way ANOVA results on the treatment effect in the nutrient addition plants that received a nutrient solution (0.2 ± 0.1 mg P) compared to plants grown with test (nutrient solution, inoculum and plant only) on dry mass, N and P content and N/P ratio, for each inoculum (0.1 ± 0.1 mg P, p<0.05) or without nutrient additions (0.1 ± 0.0 mg P, p=0.007). plant species and plant organ (total plant, total shoot and roots) separately. An asterix indicates a Thus, for both species, the P content was approximately two times as high when plants significant p-value (<0.05), while an open circle indicates a trend (p<0.10). received a nutrient solution as opposed to plants receiving either inoculum or no nutrient df F p additions. Dry mass C. maritima Total plant 2 1.1 0.38

Total shoot 2 1.0 0.41 Roots 2 2.4 0.14 A E. juncea Total plant 2 0.5 0.64 Total shoot 2 0.6 0.57 Roots 2 0.6 0.58 N content C. maritima Total plant 2 12.7 0.001 *

Total shoot 2 29.8 <0.001 * Roots 2 0.7 0.50 E. juncea

Total plant 2 4.7 0.03 * Total shoot 2 5.4 0.02 * Roots 2 3.1 0.08 ° P content C. maritima Total plant 2 12.8 0.001 * Total shoot 2 13.4 <0.001 * Roots 2 5.9 0.02 * E. juncea

B Total plant 2 3.7 0.06 ° Total shoot 2 2.2 0.16 Roots 2 7.5 0.008 *

N/P ratio C. maritima

Total plant 2 0.03 0.97 Total shoot 2 10.9 0.002 * Roots 2 7.84 0.007 * E. juncea Total plant 2 2.06 0.17 Total shoot 2 0.96 0.41 Roots 2 3.00 0.09 °

The N/P ratio of the total shoot was significantly higher in C. maritima that received a nutrient solution (N/P = 9.5 ± 1.8) than those grown with inoculum (N/P = 5.6 ± 0.7, p=0.003) or without nutrient additions (N/P = 6.0 ± 1.6, p=0.007; Table A5.2, Figure A5.4). In contrast, the N/P ratio

Figure A5.5. N/P ratio of the total plant (roots and shoot), total shoot (stem and leaves) and roots of of the roots was significantly lower in C. maritima that received a nutrient solution (N/P = 13.0 A) Cakile maritima and B) Elytrigia juncea shown for the three treatments in the nutrient addition test: ± 4.0) than those grown with inoculum (N/P = 34.4 ± 7.2; p=0.007) or without nutrient plant only, added nutrient solution equivalent to 100% wrack in trial (Nutrients) and added inoculum additions (N/P = 29.0 ± 13.0, p=0.037). For E. juncea, there were no significant differences based on fresh wrack (Inoculum). For all treatments n=5. Error bars indicate the standard error from between the treatments in the nutrient addition test for the N/P ratio of either the total plant, the mean. total shoot or root (Table A5.2, Figure A5.5).

Growth of pioneer beach plants 125

Total shoot 2 1.0 0.41 Roots 2 2.4 0.14 A E. juncea Total plant 2 0.5 0.64 Total shoot 2 0.6 0.57 Roots 2 0.6 0.58 N content C. maritima Total plant 2 12.7 0.001 *

Total shoot 2 29.8 <0.001 * Roots 2 0.7 0.50 E. juncea

Total plant 2 4.7 0.03 * Total shoot 2 5.4 0.02 * Roots 2 3.1 0.08 ° P content C. maritima Total plant 2 12.8 0.001 * Total shoot 2 13.4 <0.001 * Roots 2 5.9 0.02 * E. juncea

B Total plant 2 3.7 0.06 ° Total shoot 2 2.2 0.16 Roots 2 7.5 0.008 *

N/P ratio C. maritima

Total plant 2 0.03 0.97 Total shoot 2 10.9 0.002 * Roots 2 7.84 0.007 * E. juncea Total plant 2 2.06 0.17 Total shoot 2 0.96 0.41 Roots 2 3.00 0.09 °

126 Chapter 5

5.6.3 Analyses performed on all mesocosms In the following analyses, all mesocosms in the experiment were included, also those A mesocosms to which macroinvertebrates were added, but none were retrieved upon harvest.

Figure A5.7. N content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack Figure A5.6. Dry mass of the total plant (roots and shoot), total shoot (stem and leaves) and roots of and in the presence or absence of the amphipod Talitrus saltator. For all treatments n=8. Error bars A) Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack indicate the standard error from the mean. and in the presence or absence of the amphipod Talitrus saltator. For all treatments n=8. Error bars indicate the standard error from the mean.

Growth of pioneer beach plants 127

128 Chapter 5

A A

B B

Figure A5.9. N/P ratio of the total plant (roots and shoot), total shoot (stem and leaves) and roots of Figure A5.8. P content of the total plant (roots and shoot), total shoot (stem and leaves) and roots of A) Cakile maritima and B) Elytrigia juncea shown for both buried or surface-exposed wrack and in the A) Cakile maritima and B) Elytrigia juncea at harvest shown for both buried or surface-exposed wrack presence or absence of the amphipod Talitrus saltator. For all treatments n=8. Error bars indicate the and in the presence or absence of the amphipod Talitrus saltator. For all treatments n=8. Error bars standard error from the mean. indicate the standard error from the mean.

Growth of pioneer beach plants 129

A A

B B

130 Chapter 5

Table A5.3. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and Table A5.4. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and macroinvertebrate presence or absence (Macroinvertebrates) on plant dry mass, for two species macroinvertebrate presence or absence (Macroinvertebrates) on N content, for two species (Cakile (Cakile maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p- maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value value (<0.05), while an open circle indicates a trend (p<0.10). (<0.05), while an open circle indicates a trend (p<0.10).

df F p df F p C. maritima C. maritima Total plant Wrack 1 23.6 <0.001 * Total plant Wrack 1 105.3 <0.001 * Macroinvertebrates 1 0.2 0.64 Macroinvertebrates 1 0.7 0.41 Wrack * Macroinvertebrates 1 0.3 0.57 Wrack * Macroinvertebrates 1 1.9 0.17 Total shoot Wrack 1 20.4 <0.001 * Total shoot Wrack 1 107.7 <0.001 * Macroinvertebrates 1 0.2 0.66 Macroinvertebrates 1 0.0 0.90 Wrack * Macroinvertebrates 1 0.1 0.78 Wrack * Macroinvertebrates 1 0.9 0.35 Roots Wrack 1 19.1 <0.001 * Roots Wrack 1 44.9 <0.001 * Macroinvertebrates 1 0.2 0.69 Macroinvertebrates 1 1.1 0.30 Wrack * Macroinvertebrates 1 3.7 0.07 ° Wrack * Macroinvertebrates 1 5.3 0.03 * E. juncea E. juncea Total plant Wrack 1 0.0 0.97 Total plant Wrack 1 0.1 0.76 Macroinvertebrates 1 1.6 0.22 Macroinvertebrates 1 1.3 0.26 Wrack * Macroinvertebrates 1 0.3 0.61 Wrack * Macroinvertebrates 1 0.2 0.70 Total shoot Wrack 1 0.0 0.99 Total shoot Wrack 1 0.7 0.42 Macroinvertebrates 1 2.9 0.10 ° Macroinvertebrates 1 3.2 0.08 ° Wrack * Macroinvertebrates 1 0.3 0.61 Wrack * Macroinvertebrates 1 0.1 0.84 Roots Wrack 1 0.0 0.83 Roots Wrack 1 0.1 0.86 Macroinvertebrates 1 0.0 0.83 Macroinvertebrates 1 0.0 1.00 Wrack * Macroinvertebrates 1 0.0 0.86 Wrack * Macroinvertebrates 1 0.5 0.48

Growth of pioneer beach plants 131

132 Chapter 5

Table A5.5. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and Table A5.6. Overview of the two-way ANOVA results on the effect of wrack burial (Wrack) and macroinvertebrate presence or absence (Macroinvertebrates) on P content, for two species (Cakile macroinvertebrate presence or absence (Macroinvertebrates) on N/P ratio, for two species (Cakile maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value maritima and Elytrigia juncea) and plant organs separately. An asterix indicates a significant p-value (<0.05). (<0.05), while an open circle indicates a trend (p<0.10).

df F p df F p

C. maritima C. maritima Total plant Wrack 1 25.6 <0.001 * Total plant Wrack 1 3.0 0.10 ° Macroinvertebrates 1 0.2 0.66 Macroinvertebrates 1 0.7 0.41 Wrack * Macroinvertebrates 1 0.8 0.37 Wrack * Macroinvertebrates 1 5.7 0.02 * Total shoot Wrack 1 18.3 <0.001 * Total shoot Wrack 1 4.6 0.04 *

Macroinvertebrates 1 1.3 0.26 Macroinvertebrates 1 1.1 0.30 Wrack * Macroinvertebrates 1 1.7 0.20 Wrack * Macroinvertebrates 1 5.7 0.02 * Roots Wrack 1 20.5 <0.001 * Roots Wrack 1 0.0 0.84 Macroinvertebrates 1 0.8 0.37 Macroinvertebrates 1 0.7 0.40 Wrack * Macroinvertebrates 1 0.7 0.41 Wrack * Macroinvertebrates 1 0.5 0.48 E. juncea E. juncea Total plant Wrack 1 0.5 0.48 Total plant Wrack 1 0.1 0.81 Macroinvertebrates 1 0.8 0.38 Macroinvertebrates 1 0.5 0.48 Wrack * Macroinvertebrates 1 0.1 0.72 Wrack * Macroinvertebrates 1 1.2 0.28 Total shoot Wrack 1 0.0 0.97 Total shoot Wrack 1 1.6 0.21 Macroinvertebrates 1 2.1 0.16 Macroinvertebrates 1 1.0 0.34 Wrack * Macroinvertebrates 1 0.4 0.54 Wrack * Macroinvertebrates 1 1.5 0.23 Roots Wrack 1 2.1 0.16 Roots Wrack 1 1.5 0.23 Macroinvertebrates 1 0.4 0.53 Macroinvertebrates 1 0.4 0.56 Wrack * Macroinvertebrates 1 0.2 0.65 Wrack * Macroinvertebrates 1 1.2 0.29

Growth of pioneer beach plants 133

df F p df F p

Chapter 6

General discussion

Chapter 6

General discussion

136 Chapter 6

6.1 General findings included in this litter bag experiment. Season was a strong driver of both N and P mineralisation and the supratidal macroinvertebrate community. Drift line did not have a This thesis addressed the following two main aims: 1) to improve our understanding of the strong effect on N and P mineralisation or the supratidal macroinvertebrate community, effect of resource availability on species interactions and community assembly of the except for macroinvertebrate diversity which was higher in young than old drift lines. N and P macroinvertebrate community on sandy beaches, and how this influences ecosystem mineralisation was mainly predicted by season and macroinvertebrate abundance, while P functioning, and 2) to investigate the effect of sand nourishment on the macroinvertebrate mineralisation was additionally to some extent positively affected by macroinvertebrate community of the sandy beach and identify implications for future sand nourishments. For richness and diversity. this purpose, both the intertidal and supratidal zone were studied and a mix of field studies (both monitoring and experimental) and mesocosm studies was used. Below, I give a brief What is the effect of wrack burial and supratidal macroinvertebrate presence on nutrient summary of the research questions and main findings for each chapter, followed by bringing availability and beach pioneer plant growth? together the outcomes of each chapter and indicating how they contributed to the overall In Chapter 5 we assessed the effect of wrack burial and supratidal macroinvertebrate thesis aims. Finally, I present ideas and recommendations for future ecological research and presence on decomposition-driven nutrient availability and beach pioneer plant growth. coastal management respectively and I finish with the main conclusions of this thesis. Buried wrack had a strong positive effect on plant dry mass and both N and P content of Cakile How does the intertidal macroinvertebrate community develop after a mega-nourishment? maritima compared to surface wrack, while effects for Elytrigia juncea were largely absent. For C. maritima, an effect of macroinvertebrate presence on the N content of the total plant In Chapter 2 we assessed the spatial and temporal effects on the intertidal macroinvertebrate was observed, with a higher N content in the absence of macroinvertebrates. For buried community after placement of a mega-nourishment and compared these to the communities wrack, P content was higher for both the total plant and total shoot in the presence of present on beaches subject to regular beach nourishment and unnourished beaches. There macroinvertebrates. Differences in N and P content of plants due to macroinvertebrate were strong spatial effects within the mega-nourishment, where a distinct intertidal presence did however not result in differences in plant dry mass. macroinvertebrate community was present in the lagoon as compared to the wave-exposed locations. Temporal effects on the macroinvertebrate community within the mega- 6.2 Resource availability effects on the macroinvertebrate community nourishment, up to four years after construction, were limited. Wave-exposed locations at the Resource availability is key for the survival, growth and reproduction of species in any given mega-nourishment had a higher macroinvertebrate richness, lower macroinvertebrate environment and hence drives the outcome of biological interactions, shaping final abundance and did not converge into a macroinvertebrate community composition similar to community composition (e.g. Chapin III et al. 2000). Sandy beach communities have those on unnourished beaches. traditionally been considered to be primarily structured by physical control, i.e. the How does resource availability affect the non-additive effects of consumption between environmental filter, while biological interactions such as competition, i.e. the limiting intertidal macroinvertebrate species? similarity filter, are considered to be less influential (Defeo and McLachlan 2005, McLachlan and Brown 2006). This is in contrast to rocky shore communities, where biological interactions, In Chapter 3 we studied the effect of diatom availability on the non-additive effects of including resource competition, have been widely shown to play an additional role to the consumption by a simple intertidal macroinvertebrate community. Of the three influence of the physical environment in macroinvertebrate community assembly (e.g. Menge macroinvertebrate species, Bathyporeia pilosa was the most successful competitor in terms 2000, Liess and Hillebrand 2004, Guerry and Menge 2017). Recently, however, evidence has of consumption at both high and low diatom availability, while Haustorius arenarius and been accumulating that resource availability and related biological interactions may be more Scolelepis squamata consumed less in community than in their respective monocultures. Non- important in structuring intertidal macroinvertebrate communities on sandy beaches as well additive effects of consumption were present and were larger than mere additive effects, (e.g. Schlacher and Hartwig 2013, Bergamino et al. 2016). The findings of Chapter 3 strongly which were similar across diatom availabilities. Complementary effects related to niche- support this idea by identifying the importance of resource availability for species interactions partitioning were the main driver of the non-additive effects of consumption, with a slightly and consumption between intertidal macroinvertebrates of sandy beaches. Also, the findings increasing contribution of selection effects related to competition with decreasing diatom of Chapter 4 show that wrack attracts a diverse supratidal macroinvertebrate community, availability. where a change in wrack quality during decay is suggested to support a succession of Is the supratidal macroinvertebrate community a driver of wrack mineralisation and does this supratidal macroinvertebrate species. differ between drift lines and seasons? On sandy beaches, resource availability is highly variable in time and space, both in the In Chapter 4 we addressed the question whether the supratidal macroinvertebrate intertidal (Shanks et al. 2017, Morgan et al. 2018) and supratidal (Liebowitz et al. 2016) zone, community, in terms of abundance, richness and diversity, is a driver of N and P mineralisation and macroinvertebrates are expected to respond strongly to these changes as resources can of wrack. In addition, temporal (seasonal) and spatial (young and old drift lines) effects were temporally or locally be scarce. At the same time, macroinvertebrate species may be well

General discussion 137

138 Chapter 6 adapted to this low food environment. In Chapter 3 it became evident that resource In conclusion, this thesis showed a clear effect of resource availability on macroinvertebrate availability is a driver of the outcome of biological interactions between intertidal species interactions and subsequent consumption in the intertidal zone, which may indirectly macroinvertebrates, with complementary effects (i.e. niche segregation) being dominant at affect community composition and ecosystem functioning (primarily nutrient cycling). high diatom availability, but with a larger role for negative species interactions (i.e. Resource availability had a direct effect on macroinvertebrate community composition in the competition) when diatom availability was low. Nevertheless, positive non-additive effects of supratidal zone as supratidal macroinvertebrates colonised deposited wrack. Biological consumption were maintained across diatom availabilities, regardless of a shift in species interactions related to resource availability thus need be taken into account in future studies interactions. This finding emphasises the flexibility of intertidal macroinvertebrates to the on macroinvertebrate community assembly on sandy beaches. availability of food. When diatom availability is low, less successful competitors for diatoms in the community may have shifted their diet towards other food sources if these would have Take home message: Resource availability affects species interactions and community been available. Intertidal macroinvertebrate species indeed exhibit plasticity in resource use composition of macroinvertebrates on sandy beaches and have been shown to adjust their consumption pattern based on the presence of surf diatoms with a higher nutritional quality, consuming more POM and zooplankton when diatoms were absent (Bergamino et al. 2016). This suggests that if abundant lower nutritional 6.3 Macroinvertebrate community effects on ecosystem functioning quality food sources are available, macroinvertebrate species can cope with a decreased The macroinvertebrate community of sandy beaches contributes to two main ecosystem availability of high nutritional quality food sources by strong competition. Hence, co-existence functions: 1) nutrient cycling and 2) food to support higher trophic levels, while adding to a is promoted between intertidal macroinvertebrates and overall non-additive effects of unique biodiversity exclusively associated with sandy beaches (Schlacher et al. 2007). Changes consumption may be maintained over a longer period of time. Furthermore, we have shown in community composition alter ecosystem functioning when species are lost or added with in Chapter 2 that intertidal macroinvertebrate densities can locally be high (see also Leewis et specific functional traits or when abundances of a functionally important species significantly al. 2012), indicating that biological interactions may potentially be important in driving increase or decrease (Hooper et al. 2005, Cardinale et al. 2006, Hillebrand et al. 2008). We intertidal macroinvertebrate community composition on sandy beaches. Biological have shown in Chapter 4 that supratidal macroinvertebrate community abundance, richness interactions should therefore not be disregarded when trying to understand and diversity were drivers of N and P mineralisation of wrack. Changes in supratidal macroinvertebrate community patterns of the intertidal zone and from the above, it can be macroinvertebrate community composition may therefore alter nutrient cycling and thus stated that the importance of biological interactions likely depends on a combination of ecosystem functioning, which has been shown on sandy beaches (Costa et al. 2017) and is in resource availability, macroinvertebrate density and macroinvertebrate diversity. line with general ecological theory (Hooper et al. 2005). Densities of supratidal In the supratidal zone, macroinvertebrates respond strongly to wrack in terms of abundance macroinvertebrates can, in addition, be locally high (Van Colen et al. 2005, Ruiz-Delgado et al. and richness (e.g. Olabarria et al. 2007, Colombini et al. 2009, Chapter 4). Wrack is deposited 2016), hence creating the potential to have a significant effect on ecosystem functioning over a restricted area on the beach and as supratidal macroinvertebrate species essentially (Hillebrand et al. 2008). Also in Chapter 4, Diptera larvae densities in wrack were similar to for use the same type of resource (i.e. wrack) for food and habitat (Ince et al. 2007, Ruiz-Delgado example Jędrzejczak (2002b), with on average 92 ± 15 (SE) Fucellia sp. larvae per litter bag et al. 2015), there is a potential for resource competition (Lastra et al. 2010). At the same time, (Chapter 4) against approximately 90 Fucellia tergina larvae per litter bag (Jędrzejczak 2002b), macroinvertebrates are expected to exhibit niche segregation in time and space to allow for in both studies after two weeks of field incubation, and thus relatively high. Furthermore, I co-existence on wrack patches (Lastra et al. 2010). The availability of wrack to the supratidal aimed in Chapter 5 to test the effect of the presence of T. saltator on the decomposition- macroinvertebrate community may differ between macroinvertebrate species within a single driven nutrient availability for beach pioneer plants, where macroinvertebrates were indeed drift line, as wrack traits that influence its resource use (e.g. nutritional quality and moisture found to enhance decomposition and mineralisation of wrack, but the effect of T. saltator content) differ between wrack species and decomposition stages (Orr et al. 2005, Liebowitz presence on final nutrient uptake by C. maritima appeared to be potentially influenced by the et al. 2016). In Chapter 4, a locally high abundance of Diptera larvae in wrack was observed competitive ability of both the microbial community and the individual plant for these while few T. saltator individuals were found, indicating a later successional stage of wrack was nutrients. In addition, early succession species, such as T. saltator may indirectly facilitate late sampled. Early succession macroinvertebrate species such as T. saltator may indirectly succession macroinvertebrate species e.g. due to their feeding activities on wrack and its facilitate late succession macroinvertebrate species such as Diptera larvae (e.g. Olabarria et biofilm (e.g. Olabarria et al. 2007). Talitrus saltator is in that case also indirectly responsible al. 2007). This suggests that resource availability (in terms of e.g. resource quality) changes for an increase in wrack decomposition and mineralisation. To summarise, the supratidal with decomposition stage of wrack, therefore supporting different macroinvertebrate species macroinvertebrate community appears to be an important driver of nutrient cycling on sandy at different moments in time. This is supported by the result that mineralisation of wrack is beaches. not uniform and depends on both abiotic and biotic factors (Chapter 4 and 5), which changes In addition to the effect of macroinvertebrate community on wrack mineralisation, the effect wrack availability to (subsequent) supratidal macroinvertebrate species. of season, wrack burial by sand and drift line position were investigated (Chapter 4 and 5).

General discussion 139 adapted to this low food environment. In Chapter 3 it became evident that resource In conclusion, this thesis showed a clear effect of resource availability on macroinvertebrate availability is a driver of the outcome of biological interactions between intertidal species interactions and subsequent consumption in the intertidal zone, which may indirectly macroinvertebrates, with complementary effects (i.e. niche segregation) being dominant at affect community composition and ecosystem functioning (primarily nutrient cycling). high diatom availability, but with a larger role for negative species interactions (i.e. Resource availability had a direct effect on macroinvertebrate community composition in the competition) when diatom availability was low. Nevertheless, positive non-additive effects of supratidal zone as supratidal macroinvertebrates colonised deposited wrack. Biological consumption were maintained across diatom availabilities, regardless of a shift in species interactions related to resource availability thus need be taken into account in future studies interactions. This finding emphasises the flexibility of intertidal macroinvertebrates to the on macroinvertebrate community assembly on sandy beaches. availability of food. When diatom availability is low, less successful competitors for diatoms in the community may have shifted their diet towards other food sources if these would have Take home message: Resource availability affects species interactions and community been available. Intertidal macroinvertebrate species indeed exhibit plasticity in resource use composition of macroinvertebrates on sandy beaches and have been shown to adjust their consumption pattern based on the presence of surf diatoms with a higher nutritional quality, consuming more POM and zooplankton when diatoms were absent (Bergamino et al. 2016). This suggests that if abundant lower nutritional 6.3 Macroinvertebrate community effects on ecosystem functioning quality food sources are available, macroinvertebrate species can cope with a decreased The macroinvertebrate community of sandy beaches contributes to two main ecosystem availability of high nutritional quality food sources by strong competition. Hence, co-existence functions: 1) nutrient cycling and 2) food to support higher trophic levels, while adding to a is promoted between intertidal macroinvertebrates and overall non-additive effects of unique biodiversity exclusively associated with sandy beaches (Schlacher et al. 2007). Changes consumption may be maintained over a longer period of time. Furthermore, we have shown in community composition alter ecosystem functioning when species are lost or added with in Chapter 2 that intertidal macroinvertebrate densities can locally be high (see also Leewis et specific functional traits or when abundances of a functionally important species significantly al. 2012), indicating that biological interactions may potentially be important in driving increase or decrease (Hooper et al. 2005, Cardinale et al. 2006, Hillebrand et al. 2008). We intertidal macroinvertebrate community composition on sandy beaches. Biological have shown in Chapter 4 that supratidal macroinvertebrate community abundance, richness interactions should therefore not be disregarded when trying to understand and diversity were drivers of N and P mineralisation of wrack. Changes in supratidal macroinvertebrate community patterns of the intertidal zone and from the above, it can be macroinvertebrate community composition may therefore alter nutrient cycling and thus stated that the importance of biological interactions likely depends on a combination of ecosystem functioning, which has been shown on sandy beaches (Costa et al. 2017) and is in resource availability, macroinvertebrate density and macroinvertebrate diversity. line with general ecological theory (Hooper et al. 2005). Densities of supratidal In the supratidal zone, macroinvertebrates respond strongly to wrack in terms of abundance macroinvertebrates can, in addition, be locally high (Van Colen et al. 2005, Ruiz-Delgado et al. and richness (e.g. Olabarria et al. 2007, Colombini et al. 2009, Chapter 4). Wrack is deposited 2016), hence creating the potential to have a significant effect on ecosystem functioning over a restricted area on the beach and as supratidal macroinvertebrate species essentially (Hillebrand et al. 2008). Also in Chapter 4, Diptera larvae densities in wrack were similar to for use the same type of resource (i.e. wrack) for food and habitat (Ince et al. 2007, Ruiz-Delgado example Jędrzejczak (2002b), with on average 92 ± 15 (SE) Fucellia sp. larvae per litter bag et al. 2015), there is a potential for resource competition (Lastra et al. 2010). At the same time, (Chapter 4) against approximately 90 Fucellia tergina larvae per litter bag (Jędrzejczak 2002b), macroinvertebrates are expected to exhibit niche segregation in time and space to allow for in both studies after two weeks of field incubation, and thus relatively high. Furthermore, I co-existence on wrack patches (Lastra et al. 2010). The availability of wrack to the supratidal aimed in Chapter 5 to test the effect of the presence of T. saltator on the decomposition- macroinvertebrate community may differ between macroinvertebrate species within a single driven nutrient availability for beach pioneer plants, where macroinvertebrates were indeed drift line, as wrack traits that influence its resource use (e.g. nutritional quality and moisture found to enhance decomposition and mineralisation of wrack, but the effect of T. saltator content) differ between wrack species and decomposition stages (Orr et al. 2005, Liebowitz presence on final nutrient uptake by C. maritima appeared to be potentially influenced by the et al. 2016). In Chapter 4, a locally high abundance of Diptera larvae in wrack was observed competitive ability of both the microbial community and the individual plant for these while few T. saltator individuals were found, indicating a later successional stage of wrack was nutrients. In addition, early succession species, such as T. saltator may indirectly facilitate late sampled. Early succession macroinvertebrate species such as T. saltator may indirectly succession macroinvertebrate species e.g. due to their feeding activities on wrack and its facilitate late succession macroinvertebrate species such as Diptera larvae (e.g. Olabarria et biofilm (e.g. Olabarria et al. 2007). Talitrus saltator is in that case also indirectly responsible al. 2007). This suggests that resource availability (in terms of e.g. resource quality) changes for an increase in wrack decomposition and mineralisation. To summarise, the supratidal with decomposition stage of wrack, therefore supporting different macroinvertebrate species macroinvertebrate community appears to be an important driver of nutrient cycling on sandy at different moments in time. This is supported by the result that mineralisation of wrack is beaches. not uniform and depends on both abiotic and biotic factors (Chapter 4 and 5), which changes In addition to the effect of macroinvertebrate community on wrack mineralisation, the effect wrack availability to (subsequent) supratidal macroinvertebrate species. of season, wrack burial by sand and drift line position were investigated (Chapter 4 and 5).

140 Chapter 6

Even though the relative effect of wrack burial against macroinvertebrate community metrics, Table 6.1. Summary of N and P mineralisation of wrack (standardised per g of initial wrack) in the season and drift line remains unknown, since these were tested in two separate experiments, experiments performed in Chapter 4 and 5. Incubation periods were two and four weeks in Chapter 4 and two different macroalgae species (Ulva lactuca and Fucus sp. respectively) were used, a and 5 respectively. summary of the main drivers of wrack decomposition and mineralisation as assessed in this Treatment N mineralisation (mg) P mineralisation (mg) thesis is given (Figure 6.1). Litter bag experiment Spring 9.4 (± 0.9) 1.1 (± 0.1) Wrack patches found at drift lines higher up the supratidal zone are commonly buried by sand (Chapter 4) Summer 14.8 (± 2.6) 1.3 (± 0.1) (Hammann and Zimmer 2014). Sand burial had a large, positive effect on wrack mineralisation and subsequent beach pioneer plant growth (Chapter 5). However, in the field, litter bags Autumn 15.0 (± 2.6) 1.6 (± 0.1) containing wrack were (partly) buried by sand in both young and old drift lines. This could Mesocosm experiment Shallow 5.8 (± 1.8) 0.8 (± 0.2) have created similar environmental conditions compared to sand burial, potentially explaining (Chapter 5) Deep 16.1 (± 2.8) 2.2 (± 0.4) why no difference in wrack mineralisation was found between drift line positions in Chapter 4. Nevertheless, when comparing mineralisation between Chapter 4 and 5 (Table 6.1), mineralisation in the field was intermediate between mineralisation observed for shallow and deep buried wrack. It is important to note that the incubation period between experiments differed: two weeks in the litter bag experiment and four weeks in the mesocosm experiment. Since decomposition is a non-linear process which depends on a.o. macroalgae species (Jędrzejczak 2002a, Olabarria et al. 2007), we cannot calculate the exact mineralisation after two weeks in the mesocosm experiment, but it can be assumed that less material was decomposed than after four weeks of incubation. Mineralisation in the field, where a variety of factors affects wrack decomposition, may in that case actually be higher than in the mesocosm experiment. This suggests that sand burial of wrack was not the only factor influencing N and P mineralisation of wrack, supporting the results of Chapter 4. Indeed, mesocosm experiments may only capture a subset of possible mechanisms that occur under natural conditions in the field (e.g. Stachowicz et al. 2008). As to the second main ecosystem function, the macroinvertebrate community is an important food source for higher trophic levels (e.g. birds), thereby connecting marine and terrestrial food webs (McLachlan and Brown 2006). Changes in macroinvertebrate community composition are therefore expected to propagate upwards in the sandy beach food web and finally alter ecosystem functioning. Lower macroinvertebrate abundance may attract fewer predators, both in the intertidal (Peterson et al. 2006, Costa et al. 2017) and supratidal zone (Dugan et al. 2003, Reyes-Martínez et al. 2015). These predators, especially birds, are however crucial in linking the intertidal and supratidal zone, together forming the sandy beach food web. As a lower intertidal macroinvertebrate abundance and a different intertidal macroinvertebrate community composition was observed at the Sand Motor mega- nourishment compared to other sandy beaches (Chapter 2), this may influence predators depending on these food sources (e.g. Linnartz 2012). Shore birds avoid sandy beaches where prey availability is low in the intertidal zone e.g. due to anthropogenic pressures (Peterson et al. 2006, Costa et al. 2017). For the supratidal macroinvertebrate community, we assessed the Figure 6.1 Summary of the drivers of wrack decomposition and mineralisation on sandy beaches. macroinvertebrate community composition associated with wrack (Chapter 4), but how these Arrows indicate processes (identified in bold text) between biotic and abiotic ecosystem components. findings relate to wrack communities on other Dutch sandy beaches and the subsequent effect Thickness of arrows indicate the strength of the relationship. All relationships are positive, except for on predators is unclear due to a lack of relevant studies. As indicated above, Diptera larvae the effect of drift line position which can be neutral (also indicated within the figure). abundance in wrack was similar compared to e.g. Jędrzejczak (2002b), suggesting predators such as birds may benefit from the availability of this prey source (Dugan et al. 2003).

General discussion 141

142 Chapter 6

It is clear that both the intertidal and supratidal macroinvertebrate community are involved Motor mega-nourishment therefore has a direct effect on the macroinvertebrate community in the recycling of nutrients via both bottom-up (consumption and decomposition of organic by changing beach habitat characteristics. As different intertidal ecosystems (e.g. mud and matter) and top-down processes (being available as prey to predators) on sandy beaches. The sand flats) hold different species and show different food web characteristics, habitat diversity results of this thesis thus strengthen the idea of a central role of the macroinvertebrate is likely important in maintaining overall ecosystem functioning (Horn et al. 2017). community within sandy beach ecosystem functioning. This is in line with observations in The development of a beach with a high mud and organic matter content (Wijsman 2016), the other ecosystems, such as salt marshes (Schrama et al. 2015), freshwater stream ecosystems formation of a microbial mat in the supratidal zone (personal observation, Figure 6.2) and the (Wallace and Webster 1996, Covich 1999) and terrestrial soil ecosystems (e.g. Heemsbergen presence of wrack patches colonised by macroinvertebrates and support pioneer plants et al. 2004, Lavelle et al. 2006). (Chapter 4, personal observation Figure 6.3) at the lagoon of the Sand Motor mega- nourishment, raises the question whether there is the potential for green beach development Take home message: Mineralisation of wrack is mainly driven by season, wrack burial and (Bakker et al. 2005, Esselink et al. 2009). Green beaches consist of a mosaic of salt marsh and supratidal macroinvertebrate abundance, and supports beach pioneer plant growth dune vegetation in combination with microbial mats and develop on the seaward side of a dune ridge (De Groot et al. 2017a, Esselink et al. 2017). Salt marsh succession has been shown 6.4 Mega-nourishment effects on the sandy beach ecosystem to be initiated by a decomposer-based food web, with a significant contributing role of microbial mats, rather than a terrestrial plant-based food web (Schrama et al. 2012). In Mega-nourishments are not fundamentally different from other sand nourishments, but do particular, Diptera larvae of the species Fucellia maritima present on wrack deposits are a differ in shape, size and frequency. Consequently, a mega-nourishment can have direct (e.g. dominant detritivore group in the first years of salt marsh succession (Schrama et al. 2012). In change in habitat characteristics) and indirect (e.g. change in dispersal and food availability) Chapter 4 we found that Fucellia sp. larvae were also the most abundant group on wrack effects on the macroinvertebrate community and the sandy beach ecosystem that differ from adjacent to the lagoon. Thus, marine organic input plays an important role in initiating early other types of sand nourishment. The results of Chapter 3 suggest that the Sand Motor mega- succession of coastal ecosystems and facilitating pioneer plant establishment (Chapter 4 and nourishment could have an indirect effect on the intertidal macroinvertebrate community by 5). Another important factor for green beach development is the stabilization of the sand and changing food availability. The hook-shape of the Sand Motor mega-nourishment resulted in provision of nutrients to pioneer plants via a microbial mat (Leewis 2017), which mainly significant changes in local hydrodynamics (Meirelles et al. 2017). This is expected to influence consists of cyanobacteria and benthic microalgae that fix nitrogen (Severin and Stal 2008, the distribution of organic particles (including diatoms), as these are strongly driven by Dijkman et al. 2010, Bolhuis and Stal 2011). Already in the first year after construction (2012) hydrodynamic processes which are related to the coastal morphology of a certain beach of the Sand Motor mega-nourishment, a microbial mat was present at the lagoon. However, (Shanks et al. 2017, Morgan et al. 2018). Phytoplankton may then become an important food up till now (2018, seven years after construction), no plants have established on this microbial source for the intertidal macroinvertebrate community in highly hydrodynamic environments (Menge 2000), for example around at the hook of the Sand Motor mega-nourishment. Indeed, intertidal macroinvertebrates do change their feeding behaviour, hence biological interactions, based on food availability in the field, with surf zone diatoms being a more important food source at dissipative than reflective beaches (Bergamino et al. 2016, Shanks et al. 2017). Measurements identifying the distribution of phytoplankton and relating this to the intertidal macroinvertebrate community in the field is necessary to establish this link directly. A relatively extensive system of tidal (sand) flats has been formed north and south of the Sand Motor mega-nourishment (from 2013 onwards) as a result of the distribution of sand originating from the hook of the Sand Motor mega-nourishment (Figure 1.3 in the General Introduction). A mosaic of intertidal micro-habitats with varying environmental conditions is created in this way, which may facilitate a higher intertidal macroinvertebrate abundance and richness as observed south of the Sand Motor mega-nourishment (Chapter 2). Interestingly, this result was not related solely to median grain size, supporting the growing notion that intertidal macroinvertebrate communities are assembled by a complex set of drivers including both abiotic factors and food availability (e.g. Rodil et al. 2012). Furthermore, the shape of the Figure 6.2 Microbial mat formation at the south-east side of the lagoon of the Sand Motor mega- nourishment (left: overview, lower right: detail). Directly below the surface of the microbial mat a black Sand Motor mega-nourishment created a hydrodynamically benign beach with a high mud layer of sand is observed (upper right picture), indicating anoxic conditions due to the presence of iron and organic matter content (Wijsman 2016), resulting in the attraction of a distinct intertidal sulphide (Pit et al. 2018, Bolhuis and Stal 2011). macroinvertebrate community typically associated with mud flats (Chapter 2). The Sand

General discussion 143

144 Chapter 6 mat. This may be due to a combination of factors including the lack of increased shelter by embryo dunes, high sand supply and low supply of fresh water (Bakker et al. 2005, van Puijenbroek 2018). Even mega-nourishments that were specifically designed to facilitate green beach succession did not develop as such to date (van Puijenbroek 2018). The lagoon at the Sand Motor mega-nourishment therefore seems unlikely to develop into a green beach or salt marsh, even though (parts of) the initial successional stage of a salt marsh ecosystem is present with a dominant role for the brown, decomposer-based food web (Schrama et al. 2012, Schrama et al. 2016). In the general introduction, a conceptual scheme was proposed that indicated the expected effects of a change in coastal zone geomorphology (placement of a mega-nourishment) on niche-based community assembly and ecosystem functioning (Figure 1.4. Based on the outcomes of this thesis, I will indicate for which links evidence was found (Figure 6.4). For the intertidal macroinvertebrate community, we found that dispersal was not strongly limiting richness at the Sand Motor mega-nourishment as there was no effect of year after nourishment (Chapter 2), even though local hydrodynamic forces did change (Meirelles et al. 2017). No effect of median grain size was found on the intertidal macroinvertebrate community of the wave-exposed locations at the mega-nourishment, but the hook of the Sand Motor mega-nourishment did result in a change in beach environment and subsequent intertidal macroinvertebrate community composition (Chapter 2). The hook protected part of the beach from hydrodynamic forces thus enhancing habitat relief, which resulted in a benign Figure 6.4 A model of niche-based community assembly and the impact of changes in coastal zone lagoon which finally attracted a distinct intertidal macroinvertebrate community. The link geomorphology (placement of a mega-nourishment) on the three filters: dispersal, environmental and between a change in coastal zone geomorphology and resource availability via a change in limiting similarity, which are indicated above. A change in the coastal zone geomorphology can have both direct effects (continuous arrows in the lower part of the figure) and indirect effects (dotted hydrodynamic forces was not explicitly studied, but the results of Chapter 3 indicate that even arrows in the lower part of the figure) on the assembly filters. After each filter, fewer species remain though diatom availability to the intertidal macroinvertebrate community changes species in the species pool, finally resulting in a specific biological community (the far-right and smallest circle). interactions, co-existence can occur at least temporally. Whether this holds over a longer This actual biological community then influences ecosystem functioning. Numbers in brackets period of time remains the question. The presence of benthic microalgae as an additional food correspond to the chapters in this thesis that provided evidence for specific links and whether these were found to have a neutral, positive or negative effect on the intertidal macroinvertebrate community. source in the lagoon can furthermore support co-existence of intertidal macroinvertebrates. Finally, Chapter 2 clearly showed that a mega-nourishment changes intertidal macroinvertebrate community composition, but subsequent effects on ecosystem functioning (e.g. nutrient cycling) have not been studied so far. Adapting this model for the supratidal zone works less well, as links between changes in the coastal zone geomorphology and the supratidal macroinvertebrate community are expected to be less pronounced compared to the intertidal zone. These links have not been explicitly tested in this thesis. It is therefore more useful to implement knowledge on the relationship between supratidal macroinvertebrate community composition and wrack mineralisation (Figure 6.1) to apply to coastal management, e.g. after construction of a mega-nourishment.

Take home message: A mega-nourishment creates novel habitat for intertidal Figure 6.3 Pioneer plant growth (left: Honckenya peploides, right: Cakile maritima) in a drift line on the macroinvertebrates, but abundance is lower than at regular beach nourishments beach of the Sand Motor mega-nourishment.

General discussion 145 mat. This may be due to a combination of factors including the lack of increased shelter by embryo dunes, high sand supply and low supply of fresh water (Bakker et al. 2005, van Puijenbroek 2018). Even mega-nourishments that were specifically designed to facilitate green beach succession did not develop as such to date (van Puijenbroek 2018). The lagoon at the Sand Motor mega-nourishment therefore seems unlikely to develop into a green beach or salt marsh, even though (parts of) the initial successional stage of a salt marsh ecosystem is present with a dominant role for the brown, decomposer-based food web (Schrama et al. 2012, Schrama et al. 2016). In the general introduction, a conceptual scheme was proposed that indicated the expected effects of a change in coastal zone geomorphology (placement of a mega-nourishment) on niche-based community assembly and ecosystem functioning (Figure 1.4. Based on the outcomes of this thesis, I will indicate for which links evidence was found (Figure 6.4). For the intertidal macroinvertebrate community, we found that dispersal was not strongly limiting richness at the Sand Motor mega-nourishment as there was no effect of year after nourishment (Chapter 2), even though local hydrodynamic forces did change (Meirelles et al. 2017). No effect of median grain size was found on the intertidal macroinvertebrate community of the wave-exposed locations at the mega-nourishment, but the hook of the Sand Motor mega-nourishment did result in a change in beach environment and subsequent intertidal macroinvertebrate community composition (Chapter 2). The hook protected part of the beach from hydrodynamic forces thus enhancing habitat relief, which resulted in a benign Figure 6.4 A model of niche-based community assembly and the impact of changes in coastal zone lagoon which finally attracted a distinct intertidal macroinvertebrate community. The link geomorphology (placement of a mega-nourishment) on the three filters: dispersal, environmental and between a change in coastal zone geomorphology and resource availability via a change in limiting similarity, which are indicated above. A change in the coastal zone geomorphology can have both direct effects (continuous arrows in the lower part of the figure) and indirect effects (dotted hydrodynamic forces was not explicitly studied, but the results of Chapter 3 indicate that even arrows in the lower part of the figure) on the assembly filters. After each filter, fewer species remain though diatom availability to the intertidal macroinvertebrate community changes species in the species pool, finally resulting in a specific biological community (the far-right and smallest circle). interactions, co-existence can occur at least temporally. Whether this holds over a longer This actual biological community then influences ecosystem functioning. Numbers in brackets period of time remains the question. The presence of benthic microalgae as an additional food correspond to the chapters in this thesis that provided evidence for specific links and whether these were found to have a neutral, positive or negative effect on the intertidal macroinvertebrate community. source in the lagoon can furthermore support co-existence of intertidal macroinvertebrates. Finally, Chapter 2 clearly showed that a mega-nourishment changes intertidal macroinvertebrate community composition, but subsequent effects on ecosystem functioning (e.g. nutrient cycling) have not been studied so far. Adapting this model for the supratidal zone works less well, as links between changes in the coastal zone geomorphology and the supratidal macroinvertebrate community are expected to be less pronounced compared to the intertidal zone. These links have not been explicitly tested in this thesis. It is therefore more useful to implement knowledge on the relationship between supratidal macroinvertebrate community composition and wrack mineralisation (Figure 6.1) to apply to coastal management, e.g. after construction of a mega-nourishment.

146 Chapter 6

6.5 Recommendations for future sand nourishments and coastal management diverse supratidal macroinvertebrate community, especially in summer. Summer is however also the period when the pressure of recreation is high and beaches are intensively cleaned Based on the above, recommendations are given for the development of future mega- (McLachlan and Brown 2006). The Sand Motor mega-nourishment was positioned in an area nourishments and coastal management to be applied on sandy beaches in general, to support with a high recreational pressure (Jonker and Janssen 2007) and was therefore expected to the sandy beach ecosystem and macroinvertebrate communities in particular. attract many beach visitors. In 2004, Scheveningen, the beach directly north of the Sand Motor First, a future mega-nourishment should be highly heterogeneous in shape, creating a variety mega-nourishment, is yearly visited by 560.000 people and Kijkduin, the beach directly south of habitats of exposed versus sheltered beach areas to temporally enhance intertidal of the Sand Motor mega-nourishment, is visited by 428.000 people a year (Otto 2004 in Jonker macroinvertebrate diversity (Chapter 2). Sheltered habitats also lead to local concentrations and Janssen 2007). These numbers are not expected to have changed considerably over the of diatoms, promoting co-existence of intertidal macroinvertebrate species (Chapter 3) or years, as beach recreation remains to be popular and was an additional management goal of potentially accumulate wrack of a different species composition and total mass (Orr et al. this mega-nourishment. High recreational pressure may, however, have a negative effect on 2005, Liebowitz et al. 2016). This may initiate the early successional stage of green beach both intertidal and supratidal macroinvertebrates, for example by trampling, high use of off- development (Schrama et al. 2012). Secondly, the beach should have a gentle slope to create road vehicles and wrack removal during beach cleaning (Defeo et al. 2009, Schlacher et al. a dissipative beach, which also reduces hydrodynamic stress on macroinvertebrate 2016). At the Sand Motor mega-nourishment itself, wrack was allowed to remain on the beach communities. A wider beach is then created with a wider intertidal zone, with a greater and beaches were cleaned by handpicking trash bi-monthly (John van Nierop, personal potential for nature to develop. The highest part of the Sand Motor mega-nourishment was communication). Beaches directly adjacent to the Sand Motor mega-nourishment, however, 7.3 m above NAP (NAP being the Dutch datum at mean sea level (MSL)) directly after were mechanically cleaned from all trash and organic material by a beach cleaner, either daily construction, creating a relatively steep increase from the low water line to the highest part in summer (May-September) or as required outside this period (John van Nierop, personal of the beach (De Schipper et al. 2016). On the northern part of the hook, even ‘sand cliffs’ up communication). This is where the municipality border runs and Dutch municipalities are able to 1.5 m high were formed over the first years after construction as erosion occurred, resulting to make their own decisions regarding beach cleaning management. The Sand Motor mega- in an artificial break in the cross-shore beach profile (Linnartz 2012, personal observation). nourishment may have acted as a ‘refuge’ for supratidal macroinvertebrates, where food and This is expected to have a negative effect on both the intertidal and supratidal shelter in the form of wrack was available in contrast to adjacent beaches. Throughout the macroinvertebrate community and should therefore be avoided, which potentially is achieved year, Dutch sandy beaches are irregularly cleaned among others depending on season, by reducing the total height above MSL and the beach slope. Thirdly, a future mega- tourism activity and funds and equipment available. It is therefore unclear at what distance nourishment is ideally designed as an island to minimise anthropogenic impacts on from the Sand Motor mega-nourishment the next ‘refuge’ was situated for supratidal macroinvertebrate communities. An island is harder to reach for humans and results in less macroinvertebrates, which may have influenced community assembly processes related to anthropogenic disturbance of macroinvertebrate communities. A wide variety of dispersal and migration. anthropogenic activities has been observed at the Sand Motor mega-nourishment on many It is advisable to indicate the importance of wrack for the sandy beach ecosystem to those occasions (personal observation), suggesting that these may have influenced responsible for beach cleaning management at the coastal municipalities. Measures worth macroinvertebrate communities negatively (Defeo et al. 2009, Schlacher et al. 2016). considering to reduce the impact of beach cleaning on the sandy beach ecosystem include 1) Alternatively, if the development of embryo dunes is desired, it is recommended to place the reducing the frequency of beach cleaning (e.g. to monthly or every other week), 2) mega-nourishment attached to the coast line allowing for embryo dunes to become part of repositioning the collected wrack to decompose within the same beach, retaining the the current dune system. A future mega-nourishment is thus ideally heterogeneous in habitat, nutrients in the system, 3) clean only a part of the beach, where uncleaned beaches facilitate with both exposed and sheltered beach habitats, has a dissipative beach and is as much as recolonisation by supratidal macroinvertebrates of freshly deposited wrack after beach possible protected from anthropogenic disturbances. cleaning, and 4) manually cleaning beaches where possible, removing trash only and leaving Further coastal management should focus on allowing wrack to remain on the beach as it is the structure of wrack intact (Dugan and Hubbard 2010, Morton et al. 2015). Ideally, an the foundation of the sandy beach ecosystem. In Chapter 5 we found that buried wrack was inventory is made of the entire sandy coast line of the Netherlands, indicating where, how and an important driver of beach pioneer plant growth, indicating the importance of leaving wrack how often wrack is cleaned from sandy beaches. Adjacent coastal municipalities are then able untouched after deposition on the beach (i.e. at least up to several weeks). Talitrus saltator to communicate and align their beach cleaning activities, allowing wrack to be maintained on was found to be a driver of decomposition-driven nutrient availability for beach pioneer the sandy beach as much as possible in support of the sandy beach ecosystem. It would be plants, affecting plant nutrient dynamics. The field experiment performed in Chapter 4 even more effective if beach cleaning activities are included in coastal management on a showed that wrack attracted a variety of supratidal macroinvertebrate species, which likely national level as part of the nature conservation policy. Surprisingly, the supratidal zone is had a positive effect on mineralisation of wrack. In particular, this experiment stressed the currently not part of any Natura 2000 habitat type or only partly protected under the Birds importance of leaving wrack undisturbed on nourished beaches (and elsewhere) to support a and Habitat Directive (De Groot et al. 2017b). This calls for a nation and European wide change

General discussion 147

148 Chapter 6 in policy related to sandy beach ecosystems by including the supratidal zone to protect wrack would in that light be a valuable research avenue, as such studies have previously focused on communities. the intertidal zone alone (e.g. McLachlan et al. 1981). More generally, sandy beach studies now need to move from primarily trying to understand changes in community composition Sand nourishments are primarily designed to protect the hinterland against flooding, but may and food webs, but more specifically address the question how these changes alter ecosystem be intended to serve several other purposes. After a nourishment has been placed, coastal functioning (see Costa et al. 2017). For example, this question could be addressed by studying management thus continues. Beach management after placement of the nourishment can be the effect of supratidal macroinvertebrate community composition on decomposition and based on the identification of two key factors: conservation value and recreational potential nutrient mineralisation of wrack of different quality (e.g. macroalgae species) in a mesocosm of the sandy beach (McLachlan et al. 2013). Beaches in urban areas such as in the Netherlands experiment. can be best managed for multiple-purpose use, covering both aspects of ecological conservation and recreation. Thus, a compromise has to be achieved between what ecologists Follow-up studies on the intertidal macroinvertebrate community related to the Sand Motor suggest as optimal solutions and what local stakeholders will allow for the sandy beach in mega-nourishment should focus on the spatial and temporal variations of the intertidal question. macroinvertebrate over a longer period of time, as the shape of the Sand Motor mega- nourishment will continue to change. Only the first four years of monitoring after construction of the Sand Motor mega-nourishment could be included in Chapter 2. Whether abundance Take home message: A future mega-nourishment should be heterogeneous in habitats, have would increase and community composition converges to or further deviates from regular a dissipative beach and be protected from anthropogenic disturbances beach nourishment over the coming years, requires continuous monitoring of the intertidal macroinvertebrate community. In particular, the intertidal macroinvertebrate community of 6.6 Research agenda the lagoon should be monitored more intensively, in concert with taking sediment and water As with all research, while some questions received an answer in this thesis, new questions samples to assess the relation between the intertidal community and food availability have emerged. New research avenues related to the findings of this thesis are hence identified (primarily benthic microalgae). Together, this will provide more insight on the effects of a low below. frequency of sand nourishment on the intertidal macroinvertebrate community on a temporal and spatial scale. It is further interesting to study the relationship between wrack input and Resource availability showed to be important in changing species interactions and its supratidal macroinvertebrate community composition at a mega-nourishment in consumption by intertidal macroinvertebrates (Chapter 3), but it remains unclear exactly how comparison to other types of sand nourishment. Since a mega-nourishment is expected to this translates to changes in community composition and finally ecosystem functioning. Long- change the coastal zone geomorphology considerably, wrack input may subsequently change term mesocosm studies would allow for testing the effect of changing species interactions (Orr et al. 2005, Liebowitz et al. 2016, Reimer et al. 2018). Ideally, this would include studying related to food availability and give further insight in intertidal macroinvertebrate community wrack and its supratidal macroinvertebrate community at the sandy beach both before and assembly processes over time, but may be hard to establish. In the field, a study to determine after construction of the mega-nourishment, in the same time of year to account for seasonal the link between the intertidal macroinvertebrate community composition and diatom differences in wrack input and supratidal macroinvertebrate community composition (as availability would be interesting to perform, supplementing the results of the mesocosm shown in Chapter 4 for the latter). As an alternative, sandy beaches representing a range of experiment (Chapter 3). This study could then include the identification of both juveniles and potential changes in coastal zone geomorphology as a result of sand nourishment could be adults in the intertidal macroinvertebrate community, linking species interactions and sampled. This will improve our understanding of how a change in coastal zone geomorphology community composition via population dynamics of individual macroinvertebrate species. By changes wrack input to sandy beaches and subsequently supratidal macroinvertebrate also identifying abiotic factors that may structure the intertidal macroinvertebrate community community composition. (such as beach slope and median grain size), an assessment of the relative importance of abiotic and biotic factors in intertidal macroinvertebrate community assembly on sandy Finally, it is striking that sandy beach monitoring programs in the Netherlands are solely beaches can be made. Insights on this topic have recently started to emerge, but deserve focused on the intertidal and subtidal macroinvertebrate communities or the dune ecosystem, further attention (HilleRisLambers et al. 2012, Schlacher et al. 2015). but the supratidal zone is structurally being ignored. Few studies have focused on wrack and (succession of) the supratidal macroinvertebrate community in the Netherlands (but see As for ecosystem functioning, sandy beaches provide many ecosystem functions, including Schrama et al. 2012, Leewis 2017), thus requiring more study in the Dutch context (Cadée nutrient cycling, but this has rarely been quantified (Schlacher et al. 2008, Nel et al. 2014). The 2014). Especially on the Wadden islands in the north of the Netherlands, wrack is allowed to results of Chapter 4 and 5 place emphasis on the importance of cross-boundary connectivity accumulate and reach a higher macroinvertebrate abundance and richness than on sandy in the context of sandy beaches as a subsidised ecosystem (Polis and Hurd 1996, Schlacher et beaches along the Dutch coast (Schrama et al. 2012, Cadée 2014). This provides an interesting al. 2015; Gounand et al. 2018). Identifying nutrient cycling and performing food web analysis opportunity to study the relationship between wrack mineralisation and pioneer plant growth of the entire sandy beach ecosystem, thus including both the intertidal and supratidal zone, and the role of macroinvertebrates in this process, which will improve our understanding of

General discussion 149 in policy related to sandy beach ecosystems by including the supratidal zone to protect wrack would in that light be a valuable research avenue, as such studies have previously focused on communities. the intertidal zone alone (e.g. McLachlan et al. 1981). More generally, sandy beach studies now need to move from primarily trying to understand changes in community composition Sand nourishments are primarily designed to protect the hinterland against flooding, but may and food webs, but more specifically address the question how these changes alter ecosystem be intended to serve several other purposes. After a nourishment has been placed, coastal functioning (see Costa et al. 2017). For example, this question could be addressed by studying management thus continues. Beach management after placement of the nourishment can be the effect of supratidal macroinvertebrate community composition on decomposition and based on the identification of two key factors: conservation value and recreational potential nutrient mineralisation of wrack of different quality (e.g. macroalgae species) in a mesocosm of the sandy beach (McLachlan et al. 2013). Beaches in urban areas such as in the Netherlands experiment. can be best managed for multiple-purpose use, covering both aspects of ecological conservation and recreation. Thus, a compromise has to be achieved between what ecologists Follow-up studies on the intertidal macroinvertebrate community related to the Sand Motor suggest as optimal solutions and what local stakeholders will allow for the sandy beach in mega-nourishment should focus on the spatial and temporal variations of the intertidal question. macroinvertebrate over a longer period of time, as the shape of the Sand Motor mega- nourishment will continue to change. Only the first four years of monitoring after construction of the Sand Motor mega-nourishment could be included in Chapter 2. Whether abundance Take home message: A future mega-nourishment should be heterogeneous in habitats, have would increase and community composition converges to or further deviates from regular a dissipative beach and be protected from anthropogenic disturbances beach nourishment over the coming years, requires continuous monitoring of the intertidal macroinvertebrate community. In particular, the intertidal macroinvertebrate community of 6.6 Research agenda the lagoon should be monitored more intensively, in concert with taking sediment and water As with all research, while some questions received an answer in this thesis, new questions samples to assess the relation between the intertidal community and food availability have emerged. New research avenues related to the findings of this thesis are hence identified (primarily benthic microalgae). Together, this will provide more insight on the effects of a low below. frequency of sand nourishment on the intertidal macroinvertebrate community on a temporal and spatial scale. It is further interesting to study the relationship between wrack input and Resource availability showed to be important in changing species interactions and its supratidal macroinvertebrate community composition at a mega-nourishment in consumption by intertidal macroinvertebrates (Chapter 3), but it remains unclear exactly how comparison to other types of sand nourishment. Since a mega-nourishment is expected to this translates to changes in community composition and finally ecosystem functioning. Long- change the coastal zone geomorphology considerably, wrack input may subsequently change term mesocosm studies would allow for testing the effect of changing species interactions (Orr et al. 2005, Liebowitz et al. 2016, Reimer et al. 2018). Ideally, this would include studying related to food availability and give further insight in intertidal macroinvertebrate community wrack and its supratidal macroinvertebrate community at the sandy beach both before and assembly processes over time, but may be hard to establish. In the field, a study to determine after construction of the mega-nourishment, in the same time of year to account for seasonal the link between the intertidal macroinvertebrate community composition and diatom differences in wrack input and supratidal macroinvertebrate community composition (as availability would be interesting to perform, supplementing the results of the mesocosm shown in Chapter 4 for the latter). As an alternative, sandy beaches representing a range of experiment (Chapter 3). This study could then include the identification of both juveniles and potential changes in coastal zone geomorphology as a result of sand nourishment could be adults in the intertidal macroinvertebrate community, linking species interactions and sampled. This will improve our understanding of how a change in coastal zone geomorphology community composition via population dynamics of individual macroinvertebrate species. By changes wrack input to sandy beaches and subsequently supratidal macroinvertebrate also identifying abiotic factors that may structure the intertidal macroinvertebrate community community composition. (such as beach slope and median grain size), an assessment of the relative importance of abiotic and biotic factors in intertidal macroinvertebrate community assembly on sandy Finally, it is striking that sandy beach monitoring programs in the Netherlands are solely beaches can be made. Insights on this topic have recently started to emerge, but deserve focused on the intertidal and subtidal macroinvertebrate communities or the dune ecosystem, further attention (HilleRisLambers et al. 2012, Schlacher et al. 2015). but the supratidal zone is structurally being ignored. Few studies have focused on wrack and (succession of) the supratidal macroinvertebrate community in the Netherlands (but see As for ecosystem functioning, sandy beaches provide many ecosystem functions, including Schrama et al. 2012, Leewis 2017), thus requiring more study in the Dutch context (Cadée nutrient cycling, but this has rarely been quantified (Schlacher et al. 2008, Nel et al. 2014). The 2014). Especially on the Wadden islands in the north of the Netherlands, wrack is allowed to results of Chapter 4 and 5 place emphasis on the importance of cross-boundary connectivity accumulate and reach a higher macroinvertebrate abundance and richness than on sandy in the context of sandy beaches as a subsidised ecosystem (Polis and Hurd 1996, Schlacher et beaches along the Dutch coast (Schrama et al. 2012, Cadée 2014). This provides an interesting al. 2015; Gounand et al. 2018). Identifying nutrient cycling and performing food web analysis opportunity to study the relationship between wrack mineralisation and pioneer plant growth of the entire sandy beach ecosystem, thus including both the intertidal and supratidal zone, and the role of macroinvertebrates in this process, which will improve our understanding of

150 Chapter 6 how the marine and terrestrial ecosystems are connected and of the drivers of the first stage of salt marsh and/or dune succession (Schrama et al. 2012, Schrama et al. 2015).

Take home message: Future studies need to focus on linking community composition to ecosystem functioning on sandy beaches, especially for the largely neglected supratidal macroinvertebrate community associated with wrack

6.7 Conclusions This thesis showed a clear effect of resource availability on macroinvertebrate species interactions and subsequent consumption in the intertidal zone, which may indirectly affect community composition. Biological interactions related to resource availability therefore cannot be ignored when aiming to understand macroinvertebrate community assembly on sandy beaches. Also, it has been shown here that it is crucial for both the supratidal macroinvertebrate community and sandy beach ecosystem functioning that wrack is maintained on sandy beaches. The results of this thesis therefore emphasise the link between the marine and terrestrial ecosystems, with a central role for the macroinvertebrate community in sandy beach ecosystem functioning, in particular decomposition and nutrient cycling. For the first time, the effect of a large-scale sand nourishment on the intertidal macroinvertebrate community has been studied. In terms of the intertidal macroinvertebrate community, it is concluded that a mega-nourishment appears to be a promising coastal defence strategy compared to regular beach nourishment, at least during the first years after construction. Overall, this thesis highlights the need to include the effect of resource availability on both the intertidal and macroinvertebrate community and the sandy beach ecosystem as a whole, especially when designing and planning future coastal management practices.

how the marine and terrestrial ecosystems are connected and of the drivers of the first stage of salt marsh and/or dune succession (Schrama et al. 2012, Schrama et al. 2015).

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Vanden Eede, S., Van Tomme, J., De Busschere, C., Vandegehuchte, M.L., Sabbe, K., Stienen, E.W.M., Degraer, S., Vincx, M. and Bonte, D. 2014. Assessing the impact of beach nourishment on the intertidal food web through the development of a mechanistic-envelope model. Journal of Applied Ecology, 51: 1304-1313.

Vander Zanden, M.K. and Rasmussen, J.B. 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography, 46: 2061-2066.

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Whitman, R., Harwood, V.J., Edge, T.A., Nevers, M., Byappanahalli, M., Vijayavel, K., Brandão, J., Sadowsky, M.J., Alm, E.W., Crowe, A., Ferguson, D., Ge, Z., Halliday, E., Kinzelman, J., Kleinheinz, G., Przybyla-Kelly, K., Staley, C., Staley, Z. and Solo-Gabriele, H.M. 2014. Microbes in beach sands: Integrating environment, ecology and public health. Reviews in Environmental Science and Bio/Technology, 13: 329-368.

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Vander Zanden, M.K. and Rasmussen, J.B. 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography, 46: 2061-2066.

Villéger, S., Ferraton, F., Mouillot, D. and de Wit, R. 2012. Nutrient cycling by coastal macrofauna: Intra- versus interspecific differences. Marine Ecology Progress Series, 452: 297-303.

Wallace, J.B. and Webster, J.R. 1996. The role of macroinvertebrates in stream ecosystem functioning. Annual Review of Entomology, 41: 115-139.

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Williams, A. and Feagin, R. 2010. Sargassum as a natural solution to enhance dune plant growth. Environmental Management, 46: 738-747.

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Summary

174 Summary

Sandy beaches are among the most prevalent coastal ecosystems in the world, harbouring characteristics of the mega-nourishment. Altered local hydrodynamics around a mega- unique ecological communities and providing many ecosystem functions, including the nourishment may, for example, change macroinvertebrate dispersal patterns and resource buffering of wave energy and nutrient cycling. Due to the highly dynamic nature of sandy availability. This, in turn, may influence species interactions and drive community assembly, beaches, the in situ primary production is low and the availability of marine exogeneous resulting in the actual macroinvertebrate community composition present on a sandy beach. organic matter, in the form of phytoplankton (intertidal zone) and beach-cast macroalgae So far, the effect of a mega-nourishment on the macroinvertebrate communities and how this (supratidal zone), are highly heterogenous in time and space. The sandy beach food web is, compares to regular sand nourishment has not been studied. therefore, heavily dependent on this marine exogeneous organic matter and is thus primarily The main aims of this thesis were, therefore, to 1) improve our understanding of the effect of bottom-up controlled. In particular, the macroinvertebrate communities of the intertidal and resource availability on macroinvertebrate community dynamics and ecosystem functioning supratidal zone together form the link between marine primary production and higher trophic on sandy beaches, and 2) investigate the effect of a mega-nourishment on the levels, via microalgae consumption, wrack decomposition and as food for predators, thereby macroinvertebrate community of the sandy beach. For these purposes, I conducted both connecting the marine and terrestrial food webs. The macroinvertebrate community mainly laboratory experiments and field work in the Netherlands and worked both in the intertidal includes polychaete worms, amphipods, isopods and insects, which reside either a few and supratidal zone to cover the entire beach. centimetres in the sand or in piles of beach-cast macroalgae (termed wrack). A relatively clear separation between the intertidal and supratidal zone exists on sandy beaches. Twice a day, In Chapter 2 the spatial and temporal effects on the intertidal macroinvertebrate community intertidal sands alternate between being either dry or saturated by sea water due to the lunar after placement of a mega-nourishment were assessed. In addition, the intertidal community tidal cycle. Macroinvertebrate species living in the intertidal zone are well adapted to this composition at the mega-nourishment was compared to communities present on beaches dynamic environment. This is reflected by most species being filter or deposit feeders that subject to regular beach nourishment and unnourished beaches. To do this, we obtained, catch organic particles floating in the water column or laying on the bottom. In contrast to the combined and analysed macroinvertebrate field data from three different data sets, one data intertidal zone, the supratidal zone is very rarely submerged by the sea during the tidal cycle, set contained data for the Sand Motor mega-nourishment, while the other two data sets as it is located between the high water line and the dune foot, and the sand remains dry for a contained data on both beaches subject to regular beach nourishment and unnourished large part of the time. Wrack is important for supratidal invertebrates by serving both as a beaches, all along the Dutch coast. There were strong spatial effects within the mega- source of food and refuge (e.g. protection from desiccation and predation by birds). However, nourishment, where a distinct intertidal macroinvertebrate community, consisting of species it remains unclear how resource availability influences species interactions and community commonly encountered on intertidal mudflats, was present in the lagoon as compared to the assembly of the macroinvertebrate community on sandy beaches, and how this influences ecosystem functioning. wave-exposed locations of the mega-nourishment. The mega-nourishment thus locally gives rise to a habitat that attracts a different intertidal macroinvertebrate community as compared While of critical ecological importance, sandy beach ecosystems are globally under threat. Due to wave-exposed beaches. Wave-exposed locations at the mega-nourishment had a higher to coastal squeeze, sandy beaches are trapped between the rising sea level and an increase in macroinvertebrate richness, lower macroinvertebrate abundance and did not converge into a storm events due to climate change on the sea side on the one hand, and static anthropogenic macroinvertebrate community composition similar to those on regularly nourished and structures on the land side on the other hand. On a global scale, the coastal zone, including unnourished beaches. A mega-nourishment may thus result in an altered intertidal sandy beaches, is usually densely populated by humans and coastal populations are only macroinvertebrate community with potential cascading effects within the sandy beach food expected to further increase. This combination of factors causes severe erosion of the sandy beach, threatening the human population and livelihood as the sea advances inland, leaving web. only a narrow strip of beach for ecological communities to reside. To mitigate the effects of Chapter 3 focused on the effect of diatom availability on the non-additive effects of erosion, sand nourishment has been widely applied, but recently a mega-nourishment (the consumption by a three-species intertidal macroinvertebrate community. A mesocosm study Sand Motor pilot project) was proposed as a more ecological and sustainable alternative to was performed in which we quantified isotopically labelled diatom consumption by three regular sand nourishment. A mega-nourishment is created by placing a large volume of sand macroinvertebrate species (Bathyporeia pilosa, Haustorius arenarius and Scolelepis concentrated on a small stretch of coast, which then gradually nourishes up-stream beaches squamata), kept in either monocultures or a three-species community at a range of diatom over a long period of time. This lowers the number of pulse disturbances to the sandy beach densities. The amphipod B. pilosa was the most successful competitor in terms of ecosystem compared to regular sand nourishment. As the macroinvertebrate community is a consumption at both high and low diatom availability, while the amphipod H. arenarius and key component of the sandy beach ecosystem, it is crucial to understand what drives assembly the polychaete worm S. squamata consumed less in the community than in their respective of macroinvertebrate communities on sandy beaches in general and after nourishments in monocultures. Non-additive effects of consumption were present and larger than mere particular. After application of a mega-nourishment, macroinvertebrate communities have to additive effects, being similar across diatom availabilities. The drivers of the non-additive re-assemble, but community assembly may be directly or indirectly influenced by the effects of consumption, however, did change with diatom availability. Complementary effects

Summary 175

176 Summary related to niche-partitioning were the main drivers of the non-additive effects of macroinvertebrates colonised deposited wrack. Biological interactions related to resource consumption, with a slightly increasing contribution of selection effects related to competition availability, therefore, cannot be ignored when aiming to understand macroinvertebrate with decreasing diatom availability. Hence, in macroinvertebrate communities with community assembly on sandy beaches. Both season and supratidal macroinvertebrate functionally different, and thus complementary, species, non-additive effects of consumption community composition, especially macroinvertebrate abundance, had a strong effect on can arise even when food availability is low. mineralisation of wrack on sandy beaches. Released nutrients from wrack mineralisation are The question addressed in Chapter 4 was whether the supratidal community, in terms of subsequently taken up by plants, where buried wrack supports beach pioneer plant growth. abundance, species richness and diversity, was a driver of N and P mineralisation of wrack. In This emphasises the link between the marine and terrestrial ecosystems, with a central role addition, temporal (seasonal) and spatial (young and old drift lines) effects were included. A for the macroinvertebrate community in sandy beach ecosystem functioning. litter bag experiment was performed on the beach, where litter bags filled with wrack were For the first time, the effect of a sand nourishment of this scale on the intertidal incubated for two weeks. Season was a strong driver of both N and P mineralisation and the macroinvertebrate community has been quantified. Although the Sand Motor mega- supratidal macroinvertebrate community. Drift line did not have a strong effect on N and P nourishment may initially be beneficial for overall intertidal macroinvertebrate community mineralisation and the supratidal macroinvertebrate community, except for richness and diversity, macroinvertebrate abundance was lower. It is therefore evident that a macroinvertebrate diversity which was higher in young than old drift lines. N and P mega-nourishment can have both positive and negative effects on the intertidal mineralisation was mainly predicted by season and macroinvertebrate abundance, while macroinvertebrate community. It appears that the net effect of the Sand Motor mega- macroinvertebrate richness and diversity were also, albeit less strong, predictors of P nourishment leans towards a positive effect, but it is important to note that this depends on mineralisation. Season and the macroinvertebrate community thus have strong effects on the specific coastal management goals of the mega-nourishment. Thus, in terms of the wrack mineralisation, resulting in a positive effect on nutrient cycling on sandy beaches, intertidal macroinvertebrate community, a mega-nourishment appears to be a promising thereby linking terrestrial and marine ecosystems. coastal defence strategy compared to regular beach nourishment, at least during the first years after construction. For both the supratidal macroinvertebrate community and sandy In Chapter 5 the effects of wrack burial and supratidal macroinvertebrate presence on beach ecosystem functioning, it is crucial that wrack is maintained on both nourished and decomposition driven nutrient availability and beach pioneer plant growth were assessed. A unnourished sandy beaches. Overall, this thesis highlights the need to include the effect of mesocosm experiment was performed, where wrack was either buried or placed on the sand’s resource availability on both the intertidal and supratidal macroinvertebrate community and surface and supratidal amphipods were either present or absent, with two beach pioneer the sandy beach ecosystem as a whole, especially when designing and planning future coastal plant species as phytometers. Buried wrack had a strong positive effect on plant mass and management practices. both N and P content of the annual plant Cakile maritima compared to surface wrack, while effects for the perennial grass Elytrigia juncea were largely absent. For C. maritima, an effect of macroinvertebrate presence on the N content of the total plant was observed, with a higher N content in the absence of macroinvertebrates. For buried wrack, P content was higher for both the total plant and total shoot in the presence of macroinvertebrates. Differences in N and P content of plants due to macroinvertebrate presence did however not result in differences in plant dry mass. Together, this suggests that macroinvertebrates enhance decomposition of wrack, but that released inorganic N is either taken up by the microbial community or forming complexes with phenolic compounds, resulting in immobilisation of N for plants. Excess P on the other hand was incorporated in C. maritima, which might have been P limited. We conclude that the burial of wrack is of paramount importance for C. maritima growth in support of embryo dune formation and possibly further ecological development of the sandy beach and dune ecosystems.

To conclude, this thesis showed a clear effect of resource availability on macroinvertebrate species interactions and subsequent consumption in the intertidal zone of sandy beaches, which may indirectly affect community composition. Resource availability had a direct effect on macroinvertebrate community composition in the supratidal zone as supratidal

Summary 177 related to niche-partitioning were the main drivers of the non-additive effects of macroinvertebrates colonised deposited wrack. Biological interactions related to resource consumption, with a slightly increasing contribution of selection effects related to competition availability, therefore, cannot be ignored when aiming to understand macroinvertebrate with decreasing diatom availability. Hence, in macroinvertebrate communities with community assembly on sandy beaches. Both season and supratidal macroinvertebrate functionally different, and thus complementary, species, non-additive effects of consumption community composition, especially macroinvertebrate abundance, had a strong effect on can arise even when food availability is low. mineralisation of wrack on sandy beaches. Released nutrients from wrack mineralisation are The question addressed in Chapter 4 was whether the supratidal community, in terms of subsequently taken up by plants, where buried wrack supports beach pioneer plant growth. abundance, species richness and diversity, was a driver of N and P mineralisation of wrack. In This emphasises the link between the marine and terrestrial ecosystems, with a central role addition, temporal (seasonal) and spatial (young and old drift lines) effects were included. A for the macroinvertebrate community in sandy beach ecosystem functioning. litter bag experiment was performed on the beach, where litter bags filled with wrack were For the first time, the effect of a sand nourishment of this scale on the intertidal incubated for two weeks. Season was a strong driver of both N and P mineralisation and the macroinvertebrate community has been quantified. Although the Sand Motor mega- supratidal macroinvertebrate community. Drift line did not have a strong effect on N and P nourishment may initially be beneficial for overall intertidal macroinvertebrate community mineralisation and the supratidal macroinvertebrate community, except for richness and diversity, macroinvertebrate abundance was lower. It is therefore evident that a macroinvertebrate diversity which was higher in young than old drift lines. N and P mega-nourishment can have both positive and negative effects on the intertidal mineralisation was mainly predicted by season and macroinvertebrate abundance, while macroinvertebrate community. It appears that the net effect of the Sand Motor mega- macroinvertebrate richness and diversity were also, albeit less strong, predictors of P nourishment leans towards a positive effect, but it is important to note that this depends on mineralisation. Season and the macroinvertebrate community thus have strong effects on the specific coastal management goals of the mega-nourishment. Thus, in terms of the wrack mineralisation, resulting in a positive effect on nutrient cycling on sandy beaches, intertidal macroinvertebrate community, a mega-nourishment appears to be a promising thereby linking terrestrial and marine ecosystems. coastal defence strategy compared to regular beach nourishment, at least during the first years after construction. For both the supratidal macroinvertebrate community and sandy In Chapter 5 the effects of wrack burial and supratidal macroinvertebrate presence on beach ecosystem functioning, it is crucial that wrack is maintained on both nourished and decomposition driven nutrient availability and beach pioneer plant growth were assessed. A unnourished sandy beaches. Overall, this thesis highlights the need to include the effect of mesocosm experiment was performed, where wrack was either buried or placed on the sand’s resource availability on both the intertidal and supratidal macroinvertebrate community and surface and supratidal amphipods were either present or absent, with two beach pioneer the sandy beach ecosystem as a whole, especially when designing and planning future coastal plant species as phytometers. Buried wrack had a strong positive effect on plant mass and management practices. both N and P content of the annual plant Cakile maritima compared to surface wrack, while effects for the perennial grass Elytrigia juncea were largely absent. For C. maritima, an effect of macroinvertebrate presence on the N content of the total plant was observed, with a higher N content in the absence of macroinvertebrates. For buried wrack, P content was higher for both the total plant and total shoot in the presence of macroinvertebrates. Differences in N and P content of plants due to macroinvertebrate presence did however not result in differences in plant dry mass. Together, this suggests that macroinvertebrates enhance decomposition of wrack, but that released inorganic N is either taken up by the microbial community or forming complexes with phenolic compounds, resulting in immobilisation of N for plants. Excess P on the other hand was incorporated in C. maritima, which might have been P limited. We conclude that the burial of wrack is of paramount importance for C. maritima growth in support of embryo dune formation and possibly further ecological development of the sandy beach and dune ecosystems.

Samenvatting

180 Samenvatting

Zandstranden behoren tot de meest veelvoorkomende kustecosystemen ter wereld, welke verstoringen van het zandstrandecosysteem verlaagt ten opzichte van reguliere unieke ecologische gemeenschappen herbergen en vele ecosysteemfuncties vervullen, zandsuppletie. Aangezien de macro-evertebratengemeenschap een belangrijke component is waaronder het breken van golven en nutriënten recycling. Vanwege de hoge dynamiek op van het zandstrandecosysteem, is het cruciaal om te begrijpen welke factoren de zandstranden is de in situ primaire productie laag en is de beschikbaarheid van marien samenstelling van macro-evertebratengemeenschappen beïnvloeden op zandstranden en in exogeen organisch materiaal, in de vorm van fytoplankton (intergetijde zone) en aangespoeld het bijzonder na zandsuppleties. Na het plaatsen van een mega-zandsuppletie moeten de zeewier (supragetijde zone), zeer heterogeen in tijd en ruimte. Het voedselweb van het macro-evertebratengemeenschappen opnieuw worden samengesteld, maar dit proces kan zandstrand is daardoor in grote mate afhankelijk van de aanvoer van marien exogeen organish direct en indirect worden beïnvloed door de eigenschappen van de mega-zandsuppletie. Zo materiaal en is daarmee voornamelijk ‘bottom-up controlled’. In het bijzonder vormen de kan een verandering in de plaatselijke hydrodynamica rondom de mega-zandsuppletie macro-evertebraten gemeenschappen van het intergetijde en supragetijde gebied samen de bijvoorbeeld een verandering in de verspreiding van macro-evertebraten of de connectie tussen mariene primaire productie en hogere trofische niveau’s, via beschikbaarheid van voedsel teweeg brengen. Dit zou vervolgens een effect kunnen hebben microalgenconsumptie, afbraak van aangespoeld zeewier en als voedsel voor predatoren, op soortsinteracties en het samenstellen van de gemeenschap, resulterend in de uiteindelijke waarmee ze de mariene en terrestrische voedselwebben met elkaar verbinden. De macro- macro-evertebraten gemeenschapssamenstelling die op het zandstrand is te vinden. Tot evertebraten gemeenschap bestaat voornamelijk uit borstelwormen, vlokreeften, isopoden dusver was nog niet onderzocht wat het effect is van een mega-zandsuppletie op de macro- en insecten, die zich een paar centimeter diep in het zand bevinden of zich schuil houden in evertebratengemeenschap en hoe zich dat verhoudt tot reguliere zansuppleties. en nabij pakketten aangespoeld zeewier. Op zandstranden is een relatief duidelijke scheiding De voornaamste doelen van dit proefschrift waren om 1) het effect van tussen de intergetijde en de supragetijde zone waarneembaar. Onder invloed van de getijden voedselbeschikbaarheid op de macro-evertebraten gemeenschapssamenstelling en als gevolg van de maanstand, valt het zand in de intergetijde zone tweemaal per dag droog ecosystemfuncties van zandstranden beter te begrijpen, en 2) het effect van een mega- (laagwater) en raakt het tweemaal per dag verzadigd door zeewater (hoogwater). Macro- zandsuppletie op de macro-evertebratengemeenschap van het zandstrand te onderzoeken. evertebraten soorten die in de intergetijde zone leven zijn goed aangepast aan deze Hiervoor heb ik zowel laboratorium experimenten als veldwerk op de Nederlandse dynamische omgeving. Zo filtreren de meeste soorten zwevende organische deeltjes uit de zandstranden uitgevoerd, gericht op zowel het intergetijde als supragetijde gebied om het waterkolom of vangen organische deeltjes die op de bodem zijn gaan liggen. In tegenstelling gehele zandstrand mee te nemen. tot de intergetijde zone staat de supragetijde zone zelden onder water als gevolg van de getijdencyclus, aangezien deze zone zich tussen de hoogwaterlijn en de voet van de duinen In Hoofdstuk 2 werd het ruimtelijke en temporele effect van een mega-zandsuppletie op de bevindt, waardoor het zand voor langere perioden achtereen droog blijft. Voor macro- macro-evertebratengemeenschap van het intergetijde gebied onderzocht, waarbij ook een evertebraten in het supragetijde gebied is aangespoeld zeewier een belangrijke bron van vergelijking werd gemaakt met de macro-evertebratengemeenschap op zandstranden voedsel en habitat (bijv. bescherming tegen uitdroging en predatie door vogels). Het is echter onderheving aan reguliere suppletie of welke niet werden gesuppleerd. Hiervoor hebben we nog onduidelijk wat het effect is van voedselbeschikbaarheid op soortsinteracties en drie datasets met veldgegevens over macro-evertebraten aan de Nederlandse kust verzameld, gemeenschapssamenstelling van de macro-evertebraten gemeenschap op zandstranden, en gecombineerd en geanalyseerd: één dataset bevatte data van de Zandmotor mega- hoe dit uiteindelijk ecosysteem functioneren beïnvloedt. zandsuppletie, de andere twee datasets bevatten data van zowel zandstranden onderhevig aan reguliere suppletie of niet gesuppleerde zandstranden. Binnen de Zandmotor mega- Ondanks de hoge ecologische waarde van zandstrandecosystemen, worden deze over de hele zandsuppletie waren er sterke ruimtelijke verschillen, met een specifieke macro- wereld bedreigd. Zandstranden worden verdrukt tussen de stijgende zeespiegel en een evertebratengemeenschap, bestaande uit soorten die gewoonlijk op wadplaten worden toename in stormen als gevolg van klimaatverandering aan de ene kant, en statische, gevonden, in de lagune ten opzichte van delen van de Zandmotor mega-zandsuppletie menselijke bouwwerken aan de andere kant. Op wereldschaal is de kustzone, zandstranden onderhevig aan sterke hydrodymica. De Zandmotor mega-zandsuppletie resulteert plaatselijk inbegrepen,, gewoonlijk dichtbevolkt en de menselijke bevolking zal naar verwachting in de in een habitat dat een andere macro-evertebratengemeenschap in de intergetijde zone toekomst alleen maar stijgen in deze gebieden. Deze combinatie van factoren heeft als gevolg aantrekt. De delen van de Zandmotor mega-zandsuppletie onderhevig aan sterke dat erosie van het zandstrand optreed, waarbij de menselijke bevolking wordt bedreigd door hydrodynamica hadden een lagere soortenrijkdom, lagere abundantie en de macro- de zee die verder landinwaarts beweegt en maar een smalle zandreep overblijft voor evertebratengemeenschap convergeerde niet in een gelijke samenstelling als aangetroffen op ecologische gemeenschappen. Om de effecten van erosie tegen te gaan wordt doorgaans zandstranden onderhevig aan reguliere suppletie of niet gesuppleerde zandstranden. Een zandsuppletie toegepast, maar recentelijk is een mega-zandsuppletie (het Zandmotor pilot mega-zandsuppletie kan dus resulteren in een andere macro-evertebratengemeenschap in project) voorgesteld als een meer ecologisch en duurzaam alternatief voor reguliere het intergetijde gebied, wat mogelijk ook effecten heeft op hogere trofische niveau’s binnen zandsuppleties. Een mega-zandsuppletie wordt gemaakt door het plaatsen van een groot het zandstrandecosysteem. volume aan zand op een klein deel van het zandstrand, waarna dit zand geleidelijk, over een langere periode, de stranden die stroomopwaarts liggen suppleert. Daarmee wordt het aantal

Samenvatting 181

182 Samenvatting

Hoofdstuk 3 richtte zich op het effect van algenbeschikbaarheid op de non-additieve effecten bovengrondse delen wanneer aangespoeld zeewier was begraven macro-evertebraten van consumptie door een simpele macro-evertebratengemeenschap bestaande uit drie aanwezig waren. Verschillen in de hoeveelheid N en P als gevolg van de aanwezigheid van soorten uit de intergetijde zone. Een mesocosm studie werd uitgevoerd waarbij we de macro-evertebraten hadden echter geen effect op het drooggewicht van de planten. Samen algenconsumptie door drie macro-evertebraten soorten (Bathyporeia pilosa, Haustorius suggereert dit dat macro-evertebraten een positief effect hebben op de decompositie van arenarius en Scolelepis squamata) hebben gekwantificeerd door middel van het labellen van aangespoeld zeewier, maar dat vrijgekomen inorganische N wordt opgnomen door de algen met stabiele isotopen. Macro-evertebraten werden gehouden in monocultuur of een microbiële gemeenschap of complexen vormt met fenolen, waardoor immobilisatie van N simpele gemeenschap bij verschillende hoeveelheden algen. De vlokreeft B. pilosa was de optreedt. Vrijgekomen P leek echter te worden opgenomen door C. maritima, die mogelijk P meest succesvolle concurrent in termen van consumptie zowel bij hoge als lage gelimiteerd was. De conclusie is dat het begraven van aangespoeld zeewier van groot belang algenbeschikbaarheid, terwijl de vlokreeft H. arenarius en de borstelworm S. squamata is voor de groei van C. maritima en daarmee mogelijk de vorming van embryoduinen en minder consumeerden in de gemeenschap dan in hun respectievelijke monoculturen. Non- verdere ecologische ontwikkeling van het zandstrand en het duinecosysteem stimuleert. additieve effecten van consumptie waren groter dan alleen de additieve effecten en bleven In dit proefschrift werd een duidelijk effect gevonden van voedselbeschikbaarheid op de gelijk onder verschillende algenbeschikbaarheden. De soortsinteracties onderliggend aan de interacties tussen macro-evertebraten soorten en hun consumptie van het intergetijde non-additieve effecten van consumptie veranderden echter wel. Complementaire effecten gebied, wat een indirect effect kan hebben op de gemeenschapssamenstelling. gerelateerd aan niche-segregratie waren voornamelijk de sturende factor van de non- Voedselbeschikbaarheid had een direct effect op de macro-evertebratengemeenschap van de additieve effecten van consumptie, waarbij het effect van selectie effecten gerelateerd aan supragetijde zone, aangezien deze macro-evertbraten aangespoeld zeewier snel competitie toenam bij een lagere algenbeschikbaarheid. In macro- koloniseerden. Biologische interacties kunnen daarmee niet worden genegeerd wanneer men evertebratengemeenschappen bestaande uit functioneel verschillende, en dus als doel heeft om de factoren die de samenstelling van macro-evertebratengemeenschappen complementaire, soorten, kunnen non-additieve effecten van consumptie ontstaan zelfs op zandstranden beïnvloeden, te onderzoeken. Zowel seizoen als de samenstelling van de wanneer voedselbeschikbaarheid laag is. macro-evertebratengemeenschap van het supragetijde gebied, met name abundantie, De vraag die in Hoofdstuk 4 werd behandeld was of de macro-evertebratengemeenschap van hadden een sterk effect op de mineralisatie van aangespoeld zeewier op zandstranden. Het het supragetijde gebied, in termen van abundantie, soortenrijkdom en diversiteit, een effect overstuiven van aangespoeld zeewier had een positief effect op de groei van planten op het had op N en P mineralisatie van aangespoeld zeewier. Daarnaast is er gekeken naar het effect strand. Dit benadrukt de verbinding tussen mariene en terrestrische ecosystemen, met een van seizoen en vloedmerklijn (jong en oud) op dit mineralisatie proces. Hiervoor werd een centrale rol voor de macro-evertebratengemeenschap in het ecosysteem functioneren van veldexperiment uitgevoerd waarbij zakjes gemaakt van gaas werden gevuld met zeewier en zandstranden. twee weken op het strand werden geïncubeerd. Seizoen had een sterk positief effect op zowel Voor het eerst is het effect van een zandsuppletie van deze schaal op de macro- N als P mineralisatie en de macro-evertebratengemeenschap van het supragetijde gebied. evertebratengemeenschap van het intergetijde gebied gekwantificeerd. Hoewel de Vloedmerklijn had geen effect op N en P mineralisatie of de macro-evertebratengemeenschap Zandmotor mega-zandsuppletie in eerste instantie bevorderlijk lijkt voor de soortenrijkdam van het supragetijde gebied, behalve voor diversiteit welke hoger was in jonge dan in oude en diversiteit van macro-evertebraten, was de abundantie van macro-evertebraten lager. Het vloedmerklijnen. N en P mineralisatie werd voornamelijk beïnvloed door seizoen en macro- is daarom duidelijk dat een mega-suppletie zowel positieve als negatieve effecten op de evertebraten abundantie, terwijl P mineralisatie daarnaast ook werd beïnvloed, alhoewel in macro-evertebratengemeenschap van het intergetijdegebied kan hebben. Alles bij elkaar mindere mate, door macro-evertebraten soortenrijkdom en diversiteit. Seizoen en de macro- genomen lijkt het effect van de Zandmotor mega-zandsuppletie te gaan richting een licht evertebratengemeenschap hebben dus een sterk positief effect op de mineralisatie van overwegend positief effect, maar het is belangrijk om op te merken dat dit van de specifieke aangespoeld zeewier en daarmee een op de nutriënten recycling van zandstranden. Daarmee beheersdoelen van de mega-zandsuppletie afhangt. Dit leidt tot de conclusie dat, in termen dragen macro-evertebraten bij aan het verbinden van mariene en terrestrische ecosystemen. van de macro-evertebratengemeenschap van het intergetijde gebied, een mega- In Hoofdstuk 5 werd het effect van het begraven van aangespoeld zeewier en de aanwezigheid zandsuppletie een veelbelovend strategie voor kustverdediging lijkt te zijn vergeleken met van macro-evertebraten op nutriëntenbeschikbaarheid, als gevolg van decompositie, en reguliere zandsuppleties, in ieder geval gedurende de eerste paar jaar na voltooing. Voor plantengroei van pioneerssoorten onderzocht. In een mesocosm experiment werd zowel de macro-evertebratengemeenschap van het supragetijde gebied als het ecosysteem aangespoeld zeewier begraven of op het zandoppervlak geplaatst en de vlokreeft Talitrus functioneren van zandstranden is het van belang dat aangespoeld zeewier blijft liggen op saltator uit het supragetijde gebied was danwel aan- of afwezig. Begraven van aangespoeld zowel gesuppleerde als niet gesuppleerde zandstranden. In het algemeen benadrukt dit zeewier had een sterk positief effect op het drooggewicht en de hoeveelheid N en P van het proefschrift de noodzaak om het effect van voedselbeschikbaarheid op de macro- eenjarige kruid Cakile maritima, maar nauwelijks op het meerjarige gras Elytrigia juncea. Voor evertebratengemeenschap van zowel het intergetijde als het supragetijde gebied, en het C. maritima werd een hogere hoeveelheid N gevonden in planten in de afwezigheid van zandstrandecosysteem als geheel, mee te nemen, met name in het ontwerp en plannen van macro-evertebraten. De hoeveelheid P was hoger voor zowel de gehele plant als de toekomstige strategiën voor kustverdediging.

Samenvatting 183

Acknowledgements

186 Acknowledgements

It is absolutely true that, although this PhD thesis carries my name, numerous people have much enjoyed the department day outs and dinners which made me feel connected, even given me endless help, guidance and enjoyment to be able to complete this work. I am grateful though we work on different research topics. for every person that (in)directly contributed to this thesis and ideally, I would mention each I am happy to have been a part of NatureCoast, the research program that united PhD and every one of them! As this is not feasible due to limited space, I will highlight some of the students (Jantien, Max, Corjan, Lianne, Isaac, Simeon, Marjolein, Marinka, Sebastiaan, Iris, people who had the greatest impact. Ewert and Lotte) and post docs (Arjen, Vera, Ewert, Timothy and Alexander) from diverse Rien, as my promotor you have been more than essential to the completion of this thesis. I disciplines all focused on the Sand Motor. I found it very interesting to listen to your views and would like to thank you for your trust and patience when guiding me through this PhD from have cross-disciplinary discussions about the effects of the Sand Motor on many different start to finish. Your birds’ eye view kept things for me in perspective when they seemed too aspects. In particular, I will always remember the time that we went surfing and stand-up complicated or overwhelming. When this happened, you taught me to always go back to the paddling in wet suits (in the rain) at the Sand Motor! Thank you for your inspiration and ‘why’ and focus on the core of the subject matter. I always felt you were interested and companionship. involved in what was going on, both in the project and on a personal level, and I would like to My friends regularly gave me the much-needed relaxation to be able to continue with my thank you for your good care as a supervisor. thesis with a refreshed mind. Samantha, Rosa, Rozemarijn, Janneke, Jeltje and Janna, thank Peter, I deeply appreciate all the times that you made time, sometimes on a whim, to help me you for being there and creating wonderful memories together! Rozemarijn, Janneke and with my calculations and statistical analyses. On these occasions, I hardly had to explain what Jeltje, a special thank you for helping me in the field. I will never forget that one time when I was working on: you immediately understood what the problem was and gave several Jeltje and I got stuck with the four-wheel drive on the beach late at night, but we managed to options to deal with it. This has sped up the work process immensely and added more depth get ourselves out of the sand! Janna and Jeltje, I found it valuable to share both the positive to my research. Thank you for your patience when I asked yet another question and guiding and negative aspects of our PhDs with each other, which provided me with a lot of perspective. me when setting my first steps in R. This helped me to organize my thoughts, making me a Janna, it was great to stay with you in a cottage for several times where we could write on our better researcher than when I started this PhD. theses and had both fun and interesting discussions, which were fueled on tea and chocolate. Matty, I would like to thank you for your open attitude and the welcoming atmosphere you There would definitely not have been a thesis if my husband Björn would not have been create. Your positive spirit kept me going when something did not go as planned and needed around to support me every step of the way, from the moment I accepted this position to the last-minute decision-making. You took the time to explain ecological concepts to me in detail moment that I wrote the final word of this thesis. Thank you for your infinite amount of love, and helped me tremendously with the identification of the macroinvertebrates. You even patience and confidence in me. I am also grateful for your practical help in the lab and field inspired me to think like a macroinvertebrate to understand how it would respond to certain and I will never again send you to the beach with a broken bike trailer, I promise! Finally, my changes in its environment, which improved my ecological thinking. daughter Maja has brought countless smiles on my face when I felt discouraged and I am very happy she entered my life. I started my PhD without her, but finished it with her by my side. Jurgen, Richard and Rob, you have been invaluable with regard to the practical and technical aspects of my research. Jurgen, I cannot thank you enough for all the times you joined me to do field work on the beach, both in the heat of summer and in pouring autumn rains. I very much enjoyed working together and talking about food, art and family life. I greatly appreciate your advice when I did not know what to do about a practical issue, giving me the space to figure something out. Richard, thank you for thinking along with me and providing solid advice on how to do certain analyses or measurements. I am grateful for all the measurements you have performed and your patience with me when I arrived with even more samples. Rob, thank you for stepping in to help me with the harvest of my final experiment and grinding, weighing and chemically analyzing a large part of my samples. I have been very fortunate to work among so many kind and interested colleagues at the Systems Ecology department: Hans, James, Jelte, Sebastiaan, Stef, Josh, Saori, Guillaume, Michelle, Luke, Juan, Becca, Milou, Chang, Ding, Stefanie, Qiaoli, Wei-Wei, Bin, Spring, Nadia, Bas, Andries, Yasmijn, Sunu, Lieneke, Diana, Eva (and many others!). I found it interesting to listen to you explaining your research and see how passionate everyone is about their work. Thank you for helping me with R-issues/practical work/taking a break once in a while! I very

Acknowledgements 187

About the author

Emily van Egmond was born on 7 September 1988 in Amsterdam, the Netherlands. In 2006 she received here VWO diploma and started with the BSc Biology at Wageningen University. Her BSc thesis focused on the importance of arbuscular mycorrhizal fungi (AMF) for competitive interactions and community structure in plant communities. She graduated in 2010 and started directly with the MSc Biology, also at Wageningen University, with a specialisation in ecology. She completed two MSc theses and an internship. Her first MSc thesis was about relating plant functional traits to successful pine tree establishment in peatlands, which was later published. Her second MSc thesis was performed in Sweden at Uppsala University on the influence of grazing pressure by large herbivores on the population biology of the perennial herb Primula farinosa. At Artis Amsterdam Royal Zoo she performed an internship where she was responsible for writing and producing new species information signs (mainly birds and mammals). In 2012 she received her MSc diploma. For two months she continued to work at Artis, followed by a six-month period at Naturalis Biodiversity Centre digitising herbarium plant material. In 2013 she started with her PhD research at the Systems Ecology department of the Vrije Universiteit Amsterdam, which resulted in this PhD thesis on sandy beach ecology. Currently, she works on the ICEDIG project at Naturalis Biodiversity Centre to help make natural history collections available through digitisation for biodiversity research on a European scale.

About the author 191

Publications

Peer-reviewed publications Pit, I.R., van Egmond, E.M., Wassen, M.J., van Wezel, A.P., Griffioen, J. and Dekker, S.C. (in press) Ecotoxicological risk of trace element mobility in coastal semi-artificial depositional areas near the mouth of the River Rhine, the Netherlands. Environmental Toxicology and Chemistry.

van Egmond, E.M., van Bodegom, P.M., Berg, M.P., Wijsman, J.W.M., Leewis, L., Janssen, G.M. and Aerts, R. 2018. A mega sand nourishment creates novel habitat for intertidal macroinvertebrates by enhancing habitat relief of the sandy beach. Estuarine, Coastal and Shelf Science, 207: 232-241, doi: 10.1016/j.ecss.2018.03.003.

van Egmond, E.M., van Bodegom, P.M., van Hal, J.R., van Logtestijn, R.S.P., Berg, M.P. and Aerts, R. 2018. Non-additive effects of consumption in an intertidal macroinvertebrate community are independent of food availability but driven by complementarity effects. Ecology and Evolution, 00:283-290, doi: 10.1002/ece3.3841.

Limpens, J., van Egmond, E., Li, B. and Holmgren, M. 2014. Do plant traits explain tree seedling survival in bogs? Functional Ecology, 28:283-290, doi: 10.1111/1365-2435.12148.

Other publications

van Egmond, E.M. Paragraph 5.3 (‘Washed ashore’) in Sand Motor book on the ecology of the intertidal and supratidal macroinvertebrate community (in production).

Publications 195

Limpens, J., van Egmond, E., Li, B. and Holmgren, M. 2014. Do plant traits explain tree seedling survival in bogs? Functional Ecology, 28:283-290, doi: 10.1111/1365-2435.12148.

Other publications

van Egmond, E.M. Paragraph 5.3 (‘Washed ashore’) in Sand Motor book on the ecology of the intertidal and supratidal macroinvertebrate community (in production).

LIVING ON THE EDGE LIVING ON THE EDGE INVITATION Resource availability and macroinvertebrate community dynamics To attend the public defence of my in relation to sand nourishment PhD thesis entitled: LIVING ON THE EDGE

Resource availability Emily van Egmond and macroinvertebrate community dynamics in relation to sand nourishment

By Emily van Egmond

Thursday 13th of December 2018 at 11.45 hours

In the Aula of the Vrije Universiteit Amsterdam You are kidnly invited to join the reception following the defence.

Emily van Egmond [email protected]

Emily van Egmond Paranymphs

Milou Huizinga Björn van Loon [email protected]