CONCEPTS & SYNTHESIS EMPHASIZING NEW IDEAS TO STIMULATE RESEARCH IN ECOLOGY

Ecological Monographs, 85(3), 2015, pp. 333–351 Ó 2015 by the Ecological Society of America

Tube-dwelling invertebrates: tiny ecosystem engineers have large effects in lake ecosystems

1,10 2 3 4 1 5 FRANZ HO¨ LKER, MICHAEL J. VANNI, JAN J. KUIPER, CHRISTOF MEILE, HANS-PETER GROSSART, PETER STIEF, 1 6 7 8 1 3,9 RITA ADRIAN, ANDREAS LORKE, OLAF DELLWIG, ANDREAS BRAND, MICHAEL HUPFER, WOLF M. MOOIJ, 1 1 GUNNAR NU¨ TZMANN, AND JO¨ RG LEWANDOWSKI 1Leibniz Institute of Freshwater Ecology and Inland Fisheries, 12587 Berlin, Germany 2Department of Biology, Miami University, Oxford, Ohio 45056 USA 3Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB Wageningen, The Netherlands 4Department of Marine Sciences, University of Georgia, Athens, Georgia 30602 USA 5Department of Biology, University of Southern Denmark, 5230 Odense, Denmark 6Institute for Environmental Sciences, University of Koblenz-Landau, 76829 Landau, Germany 7Leibniz Institute for Baltic Sea Research, 18119 Rostock, Germany 8Department of Surface Waters–Research and Management, Swiss Federal Institute of Aquatic Science and Technology (Eawag), 6047 Kastanienbaum, Switzerland 9Department of Environmental Sciences, Wageningen University, 6708 PB Wageningen, The Netherlands

Abstract. There is ample evidence that tube-dwelling invertebrates such as chironomids significantly alter multiple important ecosystem functions, particularly in shallow lakes. Chironomids pump large water volumes, and associated suspended and dissolved substances, through the sediment and thereby compete with pelagic filter feeders for particulate organic matter. This can exert a high grazing pressure on phytoplankton, microorganisms, and perhaps small zooplankton and thus strengthen benthic-pelagic coupling. Furthermore, intermittent pumping by tube-dwelling invertebrates oxygenates sediments and creates a dynamic, three-dimensional mosaic of redox conditions. This shapes microbial community composition and spatial distribution, and alters microbe-mediated biogeochemical functions, which often depend on redox potential. As a result, extended hotspots of element cycling occur at the oxic-anoxic interfaces, controlling the fate of organic matter and nutrients as well as fluxes of nutrients between sediments and water. Surprisingly, the mechanisms and magnitude of interactions mediated by these organisms are still poorly understood. To provide a synthesis of the importance of tube-dwelling invertebrates, we review existing research and integrate previously disregarded functional traits into an ecosystem model. Based on existing research and our models, we conclude that tube-dwelling invertebrates play a central role in controlling water column nutrient pools, and hence water quality and trophic state. Furthermore, these tiny ecosystem engineers can influence the thresholds that determine shifts between alternate clear and turbid states of shallow lakes. The large effects stand in contrast to the conventional limnological paradigm emphasizing predominantly pelagic food webs. Given the vast number of shallow lakes worldwide, benthic invertebrates are likely to be relevant drivers of biogeochemical processes at regional and global scales, thereby mediating feedback mechanisms linked to climate change. Key words: biogeochemistry; chironomids; ecosystem modelling; filter-feeding; food web; nutrient cycling; tube-dwelling macrozoobenthos.

INTRODUCTION Shallow lakes represent the most abundant lake type worldwide. These ecosystems are highly susceptible to Manuscript received 19 June 2014; revised 1 December 2014; global warming and eutrophication, and are of great accepted 28 January 2015; final version received 5 March 2015. Corresponding Editor: K. L. Cottingham. importance for regional and global element cycles 10 E-mail: [email protected] (Wetzel 2001, Downing et al. 2006, Adrian et al. 333 334 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

TABLE 1. Definition of terms based on Jones et al. (1994) and Kristensen et al. (2012).

Term Definition Ecosystem engineer ‘‘... organisms that directly or indirectly modulate the availability of resources (other than themselves) to other species, by causing physical state changes in biotic or abiotic materials. In so doing they modify, maintain and/or create habitats.’’ (Jones et al. 1994:374) Bioturbation ‘‘All transport processes carried out by animals that directly or indirectly affect sediment matrices. These processes include particle reworking and burrow ventilation’’ (Kristensen et al. 2012:288) Burrow ventilation ‘‘Rapid exchange of water between the overlying water and subsurface sediment’’ (Kristensen et al. 2012:293) since ‘‘animals flush their open- or blind-ended burrows with overlying water for respiratory and feeding purposes’’ (p. 285) Particle reworking ‘‘Faunal displacement and biomixing of particles’’ including ‘‘burrowing, construction and maintenance of galleries as well as ingestion and defecation of particles‘‘ (Kristensen et al. 2012:288) Bioirrigation Radial molecular diffusion driven or pressure-induced advective pore water ‘‘... exchange of solutes between the sediment pore water and the overlying water body.’’ (Kristensen et al. 2012:285) Excretion The process by which metabolic waste products and other non-useful materials are eliminated from an organism. Note: Kristensen et al. (2012) depict the outcome of a broad discussion within the scientific community, especially the Nereis Park research group.

2009). For example, global annual carbon dioxide lent to an entire shallow lake can be pumped through the emissions from inland waters (mainly from shallow sediment on timescales of days to weeks (Roskosch et al. lakes) to the atmosphere are similar to carbon dioxide 2012). This is particularly true for the most widely uptake by the oceans, and the global burial of organic distributed and frequently the most abundant group of carbon in inland water sediments exceeds that in ocean insects in freshwater environments: the family Chirono- sediments (Tranvik et al. 2009). Small lakes are also midae, dipterans in the suborder Nematocera. Most disproportionately important in retaining and process- chironomid larvae build tubes composed of silk and ing nitrogen (Harrison et al. 2009). Additionally, various substrate materials, such as detritus, algae, and shallow lakes provide a valuable resource for human sediments (Pinder 1986, Armitage et al. 1995). In

YNTHESIS use and recreation (Vo¨ lker and Kistemann 2013). It is shallow lakes, chironomids typically occur at densities therefore important to understand the functioning of between 70 and 11 000 individuals/m2 (Armitage et al. these ecosystems, in particular the controls on their 1995, Mousavi 2002). The sheer number of individuals &S metabolism, nutrient cycling, and productivity. suggests that tube-dwelling invertebrates are relevant for A potentially important driver of lake ecosystem carbon, nutrient, and energy cycling at the ecosystem metabolism, benthic invertebrates, has traditionally level, potentially modulating a feedback with global been disregarded or viewed in a supportive food web cycles and climate.

ONCEPTS context, i.e., as a food source for fish and to a lesser To rigorously assess the ecosystem-level role of tube-

C extent as consumers of sedimentary algae and organic dwelling invertebrates, their roles in benthic-pelagic matter (Janse et al. 2010, Vander Zanden and Gratton coupling and inducing changes in alternate states needs 2011). While the interplay between productivity and the to be considered. Classical theory on alternative stable dynamics of shallow lake communities has been states in shallow lakes differentiates macrophyte-domi- documented extensively (Scheffer 1998, Ko¨ hler et al. nated (clear) from phytoplankton-dominated (turbid) 2005, Huber et al. 2008), the role of benthic inverte- lakes, and focuses on feedback effects mediated by the brates in regulating biogeochemical cycles and energy impact of fish on phytoplankton through predation on flux at the whole-lake scale has received little attention herbivorous zooplankton (trophic cascades) and via (Covich et al. 1999, Vadeboncoeur et al. 2002). Given bioturbation by fish (Scheffer 1998). Which state the prevalence of small lakes across the globe, as well as prevails under what conditions can be analyzed using the potentially large role of benthic invertebrates, it is long-term records and ecosystem models, and as with essential that we comprehensively evaluate the role of any model the predictive power depends on the validity these organisms at multiple scales. of the model parameters and assumptions. However, Benthic invertebrates represent a diverse fauna, but existing models of shallow lake ecosystems such as tube-dwelling taxa may be especially important because PCLake (Janse 2005, Mooij et al. 2010) or the PEG they pump large volumes of water, containing suspend- (Plankton Ecology Group) model (Sommer et al. 1986, ed, dissolved, and gaseous substances, through the 2012, de Senerpont Domis et al. 2013) insufficiently sediment. Small-scale laboratory studies investigating include the benthic-pelagic coupling mediated by tube- the pumping activity of tube-dwelling invertebrates dwelling invertebrates and its implications for pelagic (ventilation; see Table 1 for definition of terms) and food web regulation. There is now ample evidence to the subsequent aeration of the sediment (bioirrigation) suggest that the impacts of these animals on the suggest that tube-dwelling invertebrates play a far more dynamics of microorganisms, redox gradients, and important and diverse ecological role than previously biogeochemical cycling of nutrients must be taken into assumed by ecosystem-level analyses. Volumes equiva- account to forecast ecosystem trajectories at the whole- August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 335 C ONCEPTS

FIG. 1. Mechanisms by which tube-dwelling invertebrates may control water quality and trophic status (Chironomus plumosus larvae used as an example for tube-dwelling invertebrates). &S

lake scale (e.g., Stief and Ho¨ lker 2006, Lewandowski et flow rate of 60 mL/h (flow velocity 15 mm/s, tube YNTHESIS al. 2007). diameter 1.5–2.0 mm, tube depth up to 20 cm), The aim of this paper is to review and synthesize individual Chironomus plumosus larvae pump approxi- existing information in order to articulate the role of mately 10 times more water through their burrows than tube-dwelling invertebrates in lake ecosystems and to required to meet their oxygen demands (Roskosch et al. identify knowledge gaps for future research. First we 2010b, 2011). Reasons for such high pumping rates are evaluate current knowledge in four areas: (1) biogeo- high oxygen consumption by the microbial community chemistry at the scale of individual tubes, (2) nutrient of the burrow walls, which reduces oxygen availability cycling mediated by tube-dwelling invertebrates, (3) to the larvae (Polerecky et al. 2006) and high filter- filtration and food competition between pelagic zoo- feeding rates of the larvae, which feed predominantly on plankton and tube-dwelling invertebrates, and (4) particulate matter delivered into the burrow by the impacts of predators on tube-dwelling invertebrates water current (Fig. 1; Roskosch et al. 2010b). and nutrient dynamics. Then we evaluate how the Burrow ventilation transports oxygen more rapidly impacts of tube-dwelling invertebrates are expressed at and deeper into the sediment than does molecular the ecosystem level using two established conceptual diffusion across the sediment–water interface (Meile models and a dynamical ecosystem model. Based on and Van Cappellen 2003). In addition, the intermittent these theoretical approaches, our final goal is to identify nature of burrow ventilation affects the temporal distribution of oxygen and redox conditions in sedi- future research domains to overcome current limitations ments surrounding the burrows (Polerecky et al. 2006, in understanding how tube-dwelling invertebrates affect Roskosch et al. 2011, Volkenborn et al. 2012). This lake ecosystems. temporal oscillation in redox can greatly increase the BIOGEOCHEMISTRY AT THE SCALE OF INDIVIDUAL TUBES metabolic rates of tube-associated sediment bacteria and stimulate organic matter degradation (Aller 1994). Geochemistry Pumping activities of tube dwellers can also increase Oxygen is scarce in the sediment environment, and the release of phosphate-P and ammonium-N previously thus tube-dwelling invertebrates need to pump overlying bound in organic detritus to the overlying water column oxygen-rich water through their U-shaped burrows in (Fig. 1; Stief and Ho¨ lker 2006, Lewandowski et al. 2007, the sediment for respiration. Interestingly, given a water Stief et al. 2010). However, some studies show that 336 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

chironomids enhance phosphorus (P) fluxes across the brates can thus result in a significant net loss of nitrogen sediment–water interface (e.g., Andersson et al. 1988, from shallow aquatic ecosystems (Jeppesen et al. 1998, Andersen and Jensen 1991, Andersen et al. 2006), while Søndergaard et al. 2007), but also in the release of others show the opposite effect (e.g., Lewandowski and nitrous oxide (a greenhouse gas) from the sediment Hupfer 2005, Lewandowski et al. 2007). Lewandowski (Svensson 1998, Stief et al. 2009, Stief 2013). The extent et al. (2007) argue that the apparently contradictory of tube-dweller effects on N cycling depends on the results of chironomids on P flux may illustrate the reactivity of organic matter as a source of ammonium relative importance of opposing pathways and the for nitrification and as a substrate for denitrification, importance of variations in sediment type and compo- oxygen as a substrate for nitrification and as an inhibitor sition. The classical view of the effects of individual of denitrification, and the microbial community carrying chironomid burrows on P dynamics is that the thin, out these processes (see Microbiology). Direct observa- oxidized layer of sediment surrounding the burrow tional data on the biogeochemical conditions, let alone adsorbs P, due to the presence of oxidized compounds process rates, are very limited at the scale of tubes. such as Fe-(oxy)hydroxides. This is analogous to the However, new sensor developments such as planar well-known presence of thin oxidized layers at the optodes for O2 (Glud et al. 1996), CO2 (Zhu and Aller 2þ sediment surface in lakes with oxygenated bottom 2010), H2S (Zhu and Aller 2013), Fe (Zhu and Aller waters, which are underlain by anoxic sediments 2012), or pH (Zhu et al. 2006) hold promise for (Hupfer and Lewandowski 2008), or seen as iron plaque quantifying the extent to which tube dwellers alter the on plant roots (Christensen et al. 1998, Hupfer and biogeochemical conditions in their immediate surround- Dollan 2003). The close relation between sedimentary ings. This information will help establish a mechanistic Fe-(oxy)hydroxides and recycled phosphate (known understanding that will ultimately shed light on benthic since the early work of Einsele [1938]) has been nutrient fluxes at larger spatial scales, and how they intensively investigated in various ecosystems and by relate to sediment properties. experimental approaches (e.g., Buffle et al. 1989, Most experimental studies of biogeochemical dynam- Gunnars et al. 2002). P cycling can also be modulated ics at the tube scale are short term, lasting only a few by secondary redox-dependent geochemical reactions days to several weeks. The long-term effects of tube- (Fig. 1) that may result in ferrous or ferric authigenic P dwelling invertebrates on biogeochemical cycling are not YNTHESIS mineral precipitation, such as vivianite or strengite/ known, and thus caution is required in extrapolating tinticite phases (Lijklema 1980, Hyacinthe and Van short-term experiments to longer periods. For example, &S Cappellen 2004, Walpersdorf et al. 2013, Rothe et al. chironomid-mediated fluxes may be fundamentally 2014). As the production of phosphate is tied to organic different during the initial phase, when they build matter remineralization, organic matter input to sedi- burrows, than over longer periods. Thus, effects on ments is critical in shaping P release. It is also a biogeochemical cycling may depend on the duration of determining factor in the extent to which dissimilatory the experiment or whether the initial phase of burrow ONCEPTS

C iron reduction produces ferrous iron. The fate of that construction is included. We would expect longer reduced iron in turn depends on the availability of O2 experiments to better reflect dynamics at the lake scale, for rapid reoxidation forming amorphous iron oxides, of but long-term effects of chironomids on P fluxes sulfide for the precipitation of FeS, and of manganese between sediments and water have not been document- oxides as an alternate electron acceptor. All of these ed. We need long-term sediment core experiments reactions impact the P cycle (e.g., Giordani et al. 1996, (months or years), with regular addition of organic Yao and Millero 1996, Dellwig et al. 2010) and all are matter and chironomids, to quantify the net impacts of potentially affected by tube-dwelling invertebrates. bioirrigation on whole lake biogeochemistry. The Redox zonation around tubes can not only establish capacity for chironomids to immobilize or remineralize an ‘‘iron curtain’’ affecting benthic P fluxes, but also nutrients after reestablishment of anoxic conditions governs the transformation of other redox-sensitive needs to be investigated as a function of initial elements. For example, oxic halos surrounding tubes chironomid density, geochemical sediment composition likely stimulate nitrification, and the nitrate produced (e.g., iron and organic matter content), system state can serve as an electron acceptor for denitrification in (e.g., clear vs. turbid), as well as in the context of the nearby anoxic zones. Thus, in the presence of tube- chironomid life cycle. For example, after larvae leave dwelling chironomids, denitrification activity is stimu- burrows and emerge as adults, solid Fe (III) compounds lated mainly because nitrate is efficiently pumped into in the oxidized sediment surrounding the abandoned deep, anoxic, sediment layers where it is readily reduced burrows are rapidly reduced to soluble Fe2þ (because of to molecular nitrogen (Pelegri et al. 1994, Svensson a lack of O2 supply), and formerly adsorbed P is released 1998). The ventilation of the tubes thus bypasses the to the water. Thus, P sequestration by chironomids may nitrification layer at the sediment surface where nitrate is be only a temporary phenomenon, at least for individual produced and then slowly diffuses downward into deep, burrows (Katsev et al. 2006). In contrast, data from a anoxic layers (Thamdrup and Dalsgaard 2008). Bio- three-year experiment indicate that P immobilized in turbation activities by abundant tube-dwelling inverte- chironomid burrow walls remains in the sediment for a August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 337 long time (possibly permanently) after larvae emerge higher than in the surrounding sediment, possibly due to (M. Hupfer, S. Jordan, C. Herzog, and J. Lewandowski, the higher oxygen availability inside ventilated tubes. unpublished manuscript). The underlying mechanism for Also the diversity of certain functional guilds of bacteria the phenomenon might be the formation of ferrous Fe-P (e.g., nitrate-reducing bacteria) is enhanced in the minerals (e.g., vivianite) due to locally restricted presence of chironomid larvae, either due to metabolic supersaturation by high Fe2þ and phosphate concentra- induction of facultative anaerobes in the anoxic gut, or by tion near the former walls after reestablishment of provision of additional micro-niches and substrates in the anoxic conditions. Furthermore, the upward transport sediment (Poulsen et al. 2014). of phosphate from deeper layers to the sediment–water It has also been hypothesized that tube-dwelling interface is delayed by slow transport processes (diffu- invertebrates cultivate certain bacterial tube communi- sion) without chironomid activities. ties for food, similar to fungus-farming by ants (Mueller To elucidate temporal variation in the effects of tube- et al. 1998), an effect that goes beyond their impacts via dwelling invertebrates on P cycling, and hence the net filter feeding or deposit feeding. Such ‘‘gardening’’ effects on lake water P concentrations, long-term activity of tube-dwelling invertebrates creates a suitable experiments are needed. These experiments should microenvironment for specific functional guilds of manipulate the abundance of tube-dwelling inverte- bacteria on which the larvae feed. Jones and Grey brates and be combined with smaller-scale studies to (2011) suggest considering chironomid larvae as ‘‘con- ascertain mechanisms and quantify rates. These may stant gardeners,’’ for example cultivating methane- include high-resolution pore-water concentration mea- oxidizing bacteria (MOB) within their tubes. Evidence surements, structural analysis of solid phases (e.g., raster for the gardening of MOB comes from high ratios of electron microscopy coupled to energy dispersive X-ray MOB/methanogen DNA around the larval tubes spectroscopy, X-ray diffraction) to quantify mineral (Gentzel et al. 2012) and 13C-depleted chironomid formation, and measurement of the occurrence and tissues, resulting from acquisition of methane-derived C diagenesis of inorganic and organic P forms using carbon via methane-cycling microbes (Deines et al. ONCEPTS sequential extraction (e.g., Psenner et al. 1984, Rutten- 2007). It has been recently shown for Tinodes waeneri berg 1992) or 31P nuclear magnetic resonance (NMR) caddisflies that larval galleries enhance resource avail- spectroscopy (e.g., Reitzel et al. 2012). ability and thus play a substantial role in larval nutrition, especially at key times of food shortage (Ings Microbiology et al. 2012). Thus, gardening activities could affect &S Metabolic activities, abundance, and community whole-ecosystem functioning by increasing and selecting structure of sediment microbes are strongly influenced the standing crop of algae and other microorganisms as YNTHESIS by steep redox gradients, which can greatly vary in time well as biofilm patchiness and activity within lake and space (Frindte et al. 2013), in particular due to sediments. bioturbation and feeding activities of benthic inverte- The alteration of microbial communities in sediments brates. The intermittent ventilation of chironomid tubes inhabited by tube-dwelling invertebrates has significant causes pronounced fluctuations in the concentrations of consequences for microbial metabolism in sediments and oxygen, nitrate, and dissolved substrates that affect for solute exchange between sediments and overlying microbial metabolism in and around the tube (Fig. 1; water. Tube-dwelling invertebrates commonly stimulate Stief and de Beer 2006, Stief et al. 2010). Chironomid microbial organic matter degradation and mineralization ingestion of particle-associated microbes leads to the through bioturbation and feeding activities. Enhanced digestion and loss of microbial biomass, but may also mineralization rates in and around the tubes of tube- induce anaerobic metabolic pathways in the anoxic gut dwelling invertebrates in concert with pumping activity of larvae (Stief et al. 2009). Both bioturbation and lead to increased fluxes of CO2 and DOC from the feeding activities act simultaneously on planktonic and sediment into the water column (Goedkoop et al. 1997, sediment microbes and thus must be considered jointly. Hansen et al. 1998, Stief 2007, Hunting et al. 2012). Aside Bioturbation and feeding activities of tube-dwelling from the carbon cycle, microbial roles in the phosphorus invertebrates change the general community structure of and nitrogen cycles also are greatly affected by tube- sediment bacteria, as demonstrated with molecular dwelling invertebrates. The aforementioned temporal fingerprinting techniques (Hunting et al. 2012, Zeng et fluctuations of redox conditions inside chironomid tubes al. 2014). In contrast, the total abundance of sediment can stimulate microbially induced polyphosphate storage bacteria remains largely unaffected or increases only (Hupfer et al. 2007). Polyphosphate bacteria have the slightly in the presence of tube-dwelling invertebrates potential to control a significant portion of the P fluxes (Van de Bund et al. 1994, Wieltschnig et al. 2008). between the sediment and the overlying water by redox- Notably, the abundance of certain functional guilds of dependent changes in their physiology (Khoshmanesh et bacteria may be significantly enhanced by the activities of al. 2002, Hupfer et al. 2008, Diaz et al. 2012). Little is chironomid larvae. Inside larval tubes, the abundance of known about the effects of tube-dwelling invertebrates on methane-oxidizing (Kajan and Frenzel 1999) and iron- the role of polyphosphate storing bacteria, and clearly oxidizing bacteria (Lagauzere et al. 2011) is significantly much more research is needed. 338 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

Microbes associated with the N cycle are also affected exchange (Meile et al. 2005), intermittent pumping by tube-dwelling invertebrates. For example, the abun- (Boudreau and Marinelli 1993, Shull et al. 2009), and dance and activity of nitrifying bacteria in sediments is how tube abundance and geometry vary with depth affected by the deposit-feeding activity of chironomids. (Furukawa et al. 2001). To integrate geochemical, Grazing at the sediment surface reduces nitrifier microbial, and macrobenthic processes in a mechanisti- abundance, while ventilation of tubes in deeper layers cally adequate representation, small-scale reactive trans- increases nitrifier abundance through supply of oxygen port models need to be developed that explicitly account and ammonium (Stief and de Beer 2006). However, the for burrow geometry, advective and diffusive transport, decrease in nitrification activity at the oxygen-rich and biogeochemical reactions, requiring representations sediment surface is larger than the concomitant increase in three dimensions (or two dimensions where symme- in nitrification activity in the oxygen-poor subsurface tries can be exploited; e.g., Koretsky et al. 2005, Na et al. layers, which results in an overall net decrease of 2008, Volkenborn et al. 2012). nitrification activity in chironomid-inhabited sediment Bioirrigation models for permeable sediments have (Stief and de Beer 2006). This is another example of how recently begun to incorporate the effects of pumping on the net effect of chironomid larvae (in this case, on the advection of surrounding sediments (e.g., Timmer- nitrifier abundance and overall nitrification rate) can be man et al. 2002, Meysman et al. 2006). However, in mediated by interactions with opposing effects. muddy sediments, advection has been neglected so far The overall effects of tube dwellers on changes in (e.g., Kristensen et al. 2012). Roskosch et al. (2010a) abundance of different functional groups of bacteria and provided first indications that advection may be relevant the consequent effects on benthic element cycling and close to U-shaped burrows of C. plumosus in muddy element budgets remain largely unknown. Furthermore, sediment. By using a three-dimensional model of a data on microbial activity in the vicinity of burrows is chironomid burrow, Brand et al. (2013) showed that this even more scarce than data on abundance, and effect indeed plays a role in moderately permeable information on the microbial response to fluctuating sediments. Here, advection does not necessarily result in redox conditions, as well as their potential to buffer an increased uptake of oxygen in the sediments, since the fluxes via storage compounds such as polyphosphates, is advective flow into the sediment at the outlet branch is extremely limited. compensated by an advective flow towards the inlet YNTHESIS Given current knowledge on the relationship between branch, which opposes the diffusive flux into the the activities of tube-dwelling invertebrates, their asso- sediment. The most important consequence of burrow &S ciated microorganisms, and sediment biogeochemistry, advection is the asymmetry of redox zonations at the it remains elusive to accurately quantify the full suite of inlet and outlet, which defines the reaction space of the effects of tube-dwelling invertebrates on microbial various redox-dependent reactions (Brand et al. 2013). communities and microbially mediated biogeochemical processes. NUTRIENT CYCLING MEDIATED BY TUBE-DWELLING ONCEPTS INVERTEBRATES C Tube modelling Tube-dwelling invertebrates alter nutrient cycles An effective way to assess the potential importance of through a variety of processes. In addition to altering tube construction and associated activities for geochem- sediment biogeochemistry, they modulate benthic-pe- ical, microbial and macrobenthic processes is to lagic exchange of organic matter and nutrients and integrate them in mechanistic modelling representations. increase sedimentation rates due to their filter-feeding Numerical models are valuable tools to simulate and activity and the entrapment of particulate organic explain processes at small spatial-temporal scales that matter (and hence nutrients) inside their burrows (Fig. are hardly accessible with standard methods. For 1). Lewandowski and Hupfer (2005) highlight further example, redox shifts by intermittent pumping of possible impacts of tube-dwelling chironomids on chironomids take place in zones that are smaller than organic matter and nutrient fluxes by resuspension, the millimeter scale and are thus hard to access even ingestion, and defecation of organic particles. Further- with advanced techniques such as microsensors. In more, chironomids excrete nutrients into the water þ addition, the spatial heterogeneity of the burrow column in dissolved inorganic forms (i.e., NH4 and 3þ environment may preclude the detection of subtle PO4 ) that are available to primary producers and changes in concentration profiles that may heavily heterotrophic bacteria. Finally, effects on bacterial influence fluxes and turnover rates (Brand et al. 2009). communities can further alter nutrient cycling. One Many models dealing with the influence of ventilation notable effect of altered metabolic activity of nitrifying and bioirrigation in the sediment are based on the and denitrifying gut bacteria is the emission of the concept developed by Aller (1980), which describes the greenhouse gas nitrous oxide from oxic/anoxic burrows ventilated, bioirrigated sediment as a collection of and from anoxic guts of C. plumosus (Svensson 1998, radially symmetrical tubes. Expansions of Aller’s Stief et al. 2009). The net effect of all these processes on seminal work have focused on the effect of coupled nutrient fluxes between sediments and water is difficult geochemical reactions on biologically driven solute to predict and may differ between compounds, because August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 339 some of the aforementioned processes affect flux rates in processes (Meile and Van Cappellen 2003: Fig. 1). This opposing directions. For example, aeration of the is particularly important during thermal stratification, sediment by chironomids may increase N flux (Stief when vertical mixing of water and dissolved compounds and Ho¨ lker 2006) and at the same time decrease P flux is suppressed. Water column oxygen concentration is (Lewandowski and Hupfer 2005) from sediments, while further affected by the release of reduced species such as excretion will increase both P and N fluxes. H2S (e.g., Giordani et al. 1996) from the sediment into Over the past 10–15 years, the number of field studies the overlying water column when the buffering capacity quantifying nutrient excretion rates of freshwater of, e.g., metal oxides in surface sediments is exhausted animals has increased considerably, stimulated to a (Lewandowski and Hupfer 2005). Because variation in large extent by the development of ecological stoichi- oxygen distributions at the sediment–water interface can ometry theory (Sterner and Elser 2002). Ecological affect many redox-dependent reactions involving N and stoichiometry theory seeks to understand the coupled P, changes in oxygen mediated by tube-dwellers can cycling of multiple elements (e.g., N and P) and often influence the direction and flux of elements between focuses on elemental ratios. Of particular interest is how sediments and water, and can thus have effects on the ratio of nutrients released by consumers relates to whole-lake nutrient cycling. nutrient ratios in their bodies and their food sources. Tube-dwelling invertebrates also may play a key role While numerous studies on fish, zooplankton, and in the carbon cycle in lakes, particularly in regard to stream invertebrates have explored various components methane fluxes. It has been only recently recognized that of ecological stoichiometry, such studies are much less methane-oxidizing bacteria, which convert methane common for lake benthic invertebrates, with the produced in anoxic sediments to microbial biomass, exception of a few taxa, such as the zebra mussel provide a potentially important energy source for lake Dreissena polymorpha (e.g., Naddafi et al. 2008). food webs (Sanseverino et al. 2012), largely because they

Only a few studies have separated metabolic nutrient are consumed by chironomid larvae (Jones and Grey C excretion from other effects of tube dwellers on nutrient 2011). It can be hypothesized that active burrow ONCEPTS cycling. In fact, studies on nutrient excretion rates of ventilation enhances total methane oxidation to carbon chironomids in lakes are relatively scarce, especially dioxide within the sediment and therewith strongly considering their widespread distributions and high decreases the global warming potential of the carbon gas densities. A literature review revealed only six papers if it is eventually emitted to the atmosphere at the lake reporting on N and/or P excretion rates of lake surface (Bastviken et al. 2011). &S chironomids, and all of these were conducted for Finally, it should be noted that tube-dwelling aquatic eutrophic lakes (Table 2). Mass-specific excretion rates insects can modulate fluxes of carbon and nutrients YNTHESIS varied considerably among studies, especially for N. Only across the land–water interface. Emerging insects such four of these studies measured both N and P excretion as chironomids leave aquatic systems, thereby exporting rates, and mean N:P excretion ratios vary by more than a carbon and other nutrients to the terrestrial landscape factor of 10 among the studies (Table 2). Furthermore, (e.g., Scharnweber et al. 2014). Vander Zanden and none of these studies attempted to relate rates or ratios to Gratton (2011) suggest that emergent insect flux to land nutrient contents or ratios in animal bodies or their food increases as a function of lake size, while deposition of sources, which are goals central to ecological stoichiom- terrestrial particulate organic carbon from land to lakes etry theory. Given the complex and potentially large decreases as a function of lake size (Mehner et al. 2005, effects of chironomids on N and P cycling, it is imperative Vander Zanden and Gratton 2011). So it may be that future studies quantify N and P fluxes due to predicted that net C and nutrient burial rate, as bioturbation, aeration, excretion by benthic invertebrates mediated by aquatic insects, might be reduced with to determine net impacts on nutrient cycles, and place increasing lake size. chironomid-mediated nutrient cycling in a more explicit In summary, tube-dwelling invertebrates can modu- stoichiometric framework. Such an approach will aid in late nutrient fluxes in many ways. The overall changes in developing predictive models of the role of benthic nutrient availability and stoichiometry can in turn invertebrates in biogeochemical cycles and ascertain control primary production and thus, the structure of whether we can predict nutrient cycling effects of benthic the phyto- and zooplankton community. invertebrates using ecological stoichiometry as a concep- tual framework. For example, several of the parameters FILTRATION AND FOOD COMPETITION BETWEEN PELAGIC we use to model whole-lake effects of chironomids (see ZOOPLANKTON AND TUBE-DWELLING INVERTEBRATES Integrative ecosystem modelling) have relevance to nutri- Many tube-dwelling chironomids pump water ent excretion, such as N and P contents of sediments, the through their U-shaped burrows to obtain oxygen and soluble nutrient fraction of egested food, and others planktonic food particles (Walshe 1947). Pumping (Appendix: Table A2). periods are regularly interrupted by non-pumping Bioirrigation and ventilation may affect the oxygen periods. During non-pumping periods, chironomids concentration in the overlying water because sedimen- such as C. plumosus larvae spin conical nets of mucus tary oxygen uptake is strongly enhanced by these in their burrows (Roskosch et al. 2011). After a period 340 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

TABLE 2. N and P excretion rates of lake-dwelling chironomids from field-based studies. Table 2 continues on the next page.

Mass-specific excretion rate Source No. observations N(lgNÁg dry massÀ1ÁhÀ1)à P(lgPÁg dry massÀ1ÁhÀ1)à Devine and Vanni (2002) 21 262.42 (53.07) 33.08 (7.34)

Fukuhara (1985), Yasuda (1989)# 16 112.55 (20.20) 11.18 (3.05) Henry and Santos (2008) 55 72.09 (8.25) 68.56 (9.43) Fukuhara (1985), Yasuda (1989)# 11 84.44 (15.54) 23.13 (2.45) Ta´ trai (1982) 37 1281.79 (63.38) no data Ji et al. (2011) 29 no data 20.77 (2.17) Ji et al. (2011) 15 no data 26.66 (4.96) Note: na, not applicable. Number of replicate excretion rate measurements. Each replicate usually contains several individuals, placed together in one container. à Mean with SE in parentheses. § Mean and range (in parentheses), if available. } Dry mass estimated by multiplying wet mass times 0.167 (Waters 1977). # Fukuhara and Yasuda (1985) report data on P excretion, while Fukuhara and Yasuda (1989) report N excretion data, from the same study.

of pumping, the nets with all entrapped particles are and transmissometry (LISST) sensors could be used to eaten. As a result, chironomids can be very efficient filter quantify filtration performance for different particles. feeders, transporting significant amounts of particulate Laboratory experiments not only allow for controlled organic matter and nutrients into the sediment. Chiron- environmental conditions, but also enable easy access to omids drastically reduce particle densities in the burrow the inlet and outlet of individual burrows. Additionally, outlet fluid compared to the inlet fluid (Morad et al. medium-scale mesocosm or enclosure experiments mim- 2010). Based on known pumping rates, filtration effects icking more natural conditions and complementing the at the lake-wide scale might be comparable to the small-scale experiments should be used as well. Such YNTHESIS increased water clarity and shifts in phytoplankton experiments might be conducted, for example, with communities associated with expanding dreissenid mus- different densities of tube-dwelling invertebrates under

&S sels (Strayer 2009). A few studies on marine tube- realistic temperature and light regimes with varying dwelling invertebrates report size-specific and particle- sediment compositions. Experiments should be run from type-specific retention efficiencies. For example, Chris- spring (when cladocerans dominate zooplankton assem- tensen et al. (2000) reported that the polychaete, Hediste blages) until late summer (when copepods dominate) to diversicolor, has a capacity to retain phytoplankton at a account for seasonal fluctuations in zooplankton graz- ONCEPTS rate of 139 mmol CÁmÀ2ÁdÀ1. Riisga˚ rd (1991) found that ing pressure. C for H. diversicolor, retention efficiency was 100% for Because tube-dwelling invertebrates compete for food particles .7.5 lm, 86% for 6.3-lm particles, and 30% resources with filter-feeding pelagic zooplankton, it is for 3-lm particles. Similarly, Griffen et al. (2004) found essential to determine the relative grazing impact of 90% retention efficiency for particles .7.5 lm for the chironomids on plankton communities compared to the mud shrimp Upogebia pugettensis. pelagic zooplankton. In shallow polymictic Mu¨ ggelsee, a In contrast to data on marine benthic animals, well-studied lake with respect to the impacts of environ- surprisingly, there is no systematic study of the filtration mental change on plankton communities (Adrian et al. efficiency of chironomids that allows quantification of 2006, Wagner and Adrian 2009), the filtration capacity of their grazing impacts on phytoplankton, microorgan- chironomids was on the same order of magnitude as that isms, and small zooplankton communities. It is essential of daphnids, which are traditionally thought to be the to experimentally quantify retention efficiencies of grazers that exert the strongest effects on phytoplankton. chironomids for different particle qualities and sizes These estimates were based on observed chironomid under different environmental conditions. Particle set- densities in the sediment of the lake in 2005 (mean 700 tlement and adhesion within burrows also causes an individuals/m2 [Roskosch et al. 2010b]), long-term average unknown fraction of phytoplankton retention (Griffen (1980–2010) daphnid abundances in the pelagic zone et al. 2004). Experiments might be conducted by adding (mean 1980–1994, 37.48 individuals/L; mean 1995–2010, chironomids to microcosms filled with lake sediment 23.8 individuals/L [Gerten and Adrian 2000; R. Adrian, and overlying water. Particle image velocimetry (PIV), unpublished data]), average chironomid pumping rates of particle tracking velocimetry (PTV), and laser-induced 60 mL/h, and average Daphnia filtration rates of 400 fluorescence (LIF) might be applied to determine flow lLÁindividualÀ1ÁhÀ1. The estimates show that chironomids velocities above burrow openings and to characterize are capable of filtering the entire volume of the lake once different natural and artificial particles entering and every 5 days (;1m3ÁmÀ2ÁdÀ1) whereas daphnids clear the leaving the burrows. Additionally, laser in situ scattering lake volume every 5–15 days (;0.3–1.0 m3ÁmÀ2ÁdÀ1;R. August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 341

TABLE 2. Extended.

N:P excretion Abundance Biomass Biomass ratio molar (no./m2)§ (g wet mass/m2)§ (g dry mass/m2)§ Species investigated 19.75 (4.01) 513 (0–4348) 0.036 (0–4.92) unidentified, mixed species (probably Chironomini and Tanytarsini) 42.35 (7.62) no data 3.10 0.52} Chironomus plumosus 3.36 (0.41) 1398 (9–12907) 0.034 (0.000001–424) mostly Chironomus sp. 7.95 (0.66) no data 9.31 1.55} Tokunagayusurika akamusi na no data no data no data Chironomus sp. na no data (,0.1–84) Chironomus sp. na no data (,0.1–84) Tanypus sp.

Adrian, unpublished data). Clearance rates of pelagic are believed to be the most important in shallow lakes. Dreissena veligers are within the range of those reported Lammens et al. (1985) calculated, for example, that, when for cladocerans (MacIsaac et al. 1992). In Mu¨ ggelsee, conditions for bream (Abramis brama) are optimal, these cladocerans and Dreissena larvae had similar abundances fish can consume ;10% of chironomid standing biomass during summer, but their abundances were negatively per day. During an extensive analysis of the phosphorus correlated (Wilhelm and Adrian 2007). Thus, the relative flows within in the Loosdrecht lakes (the Netherlands), proportion of chironomid filtration efficiency on phyto- the feeding pressure of fish on benthos was estimated to plankton remained equally important in strong or weak be 1.4 mg PÁmÀ2ÁdÀ1 (or0.06gCÁmÀ2ÁdÀ1) while the cladoceran years. Although the grazing impact of settled concentration of soluble reactive phosphorus was very adult Dreissena mussels can be .1000 times greater than low (2 lg/L; Van Liere and Janse 1992). This consump- C

that that of veligers, their effects are likely restricted to tive removal of biomass and nutrients can result in ONCEPTS hard substrates above nearshore Dreissena beds (Mac- trophic cascades in both benthic and pelagic food chains, Isaac et al. 1992). Tube-dwelling chironomids filter water depending on the consumptive impact of chironomids in from layers close to sediments and thus affect the whole these chains. Furthermore, the consumption and release water column only in well-mixed water bodies. In of nutrients by predators of chironomids can represent an contrast, filter-feeding daphnids often affect the entire important flux of nutrients within the benthic habitat &S upper water column of shallow lakes. Thus, information and/or an important translocation of nutrients from the

on filtration rates alone may not necessarily predict the benthos to the water column (Vanni 2002). There is also YNTHESIS relative whole-lake effects of these different suspension evidence that a substantial portion of pupal mortalities is feeder groups. In addition, we need information on the caused by predation. Wagner et al. (2012) reported spatial scales over which they exert effects. temporary coupling of the benthic and pelagic food webs Given their high filtering rates, chironomids may by pelagic fish feeding on ascending chironomid pupae. compete with the filtering zooplankton for the same Finally, the C:N:P content of the benthos community as food resources, although vertical habitat segregation of well as the rates (and ratios) by which benthic inverte- the two groups may lessen these competitive interactions (Fig. 1). Moreover, the grazing pressure exerted by chironomids is much more constant across seasons compared to that of the pelagic zooplankton, whose abundances show stronger seasonal fluctuations (Fig. 2). The grazing impact of tube-dwelling chironomids on pelagic phytoplankton and small zooplankton has been neglected in pelagic food web models (Sommer et al. 2012), but may account for some of the unexplained interannual variability of plankton communities in productive lakes. Clearly, competitive interactions be- tween tube-dwelling invertebrates and zooplankton are possible and need to be explored experimentally. FIG. 2. Hypothetical grazing of filter feeders and biomasses IMPACTS OF PREDATORS ON TUBE-DWELLING of edible (zooplankton; light gray) and non-edible (tube- dwelling invertebrates; dark gray) algae in a eutrophic lake INVERTEBRATES AND NUTRIENT DYNAMICS (modified version of the PEG model of Sommer et al. [1986]). The larvae and pupae of tube-dwelling invertebrates The grazing pressure exerted by tube-dwelling invertebrates are important food items for many fish, amphibians, (dashed line) is much more constant across seasons compared to that of the pelagic zooplankton (solid line), whose crayfish, amphipods, and insects such as stoneflies, abundances show strong seasonal fluctuations causing, e.g., a dragonflies, true bugs, and beetles (e.g., Armitage et al. clear-water phase caused in combination with nutrient limita- 1995). Of the different predator groups, benthivorous fish tion and sedimentation. 342 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

brates transport and release nutrients can be altered via sediment structure in a way that facilitates wave size-selective predation on benthic invertebrates (Carpen- resuspension of sediment (Scheffer et al. 2003). Howev- ter et al. 1992, Vanni 2002). er, these fish can also alter the abundance and Predators can also exert non-consumptive effects on distribution of benthic invertebrates. Based on an benthic communities, i.e., by eliciting antipredator empirical relationship and a minimal model, Persson responses in prey, including habitat shifts that provide and Nilsson (2007) conclude that shallow lake systems refuge from predators and associated diet shifts that should be more resistant to switches from a clear to a balance trade-offs between foraging and risk avoidance turbid state when (1) benthic invertebrate biomass, (Schmitz et al. 2010). This in turn can alter ecosystem maximum size of benthivorous fish, and giving up processes related to nutrient cycling (Stief and Ho¨ lker density (the amount of benthic food left behind by 2006, Premo and Tyler 2013). Like many other benthic foragers) are high, and (2) biomass of benthivorous fish organisms, tube-dwelling chironomids can detect chem- is low. Thus, shifts between alternate states likely depend icals from fish and can respond with distinctive on the activities of predators and benthic invertebrates, avoidance behaviors. For example, Chironomus riparius as well as interactions between these two groups (for responds to predators by decreasing both the duration further details, see also Alternative stable states). of excursions outside their tubes and the lengths of their bodies exposed to predators (Ho¨ lker and Stief 2005). IMPACTS AT THE LAKE-WIDE SCALE This predator-avoidance behavior significantly increases Although there is ample evidence that tube-dwelling the exposure of freshly deposited organic particles to invertebrates act as tiny ecosystem engineers that oxygen, by reducing their burial in subsurface layers and significantly alter multiple important ecosystem func- by enhancing the aeration of subsurface layers via tions, it is difficult to assess their importance at a lake- burrow ventilation, conditions that together increase the wide scale. Many of the processes we have discussed rate of organic matter mineralization (Stief and Ho¨ lker interact and their combined effects are therefore difficult 2006). This is related to non-consumptive effects of to quantify. Models can be useful tools for assessing the predators that decrease zebra mussel clearance rate and propagation of processes to the ecosystem level. thus the impact of zebra mussels on phytoplankton However, we feel that existing conceptual and numerical (Naddafi et al. 2008). models of shallow lake ecosystems, such as the PEG YNTHESIS Both consumptive and non-consumptive predator model or PCLake, insufficiently account for the presence effects potentially lead to changes in the spatial of tube-dwelling invertebrates and their interactions &S distributions of organic matter in sediments. The relative within the food web (Mooij et al. 2010, Sommer et al. importance of non-consumptive vs. consumptive effects 2012). Here, we consider how tube-dwelling inverte- remains a matter of debate, even though recent studies brates can be better integrated into two conceptual on other predator–prey systems have clearly shown that models that address two of the most influential concepts non-consumptive effects can be as strong as, or even in lake ecology, seasonal succession, and alternative ONCEPTS

C more than an order of magnitude stronger than, stable states. Then we modify an established dynamical consumptive effects (Peacor and Werner 2001, Schmitz ecosystem model to assess how tube-dwelling inverte- et al. 2004, Ho¨ lker and Mehner 2005). Schmitz et al. brates influence lakes at the ecosystem level. (2010) suggest that consumptive effects may have little net effect on organic matter decomposition and redis- Seasonal succession: the PEG model tribution between sediments and overlying water. Lake phytoplankton and zooplankton communities Instead, non-consumptive effects cause redistribution undergo an annual seasonal succession in relation to of organic matter because the variation in predation risk nutrient availability, predation, and competition (Bro¨ n- may alter the spatial availability of nutrients in the water mark and Hansson 2005, Sommer et al. 2012). To column. Tracking non-consumptive effects is a chal- explain these dynamics, the PEG model was proposed, lenging task, but an important one, if we are to gain a and later revised, by Sommer et al. (1986, 2012; Fig. 2). better understanding of the functional role of predators A prominent feature of the model is the clear-water for carbon flow and nutrient cycling in aquatic systems. phase, a period of low phytoplankton biomass and Experiments are urgently needed, in which consumptive hence high water transparency, which is explained by a vs. non-consumptive effects are quantitatively evaluated. combination of zooplankton grazing, nutrient limita- It should be noted that effects of benthic invertebrates tion, and sedimentation. Strong fluctuations in the on bioturbation, redistribution of organic matter, and population density of pelagic zooplankton and density- nutrient cycling must be evaluated in comparison to mediated grazing dynamics are regarded as the main other organisms that may have similar kinds of effects, top-down effects influencing phytoplankton, including such as fish. The feeding activity of benthivorous fish the clear-water period. However, these interactions are may directly cause bioturbation and resuspension of the likely heavily influenced by filter-feeding benthic inver- sediment and mobilization of nutrients (Persson and tebrates. Based on impacts of dreissenids (e.g., Strayer Nilsson 2007, Ada´ mek and Marsˇa´ lek 2013). In addition, 2009), the filter-feeding activity of other benthic it has been shown that benthivorous fish affect the invertebrates can be expected to exert a relevant feeding August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 343 pressure on the phytoplankton community, and perhaps lakes can occur in either contrasting state, at a given small zooplankton, and hence affect the entire plank- nutrient input rate (Scheffer 1998). tonic community. An important factor delaying the ecosystem response Roskosch et al. (2012) showed the existence of to reduced external nutrient loading is the persistent seasonal and temperature-dependent variation in chi- internal nutrient loading from nutrient-rich sediments. ronomid metabolism and filter-feeding activity, resulting In addition, several positive feedback loops in the food in somewhat higher ventilation rates during summer. web and the abiotic environment act as self-stabilizing However, in contrast to zooplankton, for which the buffering mechanisms. For example, at high phyto- overall feeding activity is dependent on both tempera- plankton concentrations, macrophytes are suppressed ture and population density, the feeding pressure by by shading. As a result, the nutrients that were formerly benthic invertebrates is less dynamic throughout the sequestered by macrophytes become available for year because there is usually less seasonal variation in phytoplankton, causing a further increase in phyto- population density due to overlapping generations and plankton and decrease in transparency. In addition, with species (e.g., Armitage et al. 1995, Ho¨ lker and Breckling fewer plant roots to stabilize the sediment, wind-driven 2002, Roskosch et al. 2010b; Fig. 2). Thus, food-web resuspension and bioturbation by fish leads to even impacts of tube-dwelling invertebrates might be espe- more turbidity. As plants are generally better compet- cially relevant during periods of relatively low zoo- itors for nutrients than phytoplankton are when light is plankton abundances. In many temperate lakes, abundant, the same feedback loops, but in the opposite zooplankton biomass is high enough to exert strong direction, stabilize the clear-water state once it is top-down effects on phytoplankton only for a few attained. Such positive feedbacks are the key ingredients weeks, i.e., during the clear water phase. Thus, it is for the emergence of alternative stable states, whereby possible that tube-dwelling filter feeders are more the strength of feedback loops is important for important grazers than zooplankton during most of determining the resilience of the contrasting states. C the year. Quantifying the relative importance of the Scheffer et al. (1993) presented a conceptual model ONCEPTS more constant grazing impact of tube-dwelling filter summarizing the prevailing feedback mechanisms (Fig. feeders across seasons, as opposed to temporally 3). A simple way of evaluating whether the overall effect fluctuating grazing pressure of cladoceran-dominated of a set of indirect interactions is positive or negative is (spring) vs. copepod-dominated (summer) zooplankton to multiply the signs along the path of that loop (Fig. 3). communities, is an urgent need, and may help to Filter-feeding invertebrates influence many of the &S understand some of the unexplained variability in processes and groups that are part of known stabilizing phytoplankton succession still confronting ecologists feedback loops (Fig. 3). Therefore, their abundance and YNTHESIS (Cottingham et al. 2001). functioning are probably important for determining the If tube-dwelling filter feeders exert significant grazing nonlinear response of lakes to external pressures. For on phytoplankton and small zooplankton, this implies example, by influencing the biogeochemistry in sediments, that they may also exert a competitive pressure on pelagic tube-dwelling invertebrates have the potential to induce a zooplankton for food resources (Fig. 1). For example, net influx or net outflux of nutrients from the sediment, tube-dwelling filter feeders might contribute to the which will strengthen or dampen the competition for collapse of zooplankton communities when food resourc- nutrients between phytoplankton and macrophytes (see es become scarce after a peak in zooplankton biomass. Nutrient cycling mediated by tube-dwelling invertebrates). Because tube-dwelling filter feeders are capable of Chironomid species can also modulate the nutrient- utilizing alternative food resources (e.g., detritus), their related feedbacks by extracting nutrients when they hatch pressure on the phytoplankton community may remain and fly away, which will favor the clear water condition high, and therefore they may postpone or dampen (see Nutrient cycling mediated by tube-dwelling inverte- subsequent growth peaks of phyto- and zooplankton. brates). Via their high grazing pressure on phytoplank- These hypotheses need to be tested with field experiments. ton, filter-feeding benthos may exert a negative feedback by depleting algal resources (see Filtration and food Alternative stable states competition between pelagic zooplankton and tube-dwelling The concept of ecosystem state plays an important invertebrates). Yet, by clearing the water column tube- role in lake ecology and management. Classical theory dwelling benthos can relieve aquatic plants from their on alternative stable states predicts that shallow lakes competition with phytoplankton for light and nutrients, can exist in one of two contrasting states, clear or turbid, which stimulates the clear-water state. In a similar way, which are resilient to changes in external pressures the trapping of particulate organic matter is important in (Scheffer 1998). Indeed, while many vegetated clear keeping the water clear. Also the consumer–resource lakes have become turbid and eutrophic because of interaction with benthivorous fish, which influences the excessive nutrient input, restoration efforts to restore the turbidity via bioturbation, is in itself a negative feedback clear state have shown to be less effective than expected, (see Impacts of predators on tube-dwelling invertebrates as lakes tend to linger in a turbid state. Apparently, over and nutrient dynamics). However, phytoplankton can a substantial range of external nutrient loading rates, benefit from the bioturbation, whereby the turbidity is 344 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

FIG. 3. Interactions and feedbacks in a lake ecosystem concerning water turbidity, including the (partly unknown) effects of tube-dwelling invertebrates (in gray) that may cause alternative equilibria. Both turbidity and aquatic plants have a positive effect on themselves through different feedback loops, of which several are influenced by tube-dwelling invertebrates (figure modified

YNTHESIS from Scheffer et al. [1993]).

&S further enhanced. Lammens et al. (1985) showed that on phytoplankton productivity (due to grazing and omnivorous fish can use chironomids as an alternative changes in nutrient availability and stoichiometry), on food source, allowing them to maintain high biomass and zooplankton (due to food competition and grazing hence a high predation pressure on zooplankton, which is pressure), and on biogeochemical cycles. Also, the a more favorable food source. Phytoplankton benefit importance of the relatively constant grazing of tube-

ONCEPTS from this apparent competition, which thus stimulates the dwelling filter feeders across seasons, compared to the C turbid state. more temporally dynamic grazing capacity of zooplank- Considering the potentially large impacts of tube- ton, can be evaluated (Fig. 2). Finally, and importantly dwelling invertebrates on system processes and the the models allow us to explore feedback loops that may importance of feedbacks in governing the dynamics of be altered by these important consumers (Fig. 3). shallow lake ecosystems, it is essential that we learn Due to its extensive coverage of the aquatic food web, more about feedbacks that are influenced or established and by embracing several more key concepts such as by this group of consumers. As such, it is important to nutrient cycles, stoichiometry, and benthic-pelagic cou- gain more insight into how omnivorous feeding by pling, the ecosystem model PCLake is particularly suited chironomids and fish, and the resulting apparent for studying the impacts of tube-dwelling filter feeders, competition, influences the negative feedback in con- and assessing their importance for self-stabilizing mech- sumer–resource interactions. Also, we identify the need anisms within the framework of alternative stable states to investigate how changes in the abiotic environment (Mooij et al. 2010). This model describes the dynamics of feedback to the tube-dwelling invertebrate abundance, nutrients, phytoplankton, macrophytes, and upper tro- such as anoxia and the consolidation of the sediment by phic levels within the framework of closed cycles of plant roots and wind-induced sediment resuspension. nutrients and organic matter (Janse 2005, Janse et al. 2010; Fig. 4). PCLake has been calibrated against data Integrative ecosystem modelling from .40 lakes, resulting in lake characteristics resem- Integrative dynamical models can be useful tools to bling an ‘‘average’’ shallow lake in the temperate zone elucidate the relative importance of hypothesized (i.e., mean depth ¼ 2 m, areal hydraulic loading ¼ 20 mm/ processes for ecosystem functioning under different d, fetch ¼ 1000 m, slightly clayish sediment, no environmental conditions and various management surrounding wetland zone [Janse et al. 2010: Appendix]). scenarios. They allow for upscaling the aforementioned We used PCLake to analyze the importance of tube direct and indirect effects of tube-dwelling filter feeders dwelling filter feeders for water quality and trophic state August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 345 C ONCEPTS

FIG. 4. Structure of the ecosystem model PCLake, including the role of tube-dwelling invertebrates (modified from Janse [2005]). Black arrows with solid lines denote mass fluxes (e.g., food relations), black arrows with dotted lines denote other interactions. Red arrows with solid lines denote mass fluxes and red arrows with dotted lines denote other interactions that should be considered in future studies. Minus sign denotes negative influence (otherwise positive influence). &S in the context of alternative stable states. We tested two detritus only (not on phytoplankton in the water working hypothesis (scenarios) for a typical temperate column). Thus the top-down control of pelagic phyto- YNTHESIS shallow lake (as defined by Janse et al. 2010). Bifurcation plankton is of less importance in this scenario. Rather, analysis was used to explore effects for ecosystem-level this first analysis assesses the importance of the trophic parameters, along with manual inspection of individual interactions with benthivorous fish; specifically, an process rates (for details, see Appendix). increase in benthic invertebrates sustains a larger Scenario 1.—As a first step, we analyzed how the population of benthivorous fish, which stimulates fish- default implementation of benthic invertebrates affects mediated resuspension of inorganic matter and nutri- ecosystem functioning by varying the density of the ents, and enhances the resilience of the turbid state via zoobenthos. As in the original model, the benthic these mechanisms (Fig. 5). This mechanism is further invertebrates feed on sediment phytoplankton and discussed by Lischke et al. (2014). Conversely, when

FIG. 5. PCLake simulations of chlorophyll a (mean of summer half-year after 20 years) as a function of phosphorus loading for a default lake (medium zoobenthos abundances), a lake with high zoobenthos abundances, and a zoobenthos- free lake. Simulations based on two initial states: a clear-water state and step-wise increase of P load and a turbid state with phytoplankton dominance and step-wise decrease of P load. Other settings were identical with the shallow (2 m depth) default lake (default PCLake settings) and no filter-feeding of zoobenthos. The nitrogen loading was assumed to be always 10 times that of the phosphorus loading. Arrows denote the direction of the hysteresis loop. 346 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

FIG. 6. PCLake simulations of chlorophyll a concentrations (mean of summer half-year after 20 years) as a function of phosphorus loading, for default PCLake settings, and for the inclusion of a filter-feeding invertebrate group (e.g., chirono- mids). Arrows denote the direction of the hysteresis loop. Note: compared to Fig. 5, the x-axis has a different range.

benthic invertebrates are removed from the system, the CONCLUSIONS population of benthivorous fish collapses and the system Our evaluation of the current state of knowledge on becomes less sensitive to nutrient loading. the ecological roles and importance of tube-dwelling Scenario 2.—Next we expanded the PCLake model to invertebrates identified five major research domains that include a filter-feeding chironomid group. Based on the are insufficiently studied, and thus limit our understand- many ways that chironomids can interact with other ing of the role of tube-dwelling invertebrates in lake ecosystem components, we established several interac- ecosystems (Table 3). Major gaps in knowledge include tions, including filtering of the water column, the our understanding of how small ecosystem engineers YNTHESIS consumption of phytoplankton and detritus (leading to impact redox zonation, the microbial sediment commu- direct competition for food with zooplankton), seques- nity, organic matter and nutrient turnover, nutrient

&S tration of carbon and nutrients in sediments, excretion excretion and stoichiometry, filtration and food compe- of nutrients into the water column (both altering tition, and feedback mechanisms that influence other nutrient dynamics and stoichiometry), predation by organisms and even whole ecosystems. To overcome benthivorous fish, and extraction of matter during these scientific knowledge gaps we need integrated emergence. The bifurcation analysis reveals a clear research programs incorporating physical, biogeochem- ONCEPTS impact of chironomids on the system; phytoplankton ical and trophic processes, and their interactions, C biomass (chlorophyll) is lowered in the presence of mediated by tube-dwelling invertebrates. chironomids, at virtually all P loading rates. Further- Taxa such as the abundant and widespread chironomid more, the critical P loading rate needed to induce a larvae may significantly shape their habitat and impact catastrophic regime shift increases greatly (Fig. 6). Thus, the biogeochemical cycling of nutrients limiting lake the models suggest that chironomids confer resilience to primary production. Within a food web context, tube- shallow lakes in terms of maintaining the clear-water dwelling macrozoobenthos are probably more important state. The results of this scenario should be interpreted players than previously assumed, with far reaching with care because the parameter values we used are still ecosystem consequences. We suggest investigating the uncertain, the expanded model was not recalibrated to manifold impacts of model organisms such as C. real lakes, and a connection with a more detailed model plumosus. The central hypothesis of future studies could of individual tubes has not been made. However, the be that tiny but abundant ecosystem engineers, in results clearly indicate that the ecosystem-level effects of particular tube-dwelling invertebrates, exert high filter- tube-dwelling invertebrates are potentially very signifi- feeding pressure and affect biogeochemical cycles in cant (Fig. 6). This potential importance of tube-dwelling shallow lake ecosystems. Given the abundance of shallow invertebrates has long been overlooked, and their lake ecosystems, the cumulative effects of these animals filtration rate has probably been by mistake incorporat- may be substantial at the global or at least regional scale. ed into that of zooplankton during earlier model Experimental investigations should incorporate many calibrations (Janse et al. 2010). We thus conclude that spatial scales, from the burrow (filtration capacity, tube the inclusion of tube-dwelling filter-feeders is likely to microbiology, and sediment geochemistry) to large increase model validity and predictive power, potentially mesocosms (phytoplankton filtration, competition with leading to more complete understanding of shallow lake pelagic filter feeders, and nutrient cycling), preferably as food webs and successful applications of the model for complementary approaches within the same set of lakes. water quality management. The experimental findings need to be integrated into lake August 2015 TINY ECOSYSTEM ENGINEERS, LARGE EFFECTS 347

TABLE 3. Five main general research domains that deserve more attention in studies of how tube-dwelling invertebrates affect shallow lake ecosystems.

Impacts of tube- Impacts of predators on Small-scale tube dwelling invertebrates Filtration and food tube-dwelling invertebrates Impacts at the lake- biogeochemistry on nutrient cycling competition and nutrient dynamics wide scale How is the capacity of Do tube-dwelling What is the filtration Do top predators (e.g., Are benthic filter- P immobilization and invertebrates alter the efficiency of benthivorous fish) feeders able to remobilization availability of P, N, dominant tube- regulate nutrient cycling impact pelagic impacted by tube- and organic C in the dwelling in aquatic systems via phyto- and dwelling invertebrate water column (water invertebrates? predator induced zooplankton density, geochemical quality) and thus changes of tube-dwelling communities? sediment composition influences algal invertebrates to a (e.g., iron and growth due to altered relevant extent? organic content), and biogeochemical system state (e.g., turnover? clear vs. turbid)? Is there a long-term How do the various How is the filter rate of Do consumptive effects How does the physical impact of tube- mechanisms by which tube-dwelling may have little net effect environment dwelling invertebrates tube-dwelling inverts invertebrates on organic matter feedback to benthic on P burial rates? mediate nutrient impacted by particle decomposition and filter-feeders in terms cycling (bioturbation, properties and redistribution between of anoxia and aeration, excretion, environmental sediments and overlying sediment structure? etc.) interact and conditions? water, whereas non- impact on nutrient consumptive effects cycles? cause redistribution of organic matter? Do tube-dwelling Does the change in How does omnivory To what extent does the Can small but C invertebrates severely nutrient availability influence the feeding activity of abundant tube- impact the microbial and stoichiometry consumer resource benthivorous fish cause dwelling invertebrates ONCEPTS community of control primary interactions and the resuspension of the significantly affect the burrow walls? production and thus, filter rate? sediment? state of shallow lake the structure of the ecosystems? phyto- and zooplankton community? &S How do tube-dwelling Can we predict nutrient Do tube-dwelling tube- How does the relative invertebrates effect cycling effects of dwelling invertebrates importance of the subtle change in tube-dwelling inverts exert a relevant benthic versus pelagic YNTHESIS abundance of using ecological feeding pressure on zooplankton grazing nitrifiers and maybe stoichiometry as a small zooplankton? change especially in other bacteria on conceptual the context of global benthic element framework? warming? cycling? Are tube-dwelling Can aquatic insect Do tube-dwelling tube- Which relevant invertebrates larvae modulate dwelling invertebrates functional traits have cultivating certain fluxes of organic exert a relevant to be integrated in bacterial tube matter and nutrient feeding pressure on future ecosystem communities for also across the water- the phytoplankton models? food? terrestrial interface? community? Do competitive interactions between planktonic and benthic filter feeders exist? ecosystem models by including nutrient cycling and food compensatory mechanisms can reconfigure food webs web interactions mediated by benthic invertebrates. The such that they maintain ecosystem functioning in the face models can be used to reassess the role of these tiny of disturbance. It can be hypothesized that the relative ecosystem engineers for the trophic state of shallow lakes importance of tube-dwelling invertebrates vs. zooplank- and to better predict how lake restoration measures such ton grazing might change in the context of global as lake aeration or destratification might alter habitat warming. Climate scenarios predict shifts from dimictic distribution of redox zones. Such measures may result in to monomictic thermal regimes in many lakes by the end increased habitats for tube-dwelling invertebrates and, of the 21st century (Kirillin 2010), i.e., winter stratifica- because of their ventilation activity, in a more permanent tion will completely disappear in many lakes. In summer, P removal that stabilizes a lower trophic state. climate warming produces an opposite, stabilizing effect, Climate change is altering the global cycles of water, C, i.e., lakes that are already dimictic may stratify more N, and P (e.g., Tranvik et al. 2009). At the same time, stably or for longer durations, and shallow polymictic 348 FRANZ HO¨ LKER ET AL. Ecological Monographs Vol. 85, No. 3

lakes may become dimictic (Adrian et al. 2009). The Bastviken, D., L. J. Tranvik, J. A. Downing, P. M. Crill, and A. ecological consequences of this latter regime shift are Enrich-Prast. 2011. Freshwater methane emissions offset the continental carbon sink. Science 331:50. likely to be more drastic than dimictic-to-monomictic Boudreau, B. P., and R. Marinelli. 1993. Effects of discontin- transitions, because the abrupt detachment of the uous vs. continuous irrigation on dissolved silica fluxes from nutrient-rich hypolimnion from the euphotic zone and marine sediments. Chemical Geology 107:439–441. the increase in hypoxic sediment area is likely to trigger Brand, A., C. Dinkel, and B. Wehrli. 2009. Influence of the stronger competition between autotrophs and a change in diffusive boundary layer on solute dynamics in the sediments of a seiche-driven lake: a model study. Journal of Geophys- the relative proportions of pelagic zooplankton vs. ical Research: Biogeosciences 114:G01010. benthic macroinvertebrates. Future projections of the Brand, A., J. Lewandowski, E. Hamann, and G. Nu¨ tzmann. fluxes of matter and greenhouse gases to and from 2013. Advection around ventilated u-shaped burrows: a aquatic ecosystems, related to natural or anthropogenic model study. Water Resources Research 49:2907–2917. Bro¨ nmark, C., and L. A. Hansson. 2005. The biology of lakes environmental changes, are greatly limited by our ability and ponds. Oxford University Press, Oxford, UK. to characterize the driving forces and in particular the key Buffle, J., R. De Vitre, D. Perret, and G. G. Leppard. 1989. players in aquatic food webs. A better understanding of Physico-chemical characteristics of a colloidal iron phosphate the role of tiny ecosystem engineers in modulating overall species formed at the oxic-anoxic interface of a eutrophic ecosystem functioning will help in predicting future lake. Geochimica et Cosmochimica Acta 53:399–408. Carpenter, S. R., K. L. Cottingham, and D. E. Schindler. 1992. changes in shallow lake ecosystems and the implications Biotic feedbacks in lake phosphorus cycles. Trends in for global matter fluxes. The sheer number of small lakes Ecology and Evolution 7:332–336. suggests that benthic invertebrates are relevant in driving Christensen, B., A. Vedel, and E. Kristensen. 2000. Carbon and small-scale processes that add up to global importance. nitrogen fluxes in sediment inhabited by suspension-feeding (Nereis diversicolor) and non-suspension-feeding (N. virens) ACKNOWLEDGMENTS polychaetes. Marine Ecology Progress Series 192:203–217. Christensen, K. K., H. S. Jensen, F. Ø. Andersen, C. Wigand, This work was supported by the German Research and M. Holmer. 1998. Interferences between root plaque Foundation (DFG, LE 1356/3-1 to J. Lewandowski and formation and phosphorus availability for isoetids in the GR1540/20-1 given to H. P. Grossart), the Netherlands sediments of oligotrophic lakes. Biogeochemistry 43:107–128. Foundation for Applied Water Research (STOWA 443237 to Cottingham, K. L., B. L. Brown, and J. T. Lennon. 2001. J. J. Kuiper and W. M. Mooij), the U.S. National Science Biodiversity may regulate the temporal variability of

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SUPPLEMENTAL MATERIAL Ecological Archives The Appendix is available online: http://dx.doi.org/10.1890/014-1160.1.sm