Herbivory in a Subtropical Seagrass Ecosystem: Separating the Functional Role of Different Grazers
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Vol. 511: 83–91, 2014 MARINE ECOLOGY PROGRESS SERIES Published September 24 doi: 10.3354/meps10901 Mar Ecol Prog Ser Herbivory in a subtropical seagrass ecosystem: separating the functional role of different grazers Ameer Ebrahim1, Andrew D. Olds1,3,*, Paul S. Maxwell1, Kylie A. Pitt1, Dana D. Burfeind1,2, Rod M. Connolly1 1Australian Rivers Institute − Coast and Estuaries, School of Environment, Griffith University, Gold Coast, Queensland 4222, Australia 2School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, Australia 3Present address: School of Science and Engineering, University of the Sunshine Coast, Maroochydore, Queensland 4558, Australia ABSTRACT: Seagrass meadows provide many important ecosystem services, but they are threat- ened by human activities and are in decline globally. In particular, eutrophication arising from human activities promotes algal growth, which negatively affects seagrass. Herbivores consume algae and can, therefore, reduce eutrophication effects, but they may also consume seagrass. Little is known, however, about grazer−epiphyte−seagrass interactions in subtropical seagrass in the Indo-Pacific. We used a 5 wk exclusion experiment to quantify the influence of different graz- ers in seagrass (dominated by Zostera muelleri) in Moreton Bay, eastern Australia. Our results show that herbivory does indeed affect seagrass−epiphyte dynamics in this region and that differ- ent grazers can exert different effects in seagrass ecosystems. In particular, exclusion of small mesograzers (i.e. amphipods and juvenile shrimp) caused epiphyte biomass to increase by up to 233%. Exclusion of medium mesograzers (i.e. small fish and prawns) resulted in increases of up to 10% in seagrass cover, 53% in shoot height and 29% in shoot density. Large mesograzers (i.e. adult fish) and macrograzers (i.e. turtles and dugong) did not appear to play a role in the study system. These results demonstrate that mesograzers can be important in controlling epiphytic algae in subtropical Indo-Pacific seagrass, and show that different mesograzers can affect seagrass− epiphyte dynamics in different ways. It is critical that the functional effects of different herbivores be considered when implementing programs for seagrass conservation and restoration. KEY WORDS: Seagrass · Epiphytes · Herbivory · Mesograzers · Fish · Invertebrates · Moreton Bay · Australia Resale or republication not permitted without written consent of the publisher INTRODUCTION blooms of epiphytic and drift algae and reduce both growth and productivity of seagrasses (Hughes et al. Seagrass meadows are important habitats and 2004, Baden et al. 2010). Herbivores that remove epi- feeding areas for many organisms and support fish- phytic or drift algae have a positive effect on seagrass eries production around the world (Heck et al. 2003, by increasing light availability, which improves pho- Orth et al. 2006, Unsworth & Cullen 2010). Sea- tosynthetic capacity (Hughes et al. 2013, Whalen et grasses are, however, in decline globally due to the al. 2013). Herbivores that graze directly on seagrass, cumulative impacts of disease, declining water quali - on the other hand, can have negative, positive or ty, dredging, overfishing, invasive species and global variable effects (Heck & Valentine 2006). For exam- climate change (Waycott et al. 2009). Many of these ple, heavy grazing that removes substantial biomass stressors increase algal growth, which can lead to can fragment meadows (Fourqurean et al. 2010), *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 84 Mar Ecol Prog Ser 511: 83–91, 2014 whereas lighter grazing can stimulate growth and 2013). It is logical, therefore, to expect that grazing productivity (Valentine et al. 1997, Christianen et al. might be important for seagrass development on the 2012). Grazers may also have a more variable influ- east coast of Australia, but this hypothesis has not yet ence on seagrass by selectively removing particular been tested. species, which can alter the composition of seagrass We conducted a field experiment to evaluate the assemblages (Preen 1995, Burkholder et al. 2012). In role of different grazers in structuring seagrass and order to effectively manage seagrass ecosystems and epiphyte dynamics in Moreton Bay, eastern Austra lia. their accompanying services, it is imperative that Moreton Bay contains extensive seagrass (dominated studies seek to quantify the functional importance of by Zostera muelleri) (Roelfsema et al. 2013), supports different grazers. abundant and diverse seagrass grazers (Tibbetts & Our understanding of grazing effects on seagrass is Connolly 1998), and receives high nutrient loads from complicated by the diversity of herbivores, which in- the adjacent urbanised catchment (Leigh et al. 2013). clude macrograzers (i.e. dugongs, manatees, turtles This situation is now typical in eastern Australia and waterfowl) and mesograzers (i.e. fish and inverte- (Wolanski 2014), and this location was selected so brates) (Heck & Valentine 2006). It is also further com- that results would be relevant to other subtropical pounded by substantial variation in grazing rates and bays in the region. Based on the results of subtropical the role of different grazers in different parts of the studies from elsewhere (Kirsch et al. 2002, Burkholder world (see reviews by Hughes et al. 2004, Heck & et al. 2012, Myers & Heck 2013), we hypothesized Valentine 2006, Valentine & Duffy 2006). Grazing that: (1) large mesograzers (i.e. adult fish) would studies from different locations and latitudes have dominate direct grazing of seagrass and that experi- ten ded to focus on different groups of grazers. Tro- mental exclusion would increase seagrass growth, pical and subtropical studies emphasise the impor- cover, shoot density and shoot height, and (2) small tance of direct grazing on seagrass by fish, urchins, mesograzers (i.e. amphipods and juvenile shrimp) and turtles (e.g. Kirsch et al. 2002, Alcoverro & would dominate grazing of epiphytes and that experi- Mariani 2004, Verges et al. 2011, Christianen et al. mental exclusion would increase epiphyte biomass. 2012), whereas temperate zone studies (with a strong focus on northern Europe) emphasise the role of in- ver tebrate mesograzers (i.e. crustaceans and gastro - MATERIALS AND METHODS pods), which feed on ephemeral and epiphytic algae and rarely consume seagrass directly (e.g. Hillebrand Quantifying the roles of different herbivores et al. 2000, Moksnes et al. 2008, Svensson et al. 2012). Until the end of the 20th century, most studies of The contribution of mesograzers to seagrass and epiphyte−grazer interactions were re stricted to epiphyte dynamics was quantified using a manipula- cooler temperate waters (Heck & Valentine 2006), tive exclusion experiment. The experiment was con- but there is a growing body of work on tropical and ducted over the austral summer (2012−2013) to max- subtropical seagrasses (e.g. Klumpp et al. 1992, imize herbivore abundance and, therefore, herbivory Peterson et al. 2007, Drury McCall et al. 2009, Myers in the study area. Given the difficulty in maintaining & Heck 2013). However, seagrass grazing has not large numbers of exclusion cages over long periods been widely studied on the east coast of Australia, of deployment, the experiment was restricted to a with the exception of studies on large macrograzers single location, Waterloo Bay (27°15’ S, 153°15’ E), in (i.e. turtles and dugong) (e.g. Preen 1995, Brand- western Moreton Bay. This location was selected Gardner et al. 1999, Aragones & Marsh 2000, Kuiper- because it receives high nutrient loads (Gibbes et al. Linley et al. 2007). The focus of seagrass studies in 2014) (mean concentrations over the study period: this region has instead been on the effects of total nitrogen 0.37 mg l−1; total phosphorus 0.05 mg eutrophication and sedimentation (e.g. Carruthers et l−1), has abundant mesograzers (see Table S1 in the al. 2002, Waycott et al. 2005); with an emphasis, in Supplement at www.int-res.com/articles/suppl/ m511 subtropical waters, on understanding the effects of p083_supp.pdf) (Skilleter et al. 2005), and supports a turbidity and nutrient processing (e.g. Abal & Denni- high coverage (80%) of homogeneous Zostera muel- son 1996, Udy & Dennison 1997, Longstaff & Denni- leri, which is typically free from drift algae (Skilleter son 1999). It is now widely appreciated, however, et al. 2005, Maxwell et al. 2014). that the impacts of eutrophication commonly interact The experiment included 70 plots of seagrass: 10 with the effects of grazing in seagrass ecosystems control plots that did not exclude herbivores (Treat- (Baden et al. 2010, Hughes et al. 2013, Whalen et al. ment 1), 40 herbivore exclusion cages (Treatments 2 Ebrahim et al.: Herbivory in subtropical seagrass ecosystems 85 Table 1. Summary of herbivore exclusion treatments: mesh size of cage cover and the type and size of grazers manipulated by each treatment. Macrograzers: turtles, dugong, waterbirds; large mesograzers (>3 cm body depth): adult fish; medium meso- grazers (1–3 cm): juvenile fish, shrimp, prawns; small mesograzers (<1 cm): amphipods, juvenile shrimp and prawns Treatment Mesh size of cage cover Permitted access Excluded access number 1 Uncaged (control) All grazers None 2 6 cm Mesograzers Macrograzers 3 3 cm Medium mesograzers Macrograzers, large mesograzers 4 1 cm (no insecticide) Small mesograzers Macrograzers, large and medium mesograzers 5 1 cm (with insecticide)