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Seagrass Patch Characteristics Alter Direct and Indirect Interactions in a Tritrophic Estuarine Food Web

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Seagrass Patch Characteristics Alter Direct and Indirect Interactions in a Tritrophic Estuarine Food Web Estuaries and Coasts Vol. 29, No. 3, p. 499–510 June 2006 Seagrass Patch Characteristics Alter Direct and Indirect Interactions in a Tritrophic Estuarine Food Web MATTHEW W. JOHNSON1,* and KENNETH L. HECK JR.2 1 Marine Environmental Science Consortium, Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, Alabama 36528 2 University of South Alabama, Department of Marine Sciences, LCSB 25, Mobile, Alabama 36688 ABSTRACT: We used a mesocosm approach to examine how patch characteristics influenced predation and habitat selection in a tritrophic food web. Our experiments included juvenile red drum (Sciaenops ocellatus; RD), juvenile pinfish (Lagodon rhomboides; PF), and grass shrimp (Palaemonetes sp.; GS), members of a food web common in seagrass meadows of the northern Gulf of Mexico. We added an additional level of complexity to the experiment by including a predator that could feed at two different trophic levels. RD were top predators, PF were both prey items for RD and predators of GS, and GS were prey for RD and PF. We used 4 different artificial seagrass habitats that varied by size (0.049 and 0.203 m2) and shape (circular and stellate) to control for covariation between patch size and seagrass density. Predation on GS was measured in each habitat when PF, RD, and PF+RD were present, and predation on PF was measured when RD and RD+GS were present. Habitat selection by each of these 3 species was measured individually and in the presence of every other combination of the 3 species. Neither predation nor habitat selection were consistently influenced by patch characteristics (size, shape, or perimeter:area ratios) or the number of trophic levels. For GS, there was a significant negative relationship between patch size and predation rates in the GS+PF+RD treatment. Habitat selection by GS without the threat of predation suggested a preference for smaller habitats, but when in the presences of RDorRD+PF, GS preferred larger habitats. In predation experiments, PF predation by RD showed no significant relationships with patch characteristics or trophic structure. For our habitat selection experiments, PF preference was for larger habitats in the PF only and GS+PF+RD treatments. There were no significant relationships between patch size, shape, or trophic structure and RD habitat selection. Introduction marine, freshwater, and terrestrial systems (Dill et Direct effects by predators have been well studied al. 2003; Luttbeg et al. 2003; Trussell et al. 2004; and are often easy to identify (Luttbeg et al. 2003). Vance Chalcraft et al. 2004). The introduction of a predator can suppress the Of the studies that have examined these relation- number of prey present in a system (McIntosh and ships, the configuration of habitats can be in- Townsend 1996). Indirect effects can often occur in fluential on indirect interactions. According to Ikeda and Nakasuji (2002), the leaf beetle (Galer- trophic cascades and the effects can be evident to ucella nipponensis) had a higher survival rate in the the resource level (i.e., 3 level trophic cascade: presence of predatory water striders (Gerris nepalen- predator–prey–resource) and be difficult to discern sis) when rosettes of a host plant (Trapa japonica) (Peacor and Werner 2001). Indirect effects at the grow vertically in the water column rather than resource level are possible through two pathways, horizontally on the water’s surface, and female leaf density-mediated indirect interactions (DMII) and beetles preferentially deposited eggs on these trait-mediated indirect interactions (TMII; Miller vertically growing rosettes. Grabowski (2004) and and Kerfoot 1987). DMIIs occur when a prey’s Grabowski and Kimbro (2005) found that oyster resources are released due to the loss of prey to reefs that provided physical relief and complexity predators. TMIIs occur when a predator triggers altered the predation rate of mud crabs (Panopeus a change in the behavior or morphology of its prey, herbstii) on juvenile oysters (Crassostrea virginica) and resulting in effects that cascade down to the prey’s hard clams (Mercenaria mercenaria) in the presence resources (Abrams 1995). The incidence of TMIIs of a predation threat by toadfish (Opsanus tau). increases relative to the amount of DMIIs as the Seagrasses play a critical role in the life histories level of resource increases (Luttbeg et al. 2003). of many aquatic species (Bell et al. 1987; Bostro¨m Both types of indirect interactions have been well 2001; Heck et al. 2003). Despite their importance in studied, with examples being found in many coastal waters, seagrass meadows continue to de- cline worldwide, owing to a myriad of natural and * Corresponding author; current address: Dauphin Island Sea anthropogenic factors (Durako 1994; Duarte 1995; Lab, 101 Bienville Boulevard, Dauphin Island, Alabama 36528; Short and Wyllie-Echeverria 1996; Koch and Gust tele: 251/861-7551; fax: 251/861-7540; e-mail: [email protected] 1999; Eckrich and Holmquist 2000). The result is ß 2006 Estuarine Research Federation 499 500 M. W. Johnson and K. L. Heck Jr. the breakup of once continuous seagrass meadows separated the consequences of variable trophic into smaller functional units (Fonseca and Bell structure from the consequences of variable patch 1998; Seddon et al. 2000). This can produce shifts characteristics. in seagrass patch size, patch shape, and patch We experimentally tested if changes in seagrass perimeter : area (P : A) ratio (i.e., the amount of patch size and shape altered the direct and indirect edge present; see Schumaker [1996] for complete interactions in a tritrophic food chain consisting of discussion). Restoration efforts for seagrasses often red drum (Sciaenops ocellatus), pinfish (Lagodon result in a mosaic of seagrass patches that may rhomboides), and grass shrimp (Palaemonetes sp.). ultimately coalesce (Fonseca 1993; Fonseca et al. We examined predation on pinfish (by red drum) 1998). The presence of smaller patches and in- and grass shrimp (by red drum and pinfish) in four creased edge may influence water flow as well as different habitats that varied by shape and size. We faunal abundance and biological interactions (Fon- predicted that the direct interactions between seca et al. 1982; Keough 1984; Irlandi 1997; Bologna species would result in a greater increase in the and Heck 2000; Caley et al. 2001), yet, little is overall predation rates in the smaller habitats and known about how the alteration of seagrass land- the habitats with increased amounts of perimeter. If scapes may influence direct and indirect interac- DMIIs were present, we expected that increased tions between trophic levels. predation on pinfish by red drum would release Previous experiments examining the roles of grass shrimp from predation and enhance their seagrass patch size and shape relied heavily on the survival. If TMIIs were operating, the presence of species-area concept and found that unlike terres- a red drum predator could either force pinfish into trial environments, larger areas often did not the seagrass refuges, increasing the number of support more species in marine environments interactions between pinfish and grass shrimp and (McNeill and Fairweather 1993; Bologna 1998). resulting in an increased amount of predation of Studies of bivalves have shown that settlement can grass shrimp. In this scenario, larger seagrass occur in greater quantity on patches with increased patches may ultimately be beneficial for grass P : A ratios (Bologna and Heck 2000), but survival shrimp survival due to the increased amount of of juvenile bay scallops (Argopecten irradians concen- refuge. Forcing of pinfish into the structurally tricus) may not be related to perimeter (Irlandi et al. complex seagrass could alternatively decrease the 1999). For studies where grass shrimp (Palaemonetes ability of pinfish to forage effectively, ultimately sp.) and blue crabs (Callinectes sapidus)were enhancing grass shrimp survival in the presence of examined together, grass shrimp were more abun- red drum. If this is the case, then the effects of dant in smaller patches and blue crabs were more patch characteristics would be similar to those that abundant in larger patches (Eggleston et al. 1998). grass shrimp experience when a red drum is the Neither Bell et al. (2001) nor Johnson and Heck only predator present. (2006) found similar relationships between blue We also examined how the threat of predation crabs and grass shrimp. influenced habitat selection by testing every possible These prior studies suggest that the effects of combination of our tritrophic food chain with each changing seagrass patch characteristics in marine possible pairing of our refuge habitats (artificial habitats are more complicated than previously seagrass units or ASUs), and recording the seagrass expected. Experiments have been conducted pri- patch with which each of the taxa were associated marily in situ and were influenced by many variables (in or around ASU) after 24 h. We predicted that (including trophic structure) that fluctuate spatially the direct interactions (DMIIs) between red drum and temporally, resulting in data that are unique to and pinfish would result in more grass shrimp being a particular time. The number of predators in collected in the larger habitats due to a decrease in estuarine habitats is often underestimated (Sheaves predation pressure. For the indirect interactions 2001), and the threat of an unknown predator (DMIIs and TMIIs), we expected that grass shrimp could trigger
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