Impacts of seagrass food webs on marine ecosystems - IngentaConnect

BULLETIN OF MARINE SCIENCE, 71(3): 1361–1368, 2002

IMPACTS OF SEAGRASS FOOD WEBS ON MARINE ECOSYSTEMS: A NEED FOR A BROADER PERSPECTIVE John F. Valentine, Kenneth L. Heck, Jr. and Anna M. Cinkovich ABSTRACT While most recent efforts seek to identify which group of producers (e.g., epiphytic algae, macroalgae, or seagrasses themselves) plays the predominant role in individual seagrass meadows, few have considered the overall importance of all of these components in the flow of energy and nutrients on broader scales. Even though it is widely accepted that seagrass epiphytes can play an important role in controlling local food web productivity, recent results from understudied areas suggest that the importance of seagrasses themselves to marine food webs has been greatly underestimated. There is now ample evidence that grazing on seagrasses, especially in low latitudes, can be substantial. Similarly, the export of seagrass leaves has been correlated with high densities of invertebrates and fishes in both shallow waters and the deep sea. Since seagrass inhabitants (both consumers and their prey) vary greatly from site to site and region to region, our understanding of the importance of seagrasses to marine food webs lags far behind our understanding of such interactions in other habitats. Seagrasses often form extensive meadows that can be found along the coasts of every continent except Antarctica. As such, understanding the dynamics of food web interactions within these habitats, and the degree to which seagrass production is exported, is of considerable theoretical and practical importance.

The primary productivity of seagrass ecosystems is determined by a diverse group of plants that includes the seagrasses themselves, microepiphytic and macroepiphytic algae attached to the seagrass leaves, benthic microalgae and macroalgae living within the seagrass canopy, and phytoplankton. While the relative importance of these plants varies with location, it is clear that the majority of primary production in seagrass meadows comes from the attached algae and seagrasses (Heijs, 1984; Duarte, 1989; Buia et al., 1992; Gallegos et al., 1993; Frankovich and Zieman, 1994; Duarte et al., 1996; Cebrian et al., 1999; Lepoint et al., 2000). Both laboratory and field experiments have shown that, in the absence of predators, small grazers such as amphipods and gastropods (mesograzers) can limit epiphyte abundance and its accumulation on seagrass blades (Klumpp et al., 1992; Neckles et al., 1993; Williams and Rucklehaus, 1993; Mukai and Iijima, 1995; Jernakoff and Nielsen, 1997; Duffy and Hay, 2000; Heck et al., 2000). Their small size, high rates of growth, and low levels of structural and chemical feeding deterrents make algal epiphytes highly palatable for small grazers hiding within seagrass canopies (Orth and von Montfrans, 1984; Klumpp et al., 1989; Edgar, 1990a; Jernakoff et al., 1996; Bostrom and Mattila, 1999). The current view that the great productivity of seagrass food webs is based on algae rather than seagrass detritus represents a newly developed perspective in the study of seagrass food web dynamics. However, epiphytic assemblages vary greatly among locations, and in many areas are composed of organisms of varying palatability (some chemically and others structurally defended). Included are many kinds of algae (e.g., calcareous algae), fungi, ascidians, hydroids, organisms with calcareous exoskeletons (including barnacles and spirorbid polychaetes), as well as larger macroinvertebrates (e.g., amphipods, shrimps, crabs and gastropods) (Willcocks, 1982; Chernoff, 1985; Keough, 1986; 1361

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Borowitzka et al., 1990; Lavery and Vanderklift, 2000). The role of variation in the abundances of these organisms in determining consumer feeding preferences remains unknown. The overall importance of direct herbivory on seagrasses is also variable. There is clear evidence that living leaves are an important source of energy in many coastal food webs (summarized in Valentine and Heck, 1999). Investigators using a variety of methods have shown that living tissue is readily consumed by fishes in large quantities in parts of the Caribbean and Mediterranean Seas, and the Indian and Pacific Oceans. Yet seagrasses often remain uneaten in many areas. In part, the effects of human fishing and hunting can explain the spatial variability in seagrass grazing (Jackson, 1997; Lodge et al., 1998). These activities have significantly reduced the density of large vertebrate grazers (such as waterfowl, turtles and manatees) in both temperate and tropical environments. Additionally, the nutritional value of seagrass leaves may play an important role in determining grazing rates. The high cellulose and low protein content of seagrass leaves, coupled with the presence of chemical feeding deterrents, seem to limit seagrass consumption by some grazers (Bjorndal, 1979, 1980; Mazzella et al., 1992; Williams and Rucklehaus, 1993; Michot and Chadwick, 1994; McGlathery, 1995; Cebrian and Duarte, 1998). Herbivores, however, may have morphological adaptations or digestive capabilities that allow them to obtain nutrients and energy from marine vascular plants. For example, some fishes have low gut pH, allowing them to digest cellulose (e.g., Lobel, 1981; Montgomery and Targett, 1992), while other fishes, reptiles, and sirenians (i.e., manatees and dugongs) possess microbial symbionts capable of digesting cellulose in seagrass leaf tissues (Bjorndal, 1979; Thayer et al., 1984; Luczkovich and Stellway, 1993). Where data exist, the growth rates and secondary production of small seagrass associated invertebrates and fishes rival estimates reported from other marine communities (Coulon et al., 1992; Connolly, 1994; Edgar, 1990a,b; Fredette et al., 1990; Ferrell and Bell, 1991; Valentine and Heck, 1993; Edgar and Shaw, 1995). This means that there are large amounts of animal biomass in the intermediate trophic levels (e.g., isopods, decapods, gastropods and small fishes) (Heck, 1976; Orth and Heck, 1984; Bauer, 1985; Gambi et al., 1992; Greenway, 1995; Williams and Heck, 2001), and that the transfer of energy from seagrass consumers to higher order consumers should be quite high. In fact, seagrass habitats are sites of intense foraging by large predatory fishes (e.g., spotted sea trout, striped bass, jacks, and sharks) (Bell and Westoby, 1987; Heck and Weinstein, 1989; Hetler, 1989; Nojima and Mukai, 1990; Heck and Crowder, 1991; Burke, 1995; Edgar and Shaw, 1995). Surprisingly, there are few studies of the foraging patterns of predatory birds (e.g., ospreys, gulls, and herons) in seagrasses. The consumption of seagrass associated prey by transient predators suggests that productive seagrass communities subsidize the diets of consumers who spend a portion of their time foraging in seagrass habitats. SEAGRASS SUBSIDIES OF REGIONAL FOOD WEBS Ecosystems are open and generally extensive. Both the passive and active transport of materials inextricably link many ecological communities across boundaries via currents, larval drift and active foraging migrations. Movement of nutrients, detritus, prey, and consumers between habitats (i.e., spatial subsidies) can have major effects on food web productivity, especially in places with little or no in situ primary production, (e.g., caves, mountaintops, central ocean gyres, and the deep sea cf. Vetter, (1994, 1995, 1998); Polis

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and Strong, (1996); Persson et al., (1996); Rose and Polis, (1998)). In many locations, seagrass habitats are part of a greater landscape that is composed of both marine and terrestrial habitats, each linked to the other via the foraging patterns of consumers (both predators and herbivores), and the passive drift of seagrass detrital material. Where grazing on seagrass leaves is low, detrital seagrass leaves can be seasonally abundant (Thayer et al., 1977; Fitzhardinge, 1983; Harrison, 1989; Mazzella and Zupo, 1995; Mazzella et al., 1995; Cebrian and Duarte, 1998). Because detached seagrass leaves are carried passively by currents and waves (Robertson and Lucas, 1983; Hemminga and Nieuwenhuize, 1991), in some cases over extensive distances (Menzies and Rowe, 1969; Zieman, 1975; Wolff, 1979; Suchanek et al., 1985; Kenworthy et al., 1989; Lawson et al., 1993; Young et al., 1993), they may represent an important source of energy for other less productive marine habitats (Thresher et al., 1992; Christian and Luzcovich, 1999; Ochieng and Erftemeijer, 1999; Caddy, 2000). Such detrital inputs are likely to be important in areas where primary production is low and where habitat structure is limited. Accumulations of detrital material (in some cases a combination of seagrass leaves and kelp fronds) can support consumers in areas such as deep sea canyons or coastal beaches where they also provide an important refuge from predation for highly vulnerable macroinvertebrates (Lenanton, 1982; Lenanton et al., 1982; Lenanton and Caputi, 1989). The once great numbers of large fish consumers (e.g., groupers, jacks, snappers, sharks, and blue fin tuna), so widely reported in the earlier literature (cf Safina, 1995, 1998; Dayton et al., 1995), appear to have fed in multiple habitats to meet their nutritional needs. As such, natural marine ecosystems may once have been characterized by a high degree of cross habitat energy exchange (Eggleston et al., 1998; Valentine and Heck, 1999). If true, the productivity of seagrass communities has probably played an important role in determining the productivity of consumers in nearby habitats such as salt marshes, coral reefs and mangroves. Early studies of coral reef ecosystems, in fact, found that most reef fishes were carnivores and that carnivorous fish biomass was once 3–4 times greater than that of herbivorous fishes (Bakus, 1969; Goldman and Talbot, 1976; Parrish and Zimmerman, 1977; Grigg et al.,1984; Polunin, 1996). In addition, herbivorous fish biomass was usually much higher than plant biomass. Many reef consumers hide in structurally complex coral reefs to avoid predators and forage in nearby structurally simpler seagrass habitats (e.g., Randall, 1965; Ogden and Ehrlich, 1977; Ogden and Zieman, 1977; Zieman et al., 1984; Burke, 1995; McAfee and Morgan, 1996; Eggleston et al., 1998; Overholtzer and Motta, 1999). To date the importance of seagrass derived subsidies in determining the productivity of coral reef ecosystems remains unstudied (Randall, 1965). SUMMARY Seagrasses often form extensive meadows along the coasts of every continent except Antarctica. As such, understanding the dynamics of food web interactions within these habitats, and the degree to which seagrass production is exported, is of considerable theoretical and practical importance. Yet, as noted above, our understanding of seagrass food webs and the flow of energy and nutrients among seagrass inhabitants, and their export to other habitats, lags far behind our understanding of such interactions in other marine habitats. In part, this is because no one seagrass habitat is representative of seagrass habitats as a whole. While vegetated habitats have received substantial study in some heavily

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populated areas (e.g., the Chesapeake Bay and eastern Australia), fewer investigations have been conducted in more remote regions (e.g., the offshore areas of the West Coast of Florida or tropical Australia). Moreover, seagrasses occur in salinities ranging from oligohaline to fully marine. As a result, the fauna of seagrass habitats (both consumers and their prey) can vary greatly from site to site and region to region. Further complicating things is the recognition that coastal food webs have been dramatically altered by both inadequately managed coastal development and intense fishing pressure, leaving us to speculate as to how prehistoric seagrass food webs might have once been constructed. If we are correct, it will be necessary to develop a broader perspective that recognizes that both producer and consumer assemblages vary greatly among locations and that these differences are bound to alter the relative importance of the grazing and detrital pathways within seagrass habitats. Additionally, more studies of the connectivity between marine habitats should lead to a better estimate of the role of seagrass producers in supporting consumers in other habitats. ACKNOWLEDGMENTS This work was supported by the DISPro program, a joint program between the Environmental Protection Agency’s EMAP program and the National Park Service (Grant No. 2350-7-0882), and by the University of North Carolina at Wilmington National Undersea Research Center (UNCW #9537). MESC Contribution Number: 328

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