Coral Reefs (2005) 24: 209–213 DOI 10.1007/s00338-004-0468-9 PERSPECTIVE NOTE John F. Valentine Æ Kenneth L. Heck Jr Perspective review of the impacts of overfishing on coral reef food web linkages Received: 20 August 2002 / Accepted: 15 November 2004 / Published online: 13 May 2005 Ó Springer-Verlag 2005 Keywords Conservation Æ Habitat linkages Æ Marine rous and herbivorous fishes, coupled with the die-off of reserves Æ Predation herbivorous sea urchins, is thought to be responsible for widespread macroalgal overgrowth of coral reefs in Jamaica (Hughes 1994 but see Aronson and Precht 2001). Introduction Given that the dramatic impacts of fishing on marine food webs preceded the development of most theory in Overfishing is increasingly understood to result in indi- marine ecology, it is understandable that management rect alterations of habitat structure and function agencies have predominantly focused their efforts on the (McClanahan et al. 1995; Bowen 1997; Jackson 2001; role of bottom-up processes (nutrient concentration) in Jackson et al. 2001; Gardner et al. 2003). The intense regulating the productivity of coastal ecosystems. But harvesting of sea otters from kelp forests, for example, given the increasing evidence that food web alterations created ‘‘low- predation refuges’’ for their sea urchin have figured prominently in the collapse of marine prey. Following otter removal, sea urchin grazing ex- ecosystems, it seems clear that new studies are urgently ploded resulting in large regional losses of kelp (Estes needed to assess the degree to which large-scale food and Palmisano 1974; Duggins 1980). Further support web alterations have changed the structure and function for the impacts of large consumers was found in Alaskan of marine ecosystems (Estes and Peterson 2000; Jackson embayments where inshore migration of killer whales 2001; Pandolfi et al. 2003). changed the strength of interactions between sea otters and their herbivorous sea urchin prey, again resulting in local losses of kelp forests (Estes et al. 1998). Similarly, Habitat linkages: has overfishing altered the strength McClanahan et al. (1995) found that intense harvesting of trophic transfers among habitats? of predatory trigger fishes promoted large-scale habitat changes as their sea urchin prey, once released from The passive and active transport of materials (via currents predation, increased. More urchins subsequently led to or foraging migrations, respectively) link communities more coral reef erosion and the eventual replacement of across distinct habitat boundaries. Passive movements of corals by seagrasses (McClanahan and Kurtis 1991). nutrients, detritus, and prey between habitats (also called Moreover, the intense harvesting of both large piscivo- spatial subsidies or cross-habitat exchanges) can have major ‘bottom-up’ effects on food web productivity, especially in places with little or no in situ primary pro- Communicated by Biological Editor R.C. Carpenter duction [e.g., caves, mountaintops, stream banks, central J. F. Valentine Æ K. L. Heck Jr ocean gyres, and the deep sea (Vetter 1994, 1995, 1998; Dauphin Island Sea Lab, Polis and Hurd 1996; Polis and Strong 1996; Persson et al. 101 Bienville Boulevard, Dauphin Island, 1996; Harrold et al. 1998; Rose and Polis 1998; Hilder- AL 36528-0369, USA brand et al. 1999)]. Such trophic links between terrestrial J. F. Valentine (&) Æ K. L. Heck Jr and freshwater habitats and between marine and terres- Department of Marine Science, trial habitats are commonplace (Polis and Hurd 1996; University of South Alabama, Mobile, Polis and Strong 1996; Fagan et al. 1999; Nakano and AL 36688-0002, USA E-mail: [email protected] Murakami 2001). These subsidies of food and nutrients Tel.: +1-251-8617546 sustain greater densities of large predators than could Fax: +1-251-8617540 otherwise exist if feeding was limited to prey produced in 210 a single habitat (Moore 1998; Vetter 1998; Huxel and tions strongly point to an important transfer of seagrass McCann 1998; Rose and Polis 1998). meadow production to coral reef food webs. Great numbers of large consumers (e.g., groupers, It is noteworthy, however, that many of the existing snappers, tuna, sharks, and whales), so widely reported reports are from heavily fished areas, namely, the Virgin in the earlier literature (cf. Safina 1995, 1998; Parfit Islands and Jamaica (Ogden et al. 1973; Hay 1984; 1995; Dayton et al. 1995; Block et al. 2001), appear to Thayer et al. 1984; Hughes 1994; Greenway 1995). In have relied on the production of multiple habitats to such overfished areas, in the absence of higher order meet their nutritional needs. Where abundant, these consumers, lower order consumer biomass may have large consumers probably represented important vehi- increased to such a point that food has become limited cles for the transfer of energy and nutrients across for them and they are forced to forage in seagrass beds habitat boundaries. to obtain adequate food. In addition, the reduced risk of Early studies of coral reefs, for example, found that predation from overfished predators may allow lower most reef fishes were carnivores and that carnivorous order consumers to forage at will in nearby seagrass fish biomass was three to four times greater than that of habitats. herbivore biomass (Goldman and Talbot 1976; Parrish and Zimmerman 1977; Grigg et al. 1984; Polunin 1996), and that herbivorous fish biomass was usually much Marine reserves: opportunities for testing whether higher than plant biomass. Such an inverted biomass overfishing has altered trophic connections between pyramid suggests that cross-habitat exchanges of energy seagrass and coral reef habitats must have played a key role in sustaining large reef consumers. In fact, many ‘‘reef’’ consumers were ob- There is a critical need to rigorously assess the impacts served to hide in structurally complex coral reefs to of the human removal of large consumers on marine avoid predators, but foraged in nearby structurally ecosystem structure and function (USNSF 1998; John simple seagrass meadows (e.g., Randall 1965; Ogden and Heinz Center 1998). Most information about the im- Zieman 1977; Zieman et al. 1984; McAfee and Morgan pacts of higher order consumers on lower trophic levels 1996; but see Nagelkerken et al. 2000; Cocheret de la comes from experimental manipulations conducted at Morinie´re et al. 2003). Thus evidence suggests that coral the scale of one to tens of meters. Processes operating at reefs were once characterized by much greater cross- such small spatial scales often differ from those operat- habitat trophic exchanges than is reported in the current ing at larger spatial scales (Thrush et al. 1995; Carpenter literature (Ogden 1980; Valentine and Heck 1999). 1996; Crowder et al. 1997; Sih et al. 1998; Diehl et al. In some locations, fish and in some cases sea urchin, 2000; Estes and Peterson 2000). Thus, conclusions from grazing is so intense that unvegetated ‘halos’ are created small-scale experiments should not be extrapolated to a and maintained within seagrass meadows adjacent to larger scale without validation (Walters and Holling coral reefs (Randall 1965; Ogden and Zieman 1977; Hay 1990; Eberhardt and Thomas 1991; Menge 1992; Car- 1984; Carpenter 1986; McAfee and Morgan 1996). Not penter 1996). However, controlled manipulation of lar- all foraging in and on seagrasses is near coral reefs, ger consumers (e.g., a suitable cage size) conducted at an however. While many herbivorous fishes shelter on reefs ecologically meaningful spatial scale would likely in- at night, they commonly forage throughout seagrass volve unacceptable artifacts. habitats during the day (Randall 1965; Ogden and Instead, whole ecosystem manipulation (Carpenter Zieman 1977; Zieman et al. 1984; McAfee and Morgan 1996) is a rigorous way to test the hypothesis that the 1996). For example, Scarus guacamaia and S. coelestinus overharvesting of piscivores has altered the abundance are reported to move up to 500 m from the reef to of lower order consumers and the entire structure of feeding areas (Winn and Bardach 1960; Winn et al. food webs on many coral reefs. The whole-system 1964). Away from the reef, juvenile and smaller species experimental approach was pioneered in freshwater and of resident parrotfishes, those that are found in the diets terrestrial systems with distinct natural borders (NSF of many reef-resident predators, also feed heavily on 1998). While some predictions have been made about seagrasses and their epiphytes (Randall 1965; Ogden and the role of large marine consumers on lower trophic Zieman 1977; Handley 1984; McGlathery 1995; McAfee levels (e.g., Jackson 1997; Bowen 1997), based on the and Morgan 1996; Valentine and Heck 1999; Kirsch results from small-scale experiments, lessons derived et al. 2002). Once large enough, many species of par- from whole ecosystem manipulations of lake and forest rotfish abandon structurally simpler seagrass habitats food webs show that surprising results are likely to oc- for more complex coral reefs, where it is believed they cur. find protection from large piscivorous fishes (Ogden and The creation of replicated ‘no take’ zones around the Zieman 1977; Handley 1984; Carpenter 1986; Sweatman world effectively represents a whole ecosystem manipu- and Robertson 1994; Nagelkerken et al. 2001, 2002; lation in which enforcement of ‘no take’ regulations Cocheret de la Morinie` re et al. 2003). Similarly, reef- should allow the recovery of higher order consumers to resident lower order carnivores (e.g.,