Fishing Down a Caribbean Food Web Relaxes Trophic Cascades
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Vol. 445: 13–24, 2012 MARINE ECOLOGY PROGRESS SERIES Published January 20 doi: 10.3354/meps09450 Mar Ecol Prog Ser Fishing down a Caribbean food web relaxes trophic cascades Peter J. Mumby1,*, Robert S. Steneck2, Alasdair J. Edwards3, Renata Ferrari1, Robin Coleman4, Alastair R. Harborne1,5, Janet P. Gibson4 1Marine Spatial Ecology Lab, School of Biological Sciences & ARC Centre of Excellence for Coral Reef Studies, Goddard Building, University of Queensland, St. Lucia Campus, Brisbane, Queensland 4072, Australia 2School of Marine Sciences, University of Maine, Darling Marine Center, Walpole, Maine 04573, USA 3School of Biology, Newcastle University, Ridley Bldg, Newcastle upon Tyne NE1 7RU, UK 4Wildlife Conservation Society, PO Box 768, 1755 Coney Drive, 2nd Floor, Belize City, Belize 5Marine Spatial Ecology Lab, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4PS, UK ABSTRACT: The fishing down of marine food webs has been described in pelagic and demersal sys- tems but rarely documented in coral reef environments. We recorded a rapid shift in fish community structure in Belize that accompanied a marked decline in grouper and snapper abundance and a switch towards smaller, less desirable, herbivorous parrotfishes. In a 6 to 7 yr period (2002–2008/09), observations of large-bodied grouper (Serranidae) declined significantly from an encounter proba- bility of 21% per 200 m2 transect to just 2%. The biomass of carnivorous snappers (Lutjanidae) underwent a 7-fold decline, primarily in the species Ocyurus chrysurus. During this period, the inclusion of parrotfish in fish catches at nearby Glover’s Atoll increased from a frequency of 6% in 2004 to ~20% of speared individuals by 2008. Parrotfish biomass declined by 41% between 2002 and 2008/09, with a major decline in the large and dominant herbivore Sparisoma viride. No changes in parrotfish biomass were detectable in nearby marine reserves during this time. Several important indirect effects of fishing were observed. The biomass of mesopredators including Cephalopholis fulvus, C. cruentatus, and Epinephelus guttatus increased dramatically by 880% as compared to the 2002 levels. We putatively attribute this response to a release from predation and constraints to foraging behaviour imposed by large serranids. Further, we find that the density of adult damselfish of the species Stegastes planifrons and S. partitus decreased by ~45%. We attribute this decline to elevated predation by the increased densities of mesopredators, which have been shown to prey upon juvenile damselfish. No change in damselfish densities was found at 2 con- trol locations where fishing was prohibited. The decline in parrotfish in the central Mesoamerican barrier reef likely accounts for recent anecdotal observations of Halimeda tuna spreading to micro- habitats that have previously been grazed intensively. While these results imply that the resilience of these reefs may be seriously impaired, the Belize Government has recently enacted new legisla- tion to improve the management of grouper and outlaw harvesting of most herbivorous fish. KEY WORDS: Fishing · Coral reef · Parrotfish · Grouper · Snapper · Damselfish · Trophic cascade Resale or republication not permitted without written consent of the publisher INTRODUCTION higher trophic levels, such as large piscivores, are de - pleted first. As they become rare, the fishery progres- The phenomenon of ‘fishing down marine food sively depletes species at lower trophic levels over webs’ (Pauly et al. 1998) is well established in both time. Exploitation of successively lower trophic pelagic and demersal finfish fisheries. Species at groups can occur for 2 reasons, and both apply to *Email: [email protected] © Inter-Research 2012 · www.int-res.com 14 Mar Ecol Prog Ser 445: 13–24, 2012 many fisheries. The life history traits of species at peatable observation to date is a general lack of sup- high trophic levels, such as gaining maturity at a port for numerical increases in prey species once relatively large body size and late age, render their their piscivore predators have been heavily depleted populations highly vulnerable to fishing mortality by fishing. Examples of weak or undetectable rela- (reviewed in Jennings & Kaiser 1998, Cheung et al. tionships stem from Hawaii (Friedlander & DeMartini 2007). Species at high trophic levels may also be pref- 2002), the Seychelles (Jennings et al. 1995), Fiji (Jen- erentially targeted because of high consumer de - nings & Polunin 1997), the Bahamas (Mumby et al. mand (McManus 1997, Coleman et al. 2000). This is 2006), the Philippines (Russ 1985), and the Pacific particularly true of many coral reef systems where Line Islands (Sandin et al. 2008). large groupers (Serranidae) are preferentially tar- Here, we describe the remarkable change in fish geted (Russ 1991, Sadovy 2005). communities that occurred after a 7 yr period of fish- Despite the great cultural and economic role of fish- ing in Belize, Central America (2002–2008/09). The ing in coral reef environments, there have been few low human population density of Belize (13 people documented cases of ‘fishing down coral reef food km−2), together with the large size of its barrier reef webs’. The paucity of such studies largely reflects the system (~250 km in length), has meant that reefs long history of fish exploitation (Jackson et al. 2001) were considered to be relatively lightly fished com- such that many systems had already been heavily de - pared to many other parts of the Caribbean (Hay pleted by the time that reef fish monitoring emerged 1984, Pandolfi et al. 2003). Indeed, at the start of the in the 1960s. Some important exceptions exist includ- study (2002) the fishery for finfish focused mostly on ing detailed accounts of fish responses to the opening lutjanids and serranids (Koslow et al. 1994, Paz & and closure of fisheries in the Philippines (Russ & Truly 2007) and the exploitation of herbivorous par- Alcala 1998b), long time-series of data from the US rotfishes was uncommon and confined to subsistence Virgin Islands (Friedlander & Beets 2008) and the uses. However, our study captures a critical change Florida Keys (Ault et al. 1998), and a comparison of in the fishery during which larger, desirable species fish communities in Jamaica over a relatively long underwent a marked decline and fishers literally time interval from 1969 to 1986 (Koslow et al. 1988). began fishing down the food chain. We document the Nonetheless, much more is known about the recov- changes that have occurred in the fish communities ery of fish after the establishment of no-take reserves over time and provide correlative evidence of trophic (Roberts 1995, Russ & Alcala 1998a, McClana han & cascades, which imply that some important prey spe- Graham 2005), than the rates of declining species cies can exhibit a numerical increase once released abundance during an active fishery. from predation. In our case, the trophic cascade is tri- Given the difficulty of following the fate of a fishery trophic involving large predators (large-bodied over time, many important insights into the effects of grouper), mesopredators (small-bodied groupers), harvesting on fish communities have compared fish and damselfishes (Pomacentridae). Thus, our study communities along a gradient of human impact (Jen- de scribes the striking changes in fish communities nings & Polunin 1995, Friedlander & DeMartini 2002, that can occur through direct and indirect effects of Newman et al. 2006, Harborne et al. 2008). Of partic- fishing over a short, 7 yr period during which a prior- ular ecological interest is whether human activities ity fish group, grouper, became scarce, prompting a cause cascading impacts on community structure switch in target species. over at least 3 trophic levels (Pinnegar et al. 2000, Micheli et al. 2004, Estes et al. 2011). However, de - tecting trophic cascades, or even evidence of a single MATERIALS AND METHODS trophic interaction such as the release of prey when a predator is depleted, is a formidable challenge, in Study sites and census dates part because of the plethora of factors that influence species’ abundance (Steneck 1998). The majority of this study was carried out within It would be difficult to identify any truly global the boundaries of the South Water Caye Marine expectations for trophic cascades on coral reefs. Reserve (hereafter simply referred to as South Water Although relevant studies have been carried out in Caye). The reserve was officially announced in 1996 all 3 tropical oceans, differences in species diversity, but the fully protected area or Conservation Zones species identity, local environmental conditions, and were not fully established until 2009. South Water the intensity of exploitation all potentially confound Caye lies in the central part of the Belize Barrier Reef syntheses of multiple studies. Perhaps the most re - and 6 sites were located on the outer forereef at a Mumby et al.: Fishing down a Caribbean foodweb 15 depth of 10 to 13 m, and ranged from Tobacco Reef in Water Caye (Mumby et al. 2005). Both sites at the north to 5 km south of South Water Caye itself Glover’s were located in the reserve, which is en - (Fig. 1). While all sites at South Water Caye lie within forced. Fisheries catch outside the boundaries of the reserve boundaries, our sampling pre-dates the ces- reserve at Glover’s has been sampled since 2004 and sation of fishing at sites within the reserve, and there- these data were used to provide a context for the fish- fore our data from South Water Caye can be thought ery at our prime study sites at South Water Caye. of as representing the effects of continued fishing. To Fishing impacts were determined using a binary contrast the effects of fishing, 2 additional sites (C1 approach that distinguished the study ‘start’ in June and C2) were located at Glover’s Reef, which is an 2002 and ‘end’ in 2008/09. Surveys of study ‘end’ offshore atoll located directly east of South Water were taken over a period of ~1 yr, from March 2008 to Caye.