Friday, May 6, 2016

Groupers Threatened Globally, by Don Orth

Groupers are in big trouble.  What is a grouper?  Grouper is a common name given to fishes in the tribe Epinephelini (Family Serranidae: subfamily Epinephelinae).  In other parts of the world, groupers are cabrillas, garropas, gropers, lapu-lapu, pugapo, hapuku, or hammour.   The name, grouper, is believed to derive from the Portugese, garoupa. There are fifteen genera of groupers, the most diverse being Epinephelus with 87 species and Mycteroperca with 15 species.  All groupers are large fish with a stout body, large head, and large mouth. The body form allows them to act as rover predators or ambush predators.  The large mouth has impressive suction volume and, hence, the grouper usually swallows a single large prey whole. These superbly adapted fishes, however, are threatened with extinction throughout the world and action is needed to begin a long recovery.

Groupers are a biologically diverse group of reef fishes and at least 35 different species are harvested around the world.  They typically support small-scale, localized commercial and recreational fisheries. The flesh is a firm, lean white meat with large flake and a mild flavor that blends well with light seasoning or fresh herbs. Groupers are sold fresh in local seafood markets where they are often the highest priced fish. Catches of many groupers have declined and there is "no sign of any slowing down" of declines (Sadovy de Mitcheson et al. 2013).  In response to reduced grouper supplies, restaurants often serve some other, less expensive fish.  Some restaurants have even admitted to serving basa fish (Pangasius bocourti), labeled as "grouper's cousin."  It's a catfish, hardly a "cousin!" A handheld assay was developed to counter the extensive mislabeling of groupers (Ulrich et al. 2015).   There is no question that fishing is the major factor driving stocks on the downward spiral, but the several characteristics of their habitat use and life history make groupers particularly vulnerable.

Color phases of black grouper Mycteroperca bonaci in Belize, including (A) blotched, (B) light, (C) dark, and (D) white-headed.  source: Paz et al. 2007.
Groupers are long-lived, late maturing fishes that rely on coral reefs to provide shelter and abundant food.  They exceed 1 m in length as adults and, as opportunistic predators, they moderate the abundance of multiple prey species.  Many, but not all, groupers are sequential hermaphrodites and are born female and transition to males later.  Consequently, the sex ratio is skewed in favor of females. Theories on sex change in groupers will be a subject for a later post. Large males maintain territories on the reef and may have a harem of multiple female mates.  Young groupers typically have a different color pattern and occupy different habitats than adult groupers.  Adult groupers have multiple color patterns to communicate mating readiness (see color phases in photo).
 
Young color phase of the Giant Grouper Epinephelus lanceolatus  By © Citron  source
Why are so many groupers threatened with extinction?   One fourth of all grouper species are either near threatened or at risk of extinction if current trends continue (Sadovy de Mitcheson et al. 2013).  Many more species (33%) are data deficient, which makes assessment of fisheries status and extinction risk impossible and management interventions unlikely (Luiz et al. 2016).  Several aspects of the life history of groupers helps to explain the prevalence of overharvest.
 
Grouper Head On  Photo by Craig O'Neal.  Source

First, adult and juvenile groupers often use very different habitats and in many cases ecosystems that support juveniles and adults are threatened from human modification.  Coral reefs throughout the world are changing due to climate change, ocean acidification and coral bleaching (Arundsen et al. 2003).  Coral reef fish declines directly limit the food base for adult groupers.   Eggs and larval groupers are pelagic and are transported via currents to juvenile habitats.  Juveniles often settle in different shallow water habitats.   The juvenile habitats are essential to maintain steady recruitment of new adults to the coral reefs.  However, these shallow water habitats are often degraded or transformed to less productive habitats.   

Kite-shaped Epinephelus larvae. Photo courtesy National Marine Fisheries Service source
The Goliath Grouper Epinephelus itajara is the largest grouper in the Atlantic Ocean and one of the two largest species of groupers in the world, exceeding 2 m (6 feet) in total length. Florida is the only place in the world where Goliath Groupers can be found on a regular basis throughout the year, and in their spawning aggregation sites in late summer.  Although we fish for Goliath Grouper near reefs and structures, the species is mangrove-dependent, and shows a distinct size-related habitat shift. Juvenile goliaths (up to 1.1 m or 3 feet in total length) are found exclusively in spatially complex, fringing red mangrove (Rhizophora mangle) shorelines (Frias-Torres 2006).  The mangrove forests support high diversity of fish and invertebrates and are threatened  worldwide.  Mangroves create a narrow fringe habitat between land and sea, between latitudes 25ºN and 30ºS.  Since 1980, at least 35% of mangrove forests were lost (Valiela et al.  2001).  

During spawning the groupers aggregate at specific spawning locations. Here they are vulnerable to overexploitation. Especially where large aggregations exist, large grouper may be quickly reduced in abundance; the first fisherman to find the aggregations hit the bonanza and can’t reel them in fast enough.  Their gears are fully saturated.  It’s a phenomenon that fisheries professionals have named hyperstability  (Erisman et al. 2011). Because fisherman can’t catch them fast enough, the catch per unit effort remains high even as populations plummet.  In the case of the Nassau Grouper Epinephelus striatus, declines were first noticed when spawners failed to show at historical spawning aggregation sites (Coleman et al. 1996; Aguilar-Perera et al. 2014).   
Hyperstable relationship between catch per unit effort (cpue) and population size (N)  (Erisman et al. 2011).
Groupers are extremely vulnerable to overfishing due to a combination of life history traits that include slow growth, long life (exceeding 4 decades), late sexual maturity (up to 8 years), and strong site fidelity. Males are usually larger, older and less numerous than females.  Capture fisheries are biased toward large adults.  The larger species of groupers that also had smaller geographic ranges were most likely to be endangered or critically endangered (Luiz et al. 2016).
Photographs from the 'Gulf Stream' charter boat on (A) 14 April 1957,
(B) 9 March 1958, and (C, D) between 1965 and 1979 Source: McClenachan 2009.
Another new development that particularly threatens the groupers is the live reef food fish trade (LRFFT).  LRFFT involves the capture of reef fish that are kept alive for sale and consumption as a luxury food item, primarily in the coral triangle region.  Some small groupers are raised in cages (Pierre et al. 2008).   However, this form of mariculture depends on harvest of juvenile groupers as seed stock and the resulting fisheries are likely to be unsustainable (To and Sadovy de Mitcheson 2009).  The unfortunate reality for the groupers is that the demand for live groupers for international trade far outstrips the sustainable supply (Sadovy et al. 2003).
 
Gag Grouper  Photo by Dean Kimberly  source
One allure of the grouper is the massive size reached by some species. The Giant Grouper (Epinephelus lanceolatus) grows up to 2.7 m (8.9 ft) in length and 400 kg (880 lb) in weight.   The larger grouper species are more likely to be threatened or critically endangered (Ruiz et al. 2016).       
 
Atlantic Goliath Grouper  Photo by Brett Seymour -  source   
In November 2013, a 310-kg (686-lb) grouper had been caught and sold to a hotel in Dongyuan, China.  The largest grouper ever caught and certified by IGFA was a 680 pound Atlantic Goliath Grouper Epinephelus itajara.   The Goliath Grouper has been severely overfished throughout its range and a fishing moratorium has been in place since 1990 (McClenachan 2009).
Largest Goliath Grouper  source
The extreme size alone, adds to the interest and pressure by fisherman. In fact, the sport anglers in Florida want the current harvest moratorium on Goliath Grouper lifted. Fisherman are willing to pay between $34 and $79 for a single harvest permit (Shideler et al. 2015).
Nassau Grouper  Photo by Dean Kimberly  source
The story of the grouper is similar in all regions where they exist.  Fish are quickly overharvested and fishers move from aggregation to aggregation until the grouper population is unable to recover.  The efforts to recover Goliath Grouper and Nassau Grouper are longterm efforts that benefit from recent studies of population structure (Jackson et al. 2014).  For more background on the Nassau Grouper efforts, view the Groupers Last Stand.  The lessons from management of groupers indicates that recovery will not be quick nor easy.   Length or creel limits are often ineffective if fish are released with barotrauma after deepwater capture.  Successful efforts will most likely rely on community based management and adoption of principles from Ostrom's Governing the Commons, so that local knowledge is incorporated to match rules to local conditions and customs and community members monitor users and enforce the sanctions.  Other local management interventions may include bans on sale of grouper during reproductive seasons, wise implementation of marine protected areas, shift to grouper tourism via SCUBA diving (Rudd and Tupper 2002), and adopting international standards for the trade in international live reef food fish.  Protective management actions will take decades to evaluate because of the long time to maturity and long recovery times for groupers.  Consequently, a precautionary approach to harvest management is advisable for the many data-deficient species of groupers.

References
Aronson, R.B., et al.  2003. Causes of coral reef degradation. Science 302(5650)1502-1504.
Coleman, F.C., C. C. Koenig, and L.A. Collins.  1996.  Reproductive styles of shallow-water groupers (Pisces: Serranidae) in the eastern Gulf of Mexico and the consequences of fishing spawning aggregations. Environmental Biology of Fishes 47(2)129-141.
Erisman, B.E., L.G. Allen, J.T. Claisse, D.J. Pondella II, E.F. Miller, and J.H. Murray.  2011. The illusion of plenty: hyperstability masks collapses in two recreational fisheries that target fish spawning aggregations. Canadian Journal of Aquatic Sciences 68:1705–1716.
Frias-Torres, S. 2006.  Habitat use of juvenile goliath grouper Epinephelus itajara in the Florida Keys, USA. Endangered Species Research 2:1-6.  
Jackson, A.M., B.X. Semmens, Y. Sadovy de Mitcheson, R.S. Nemeth, S.A. Heppell, P.G. Bush, A. Aguilar-Perera, J.A.B. Claydon, M.C. Calosso, K.S. Sealey, M.T. Schärer, G. Bernardi. 2014. Population structure and phylogeography in Nassau Grouper (Epinephelus striatus), a mass-aggregating marine fish. PLoS ONE. DOI: 10.1371/journal.pone.0097508
Luiz et al 2016. Predicting IUCN Extinction Risk Categories for the World’s Data Deficient Groupers (Teleostei: Epinephelidae) Conservation Letters. doi: 10.1111/conl.12230
McClenachan, L. 2009. Historical declines of goliath grouper populations in south Florida, USA.  Endangered Species Research 7:175-181. 
Paz, G., and G.R. Sedberry. 2007. Identifying black grouper (Mycteroperca bonaci) spawning aggregations off Belize: conservation and management. Proceedings of the 60th Gulf and Caribbean Institute. Punta Cana, Dominican Republic.  577-584
Pierre, S., S. Gaillard, N. Prevot.  2008.  Grouper aquaculture: Asian success andMediterranean trials. Aquatic Conservation Marine and Freshwater Ecosystems 18(3):297-308. 
Rudd, M.A., and M.H. Tupper. 2002.  The impact of Nassau grouper size and abundance on scuba diver site selection and MPA economics.  Coastal Economics 30:133-151.
Sadovy, Y.J., T.J. Donaldson, T.R. Graham, F. McGilvray, G. Muldoon, M. Phillips, and M. Rimmer. 2003. While Stocks Last: The Live Reef Food Fish Trade.  Asian Development Bank, Manila. 
Sadovy, Y. and Domeier, M.  2005. Are aggregation fisheries sustainable: reef fish fisheries as a case study. Coral Reefs 24, 254–262.
Sadovy de Mitcheson,  Y., M.T. Craig, A. A . Bertoncini, K.E. Carpenter, W. W.L. Cheung, J.H. Choat, A.S. Cornish, S.T. Fennessy, B.P. Ferreira, P. C. Heemstra, M. Liu, R.F. Myers, D.A. Pollard, K. L. Rhodes, L.A. Rocha, B. C. Russell, M. A. Samoilys, and J. Sanciangco. 2013. Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish and Fisheries 14:119-136. DOI: 10.1111/j.1467-2979.2011.00455.x
Shideler, G.S., D.W. Carter, C. Liese, and J. E. Seafy. 2015.  Lifting the goliath grouper ban: angler perspectives and willingness to pay.  Fisheries Research   161:156-165.
To, A.W.L. and Y.J. Sadovy de Mitcheson. 2009. Shrinking baseline: the growth in juvenile fisheries, with the Hong Kong grouper fishery as a case study. Fish and Fisheries 10, 396–407.
Ulrich, R.M., D.E. John, G.W. Barton, G.S. Hendrick, D.P. Fries, and J.H. Paul. 2015.  A handheld sensor assay for the identification of grouper as a safeguard against seafood mislabeling fraud. Food Control 53:81-90.
Valiela, I., J.L. Bowen, and J.K.York. 2001.  Mangrove forests: one of the world’s threatened major tropical environments. BioScience 51(10):807-815.

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