Reef Fish Mass Mortality Event in an Isolated Island Off Brazil, with Notes

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Marine Biodiversity Records, page 1 of 4. # Marine Biological Association of the United Kingdom, 2010 doi:10.1017/S1755267210000424; Vol. 3; e47; 2010 Published online Reef ﬁsh mass mortality event in an isolated island off Brazil, with notes on recent similar events at Ascension, St Helena and Maldives hudson t. pinheiro, joa~o l. gasparini and jean-christophe joyeux Departamento de Oceanograﬁa e Ecologia, Universidade Federal do Espı´rito Santo, Avenida F. Ferrari, 514, Goiabeiras, Vito´ria, ES, Brazil, 29075-910

Events of mass mortality of marine ﬁsh have been reported to occur world wide, mainly in coastal regions of continental shelves. Here we report an event at Trindade Island, located 1160 km from the Brazilian coast. Melichthys niger was the species most commonly seen affected. Twenty-four other species were found washed ashore. Victims were demersal (72% of species), pelagic (20%) and benthonic species (8%), comprising eight trophic categories. There is evidence that ﬁsh kills have occurred at Trindade since at least the 1990s. Mortality events mainly involving primarily Balistidae (Trindade, Maldives and Ascension), Chaetodontidae (St Helena) and Serranidae (Ascension) have been reported for other isolated oceanic localities with low human occupation. It is possible that blooms of toxic algae, under certain conditions cause cascad- ing intoxication along the trophic web. A second hypothesis is that seasonal upwelling events of anoxic or hypoxic waters may be implicated.

Keywords: ﬁsh kill, dead zone, Trindade Island, southern Atlantic, Balistidae

Submitted 21 July 2009; accepted 17 March 2010

Events of mass mortality of marine fish have been reported to long), was about 1.2 stranded M. niger per linear metre of occur world wide and have been frequently linked to rapid beach. and large changes in temperature (Hsieh et al., 2008), Twenty-four other species were found washed ashore, with passage of freshwater masses or fluxes (caused by excess rain- Holocentrus adscensionis, Myripristis jacobus, Rypticus sapo- fall and near river mouths; Siung-Chang & Lum-Kong, 2001), naceus, Heteropriacanthus cruentatus, Diplodus argenteus, toxic algal blooms (Horner et al., 1997) and contamination by Kyphosus sectatrix, Canthidermis sufflamen, Cantherhines resuspension of anoxic–hypoxic or toxic sediment (Justic´ macrocerus and Diodon holocanthus being the most abundant et al., 1996). Most such reports have described mortality (Table 1). The event involved demersal (72% of species), events occurring in coastal regions of continental shelves pelagic (20%) and benthonic species (8%), comprising eight and nearby offshore islands. trophic categories (mobile invertebrate feeders, piscivores, Here we report an event of reef fish mass mortality in an planktivores, roving herbivores, territorial herbivores, omni- isolated marine environment (Figure 1), Trindade Island, vores, sessile invertebrate feeders and carnivores). There is located 1160 km from the Brazilian coast. The event was evidence (personal communications and photographs) that recorded during a scientific expedition, between 28 February fish kills have occurred periodically since at least the 1990s. and 26 April 2007. Observations were carried out daily (Permanent occupation of the island by a small contin- while monitoring the breeding activity of Chelonia mydas gent—about 30 people—was established in 1957 by the (Linnaeus, 1758) at seven beaches (TAMAR Project). The Brazilian Navy; there is no other human settlement on the fish mortality had commenced before the start of the island; Gasparini, 2004.) expedition and persisted for about two weeks until 14 Recent events of fish mass mortality have been reported for March. Melichthys niger was the species most commonly other oceanic, oligotrophic localities in the central Atlantic seen affected. It also is the most abundant fish of the coastal and elsewhere. Several such kills have affected the central zone of the island (Gasparini & Floeter, 2001). During this atolls of the Maldives in 2007 (Naeem & Sattar, 2007; period, moribund individuals were commonly seen close to Shiham Adam, Marine Research Centre of Maldives, personal the surface and numerous fish were found stranded on communication). Kills occurred between July and December beaches and rocky shores (Figure 1). Density, estimated and there were no obvious signs of algal bloom but for from one census carried out on 7 March at three beaches a single incident in July at Meemu Atoll in which victims (Tuńel, Tartarugas and Andradas, totalling about 1550 m were mostly surgeonfish and parrotfish. Several November kills at the nearby atolls Vaavu, Baa and South Ari Atolls affected mostly the Balistidae Odonus niger (Ru¨ppell, 1836).

Corresponding author: While over 30 taxa were identiﬁed, large-bodied reef food H.T. Pinheiro ﬁsh were rarely encountered and Odonus niger accounted Email: [email protected] for 91–97% of individuals depending on the atoll; the

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family Balistidae summed up to 96–99% of all fish. Three dead O. niger from Vaavu Atoll tested positive for Staphyloccocus bacteria but this result was deemed inconclu- sive due to the absence of a control test on healthy specimens (Naeem & Sattar, 2007). In early March–late April 2006, tens of thousands of cun- ningfish, Chaetodon santaehelenae Gu¨nther, 1868, died all along the coast of St Helena (Emma Bennett and Gerald Benjamin, Directorate of Fisheries, Agricultural and Natural Resources Department, Government of St Helena, personal communication). A census conducted on 26 March, at the peak of the six-week course of the event, along 10.5 km of the leeward coast of the island between James Bay to near Cat Island listed more than 16.5 thousand dead juveniles, 11 near adults, 7 adults and 3 fish belonging to two other species floating close to shore. Overall, the kill affected thir- teen species. The endemic and endangered butterflyfish is nor- mally very abundant throughout the year and, in absence of any sign that could indicate a specific cause, it was concluded at the time that the kill must have been caused by ‘over population’. Kills involving Epinephelus adscensionis (Osbeck, 1765) and Melichthys niger have occurred repeatedly at Ascension (Olivia Renshaw and Stedson Stroud, Conservation Department, Ascension Island Government, Ascension Island, personal communication). Episodes for which details were recorded extended one (mid-August to mid-September 2007, at Turtleshell, Deadman’s and Long Beaches and English Bay) to several months (early December 2007 to late May 2008 at south-east, north-east and Crystal Bays, Purpoise Point and Stack 8 area). They resulted in the stranding of hundreds of juvenile and adult groupers (2007 and 2008) and thousands of triggerfish (in 2008 and, also, in 2009). Other species were little affected albeit 2200 fry of Trachinotus ovatus (Linnaeus, 1758) were reported in mid-2007. Events coincidental to fishkills were brown and green algae washed ashore (September 2007), heavy rains and an offshore earthquake one to two Fig. 1. Trindade Island, Brazil (A) and fish mass mortality event in the island weeks before (December 2007) and a ‘brown scum’ associated (B) showing dead Melichthys niger (photographs by H. Pinheiro and P. Welff, to a ,10 individual stranding in January 2008. respectively).

Table 1. Fish species involved in mortality events in Trindade Island. The trophic category, main habitat and stranding frequency are indicated. N/A, not applicable.

Species Trophic category Habitat Stranding frequency

Holocentridae Holocentrus adscensionis (Osbeck, 1765) MIF D VC Myripristis jacobus Cuvier, 1829 PL D C Plectrypops retrospinis (Guichenot, 1853)∗ MIF D N/A Holocentridae unidentiﬁed D C Serranidae Cephalopholis fulva (Linnaeus, 1758)∗ CA D N/A Mycteroperca venenosa (Linnaeus, 1758)∗ CA D N/A Rypticus saponaceus (Bloch & Schneider, 1801) CA B C Priacanthidae Heteropriacanthus cruentatus (Lacepe`de, 1801) MIF D C Carangidae Decapterus macarellus (Valenciennes, 1833) PL P R Caranx latus Agassiz, 1829 PI P R Sparidae Diplodus argenteus (Valenciennes, 1830) O D C

Continued reef fish mortality event at trindade island 3

Table 1. Continued

Species Trophic category Habitat Stranding frequency

Kyphosidae Kyphosus sectatrix (Linnaeus, 1758) RH P C Chaetodontidae Chaetodon striatus Linnaeus, 1758 SIF D R Prognathodes brasiliensis Burgess, 2001∗ SIF D N/A Pomacanthidae Holacanthus tricolor (Bloch, 1795) SIF D R Pomacentridae Microsphatodon chrysurus (Cuvier, 1830) TH B R Scaridae Sparisoma amplum (Ranzani, 1841)∗ RH D N/A Acanthuridae Acanthurus bahianus Castelnau, 1855 RH D R Balistidae Canthidermis sufﬂamen (Mitchill, 1815) O P C Melichthys niger (Bloch, 1786) O P VC Monacanthidae Cantherhines pullus (Ranzani, 1842) O D R Cantherhines macrocerus (Hollard, 1854) O D C Ostraciidae Acanthostracion quadricornis (Linnaeus, 1758) O D R Diodontidae Diodon holocanthus (Linnaeus, 1758) MIF D C Diodon hystrix (Linnaeus, 1758) MIF D R

Trophic categories: MIF, mobile invertebrate feeders; PI, piscivores; PL, planctivores; RH, roving herbivores; TH, territorial herbivores; O, omnivores; SIF, sessile invertebrate feeders; CA, carnivores. Habitat: D, demersal; B, benthonic; P, pelagic. Stranding frequency: VC, very common (new strandings sighted daily, hundreds to thousands seen during the expedition); C, common (new strandings sighted on occasion, ten to one hundred seen); R, rare (new strandings sighted rarely or not sighted, less than ten seen). ∗, photographic records from previous expeditions.

In regards to the event at Trindade, it is possible that Renshaw and Stedson Stroud for the invaluable information blooms of toxic algae, under certain conditions, caused cas- they kindly provided on fishkills in the Maldives, St Helena cading intoxication along the trophic web. Toxic algae occur and Ascension. An anonymous referee offered suggestions in other Atlantic oceanic islands (Littler et al., 2006) and to improve the manuscript. H.T.P. and J.C.J. acknowledge there are reports of algal blooms occurring in remote areas financial support by CAPES and CNPq, respectively. that suffer low human impact (Burgess, 2006). A second hypothesis is that seasonal upwelling events of anoxic or hypoxic waters may be involved (the low oxygen content would be due to the resuspension of sediment and organic matter deposited at geological scales) often heavily loaded REFERENCES with hydrogen sulphide. Oxygen-poor waters of the Benguela upwelling have been reported to affect the south- Bakun A. (1990) Global climate change and intensification of coastal eastern Atlantic continental shelf (Mohrholz et al., 2008) ocean upwelling. Science 247, 198–201. and these waters, in years of strong Benguela upwelling, can Burgess S.C. (2006) Algal blooms on coral reefs with low anthropogenic even reach the Mid-Atlantic Ridge island of St Helena impact in the Great Barrier Reef. Coral Reefs 25, 390. (Feistel et al., 2003). There are some concerns that Feistel R., Ragen E. and Grant K. (2003) Climatic changes in the subtro- human-induced climate change is affecting oceanic circula- pical Southeast Atlantic: the St Helena Island Climate Index (1893– tion at global and regional scales and may lead to the expan- 1999). Progress in Oceanography 59, 321–337. sion of these ‘dead zones’ and alterations in the global pattern Gasparini J.L. (2004) Ilha da Trindade e Arquipe´lago Martin Vaz: Pedaços of upwelling (Bakun, 1990). de Vito´ria no azul atlaˆntico. Vito´ria: GSA. Gasparini J.L. and Floeter S.R. (2001) The shore fishes of Trindade Island, western South Atlantic. Journal of Natural History 35, 1639– ACKNOWLEDGEMENTS 1656. The authors thank TAMAR/ICMbio project team leaders Horner R.A., Garrison D.L. and Plumley F.G. (1997) Harmful algal Luciana Magnabosco and Antonio de Padua Almeida and blooms and red tide problems on the U.S west coast. Limnology and the researchers Dione Krise, Leandro Bugoni, Carlos Oceanography 42, 1076–1088. E. Stein and Pedro Welff. We also thank the logistic support Hsieh H.L., Hsien Y.-L., Jeng M.S., Tsai W.S., Su W.C. and Chen C.A. of the Brazilian Navy and Carlos E.L. Ferreira, Raphael (2008) Tropical fishes killed by the cold. Coral Reefs 27, 599. Macieira, Luiz Rocha, Alasdair Edwards and Tara Pelembe Justic´ D., Rabalais N.N. and Turner R.E. (1996) Effects of climate change for their comments and information. We are especially grate- on hypoxia in coastal waters: a doubled CO2 scenario for the northern ful to Shiham Adam, Emma Bennett, Gerald Benjamin, Olivia Gulf of Mexico. Limnology and Oceanography 41, 992–1003. 4hudsont.pinheiroet al.

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