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 cascading 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 occur world wide and have been frequently linked to rapid and large changes in temperature (Hsieh et al., 2008), passage of freshwater masses or fluxes (caused by excess rainfall and near river mouths; Siung-Chang & Lum-Kong, 2001), toxic algal blooms (Horner et al., 1997) and contamination by resuspension of anoxic –hypoxic or toxic sediment (Justic´ et al., 1996). Most such reports have described mortality events occurring in coastal regions of continental shelves and nearby offshore islands. Here we report an event of reef fish mass mortality in an isolated marine environment (Figure 1), Trindade Island, located 1160 km from the Brazilian coast. The event was recorded during a scientific expedition, between 28 February and 26 April 2007. Observations were carried out daily while monitoring the breeding activity of Chelonia mydas (Linnaeus, 1758) at seven beaches (TAMAR Project). The fish mortality had commenced before the start of the expedition and persisted for about two weeks until 14 March. Melichthys niger was the species most commonly seen affected. It also is the most abundant fish of the coastal zone of the island (Gasparini & Floeter, 2001). During this period, moribund individuals were commonly seen close to the surface and numerous fish were found stranded on beaches and rocky shores (Figure 1). Density, estimated from one census carried out on 7 March at three beaches (Tu´nel, Tartarugas and Andradas, totalling about 1550 m
Corresponding author: H.T. Pinheiro Email: htpinheiro@gmail.com
long), was about 1.2 stranded M. niger per linear metre of beach. Twenty-four other species were found washed ashore, with Holocentrus adscensionis, Myripristis jacobus, Rypticus saponaceus, Heteropriacanthus cruentatus, Diplodus argenteus, Kyphosus sectatrix, Canthidermis sufflamen, Cantherhines macrocerus and Diodon holocanthus being the most abundant (Table 1). The event involved demersal (72% of species), pelagic (20%) and benthonic species (8%), comprising eight trophic categories (mobile invertebrate feeders, piscivores, planktivores, roving herbivores, territorial herbivores, omnivores, sessile invertebrate feeders and carnivores). There is evidence (personal communications and photographs) that fish kills have occurred periodically since at least the 1990s. (Permanent occupation of the island by a small contingent—about 30 people—was established in 1957 by the Brazilian Navy; there is no other human settlement on the island; Gasparini, 2004.) Recent events of fish mass mortality have been reported for other oceanic, oligotrophic localities in the central Atlantic and elsewhere. Several such kills have affected the central atolls of the Maldives in 2007 (Naeem & Sattar, 2007; Shiham Adam, Marine Research Centre of Maldives, personal communication). Kills occurred between July and December and there were no obvious signs of algal bloom but for a single incident in July at Meemu Atoll in which victims 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). While over 30 taxa were identified, large-bodied reef food fish were rarely encountered and Odonus niger accounted for 91 –97% of individuals depending on the atoll; the 1
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Fig. 1. Trindade Island, Brazil (A) and fish mass mortality event in the island (B) showing dead Melichthys niger (photographs by H. Pinheiro and P. Welff, respectively).
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 inconclusive due to the absence of a control test on healthy specimens (Naeem & Sattar, 2007). In early March – late April 2006, tens of thousands of cunningfish, 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 thirteen species. The endemic and endangered butterflyfish is normally 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 weeks before (December 2007) and a ‘brown scum’ associated to a ,10 individual stranding in January 2008.
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 Holocentridae Holocentrus adscensionis (Osbeck, 1765) Myripristis jacobus Cuvier, 1829 Plectrypops retrospinis (Guichenot, 1853)∗ Holocentridae unidentified Serranidae Cephalopholis fulva (Linnaeus, 1758)∗ Mycteroperca venenosa (Linnaeus, 1758)∗ Rypticus saponaceus (Bloch & Schneider, 1801) Priacanthidae Heteropriacanthus cruentatus (Lacepe`de, 1801) Carangidae Decapterus macarellus (Valenciennes, 1833) Caranx latus Agassiz, 1829 Sparidae Diplodus argenteus (Valenciennes, 1830)
Trophic category
Habitat
Stranding frequency
MIF PL MIF
D D D D
VC C N/A C
CA CA CA
D D B
N/A N/A C
MIF
D
C
PL PI
P P
R R
O
D
C
Continued
reef fish mortality event at trindade island
Table 1. Continued Species Kyphosidae Kyphosus sectatrix (Linnaeus, 1758) Chaetodontidae Chaetodon striatus Linnaeus, 1758 Prognathodes brasiliensis Burgess, 2001∗ Pomacanthidae Holacanthus tricolor (Bloch, 1795) Pomacentridae Microsphatodon chrysurus (Cuvier, 1830) Scaridae Sparisoma amplum (Ranzani, 1841)∗ Acanthuridae Acanthurus bahianus Castelnau, 1855 Balistidae Canthidermis sufflamen (Mitchill, 1815) Melichthys niger (Bloch, 1786) Monacanthidae Cantherhines pullus (Ranzani, 1842) Cantherhines macrocerus (Hollard, 1854) Ostraciidae Acanthostracion quadricornis (Linnaeus, 1758) Diodontidae Diodon holocanthus (Linnaeus, 1758) Diodon hystrix (Linnaeus, 1758)
Trophic category
Habitat
Stranding frequency
RH
P
C
SIF SIF
D D
R N/A
SIF
D
R
TH
B
R
RH
D
N/A
RH
D
R
O O
P P
C VC
O O
D D
R C
O
D
R
MIF MIF
D D
C 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 blooms of toxic algae, under certain conditions, caused cascading intoxication along the trophic web. Toxic algae occur in other Atlantic oceanic islands (Littler et al., 2006) and there are reports of algal blooms occurring in remote areas 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 with hydrogen sulphide. Oxygen-poor waters of the Benguela upwelling have been reported to affect the southeastern Atlantic continental shelf (Mohrholz et al., 2008) and these waters, in years of strong Benguela upwelling, can even reach the Mid-Atlantic Ridge island of St Helena (Feistel et al., 2003). There are some concerns that human-induced climate change is affecting oceanic circulation at global and regional scales and may lead to the expansion of these ‘dead zones’ and alterations in the global pattern of upwelling (Bakun, 1990).
ACKNOWLEDGEMENTS
The authors thank TAMAR/ICMbio project team leaders Luciana Magnabosco and Antonio de Padua Almeida and the researchers Dione Krise, Leandro Bugoni, Carlos E. Stein and Pedro Welff. We also thank the logistic support of the Brazilian Navy and Carlos E.L. Ferreira, Raphael Macieira, Luiz Rocha, Alasdair Edwards and Tara Pelembe for their comments and information. We are especially grateful to Shiham Adam, Emma Bennett, Gerald Benjamin, Olivia
Renshaw and Stedson Stroud for the invaluable information they kindly provided on fishkills in the Maldives, St Helena and Ascension. An anonymous referee offered suggestions to improve the manuscript. H.T.P. and J.C.J. acknowledge financial support by CAPES and CNPq, respectively.
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Correspondence should be addressed to: H.T. Pinheiro Departamento de Oceanografia e Ecologia Universidade Federal do Espı´rito Santo Avenida F. Ferrari, 514, Goiabeiras, Vito´ria, ES Brazil, 29075-910 email: htpinheiro@gmail.com