INTRODUCTION
The Atlantic goliath grouper, Epinephelus itajara (Lichtenstein, 1822), is the largest reef fish in the western Atlantic, attaining a weight of over 300 kg and a length of over 2.5 m. The species has been vastly overfished throughout its range, which extends from North Carolina, USA to southern Brazil, and it is now considered critically endangered (IUCN, 2013). Under full protection in US territories since 1990, the species is now recovering (Koenig et al., Reference Koenig, Coleman and Kingon2011), but populations elsewhere remain at relatively low levels (Ferreira et al., Reference Ferreira, Hostim-Silva, Bertoncini, Coleman, Koenig, Mitcheson and Colin2012). The goliath grouper is extremely vulnerable to overfishing, especially in spawning aggregations, which form in shallow waters (<50 m) (Koenig et al., Reference Koenig, Coleman and Kingon2011) during summer months.
In this paper, we report the skeletal abnormalities of ‘pugheadedness’ and ‘short-tail’ for the goliath grouper during our studies of their spawning aggregations. Skeletal abnormalities have been described for a variety of species (Cobcroft et al., Reference Cobcroft, Pankhursta, Sadler and Hart2001), however, to date, none have been described for the goliath grouper. ‘Pugheadedness’ is characterized by an antero-posterior compression of the upper jaw, resulting in the apparent protrusion of the lower jaw. ‘Short-tail’ is associated with malformations of vertebrae including fusion, distortion and underdevelopment of vertebrae and abnormalities in inter-vertebral spaces (Vågsholm & Djupvik, Reference Vågsholm and Djupvik1998; Gavaia et al., Reference Gavaia, Dinis and Cancela2002). Skeletal abnormalities appear to be initiated during early development, and may be related to dietary deficiencies, pollutants, adverse temperatures, inappropriate light conditions or oxygen depletion (Vågsholm & Djupvik, Reference Vågsholm and Djupvik1998; Scott, Reference Scott2001).
MATERIAL AND METHODS
Our observations were made during research dives and captures of goliath grouper in Florida (2012) and in southern Brazil (2011 and 2013) in spawning aggregations. A Nikon D5100 camera with Ikelite underwater housing was used to take the underwater photographs.
RESULTS
Figure 1A–D is a photographic comparison of adult goliath grouper observed during the 2011 and 2012 spawning seasons off the coast of Jupiter, Florida, USA (Three-holes’ natural reef) and off Santa Catarina State, Brazil (‘Monobóia’ artificial reef). Figure 1A depicts the profile of a normal goliath grouper, which is compared with that of two ‘pugheads’, one from Brazil (Figure 1B) and one from Florida (Figure 1C). The Florida ‘pughead’ (male, 174 cm total length) was captured and photographed (Figure 1C, inset) on board our research vessel. An individual with a ‘short-tail’ skeletal anomaly (Figure 1D) was observed in 2013 on the ‘RAM’ artificial reef, off Paraná state, south Brazil.
Photographic comparison of: (A) Normal profile of goliath grouper (Epinephelus itajara); (B) ‘Pughead’ goliath grouper observed in southern Brazil; (C) ‘Pughead’ goliath grouper observed off Jupiter, Florida, USA (inset image – close-up of deformity); and (D) ‘Short-tail’ deformity observed in southern Brazil. Note, split dorsal fin was the result of sampling fin rays for age determination.
The two ‘pugheads’ and the ‘short-tail’ were robust and did not show any overt signs of stress or malnutrition. Because all the specimens were observed on spawning sites, they probably engaged in normal reproductive behaviours.
DISCUSSION
Skeletal deformities in wild populations of goliath grouper have been observed in very low frequencies. In the research conducted in Florida on the goliath grouper, we have captured and sampled nearly 600 adults and over 2500 juveniles. We have observed over three times that many underwater on dives, but have only observed ‘pugheadedness’ once. Skeletal abnormalities, including ‘pugheadedness’, although widespread among species, is rare among adults in wild populations of any one species, as reported by Gudger (Reference Gudger1937); Mansueti (Reference Mansueti1960); Cheek (Reference Cheek1965); Isaacson (Reference Isaacson1965); Briggs (Reference Briggs1966); Dahlberg (Reference Dahlberg1970); Bortone (Reference Bortone1971); Riehl & Schmitt (Reference Riehl and Schmitt1984), amongst others.
It is unknown whether the observed deformities in adult goliath grouper reduced survival potential; however, the ‘pugheaded’ and ‘short-tail’ individuals showed no overt signs of poor health, so feeding was apparently unhindered. Goliath grouper feed on slow-moving fishes and crustaceans, so once located, prey are easily ingested via suction feeding. Avoidance of predators was also not likely hindered by the observed maladies, because the fish remain close to structures such as reefs and wrecks as adults (Koenig et al., Reference Koenig, Coleman and Kingon2011) and mangrove shorelines and undercuts as juveniles (Koenig et al., Reference Koenig, Coleman, Eklund, Schull and Ueland2007), and they are quick to dive for cover when potential predators appear. The fact that individuals with abnormalities were observed in spawning aggregations suggests that they were capable of reproduction.
A wide variety of hatchery-reared fish species typically show a much greater frequency of skeletal abnormalities, including ‘pugheadedness’, than their wild populations (e.g. Grinstead, Reference Grinstead1971; Komada, Reference Komada1980; Cobcroft et al., Reference Cobcroft, Pankhursta, Sadler and Hart2001). In the sheltered conditions of a hatchery, several causes have been implicated, including: overcrowding (Shariff et al., Reference Shariff, Zainuddin and Abdullah1986), xenobiotics (Haga et al., Reference Haga, Suzuki, Kagechika and Takeuchi2003), nutrition (Cobcroft et al., Reference Cobcroft, Pankhursta, Sadler and Hart2001), inbreeding (Sadler & King, Reference Sadler and King2001) and dietary deficiencies (Takeuchi et al., Reference Takeuchi, Haga, Seikai and Watanabe1998). In these studies, it is possible that the incidence of skeletal deformities is greater because abnormal individuals are sheltered (i.e. food is supplied and predation is eliminated). That is, abnormal individuals may have a higher survival rate in the hatchery leading to the observation of a higher frequency among hatchery-reared adults.
The causes of the observed deformities in wild populations of goliath grouper are unknown, but they probably arise during early development (Cobcroft et al., Reference Cobcroft, Pankhursta, Sadler and Hart2001). Such abnormalities apparently have little effect on the normal behaviours of adults, such as feeding and reproduction, however, the survival rate of abnormal fish, especially during the early ontological stages in the wild, is unknown. To determine the overall incidence and effect of these abnormalities, survival throughout development, larva through adult, must be considered. Thus, it is unknown whether the low frequency of the occurrence of skeletal abnormalities in wild populations is due to a low incidence of occurrence or to a low survival of abnormal fish during early ontogeny, but adults appear to be little effected.
ACKNOWLEDGEMENTS
The authors acknowledge the grants received in Brazil from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Espírito Santo (FAPES) and Meros do Brasil Project, with the financial support of Programa Petrobras Ambiental – Petrobras and grants in the USA from the NOAA MARFIN Program. A capture and release permit was obtained for our research through the courtesy of the Florida Fish and Wildlife Conservation Commission (License Number: SAL-12-1244E-SRP).
