Journal of Fish Biology (2006) 68, 532–554 doi:10.1111/j.1095-8649.2006.00940.x, available online at http://www.blackwell-synergy.com
Brain morphology in large pelagic fishes: a comparison between sharks and teleosts T. J. L I S N E Y *
AND
S. P. C O L L I N
Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia (Received 7 October 2004, Accepted 10 August 2005) A quantitative comparison was made of both relative brain size (encephalization) and the relative development of five brain area of pelagic sharks and teleosts. Two integration areas (the telencephalon and the corpus cerebellum) and three sensory brain areas (the olfactory bulbs, optic tectum and octavolateralis area, which receive primary projections from the olfactory epithelium, eye and octavolateralis senses, respectively), in four species of pelagic shark and six species of pelagic teleost were investigated. The relative proportions of the three sensory brain areas were assessed as a proportion of the total ‘sensory brain’, while the two integration areas were assessed relative to the sensory brain. The allometric analysis of relative brain size revealed that pelagic sharks had larger brains than pelagic teleosts. The volume of the telencephalon was significantly larger in the sharks, while the corpus cerebellum was also larger and more heavily foliated in these animals. There were also significant differences in the relative development of the sensory brain areas between the two groups, with the sharks having larger olfactory bulbs and octavolateralis areas, whilst the teleosts had larger optic tecta. Cluster analysis performed on the sensory brain areas data confirmed the differences in the composition of the sensory brain in sharks and teleosts and indicated that these two groups of pelagic fishes had evolved different sensory strategies to cope with the demands of life # 2006 The Fisheries Society of the British Isles in the open ocean. Key words: cerebellum; ecomorphology; elasmobranch; encephalization; sensory system; telencephalon.
INTRODUCTION The pelagic realm is a highly productive marine environment in which resources are patchily distributed spatially and temporally. Consequently, the large predatory fishes, such as pelagic alopiid (thresher), carcharhinid (whaler), and lamnid (mackerel) sharks and coryphaenids (dolphinfishes), scombrids (tuna, wahoo, mackerels), gemphylids (snake-mackerels), istiophorids or billfish (sailfishes, spearfishes and marlins) and xiphiids (swordfish) that this environment supports, need to be highly migratory and extremely efficient, constantly on the move searching for prey and mates, and avoiding predators. Different
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groups of pelagic sharks and teleosts have co-evolved a number of adaptations to their environment and lifestyle, such as counter-shading, a fusiform streamlined body shape with a forked or lunate tail, efficient respiratory and digestive physiology, a high percentage of red muscle, and even endothermy (Helfman et al., 1997; Bernal et al., 2001). Many species also exhibit regular vertical oscillations, either within the epipelagic zone (0–200 m), or between the epipelagic and mesopelagic (200–1000 m) zones, which may be important for foraging (Carey & Scharold, 1990), behavioural thermoregulation (Holland et al., 1992; Bernal et al., 2001; Klimley et al., 2002), increased swimming efficiency (Weihs, 1973) and navigation (Klimley, 1993; Klimley et al., 2002). Very little is known, however, about the behavioural ecology and sensory biology of large pelagic sharks and teleosts, and whether the central nervous systems of these fishes show any degree of co-evolution similar to that exhibited by other aspects of their biology. The eyes of most pelagic species are large and well-developed (Tamura & Wisby, 1963; Gruber et al., 1975; Munz & McFarland, 1977; Kawamura et al., 1981; Fritsches et al., 2000, 2003a, b, 2005; Lisney, 2004) suggesting that vision is important in these animals. In the absence of information on the other sensory modalities, however, it is not easy to ascertain whether additional sensory systems also play an important role in their sensory ecology. A species’ lifestyle is reflected in the organization of its central nervous system (Nieuwenhuys et al., 1998), and so the study of brains can provide important insights into the biology of any given group of animals. Relationships between both brain size and the relative development of brain areas, and a range of ecological variables have been particularly well-studied in fishes (Kotrschal et al., 1998). Large brains have been correlated with factors such as habitat complexity, locomotor performance and an active predatory lifestyle (Bauchot et al., 1977, 1989; Northcutt, 1978). The relative size of sensory brain areas, which reflects sensory specializations and the relative importance of a given sensory modality, tends to be closely-related to feeding (as opposed to predator avoidance and locating mates) and the relative development of integration areas, such as the telencephalon and the cerebellum, has been related to differences in microhabitat (Kotrschal et al., 1998). The role of the telencephalon in fishes is not well understood, although this brain area is larger in fishes that live in spatially structured environments (Huber et al., 1997). The telencephalon also appears to be important for spatial learning and memory, and the performance of complex social tasks (Kotrschal et al., 1998; Hofmann, 2001; Broglio et al., 2003), while the cerebellum is involved in sensory-motor integration and receives inputs primarily from the visual and octavolateral systems (Meek & Nieuwenhuys, 1998; New, 2001). Although the brains of a number of pelagic sharks and teleosts have been described (Tuge et al., 1968; Okada et al., 1969; Kawamura et al., 1981) few quantitative analyses have been performed, and no attempts have been made to compare brain morphology in sharks and teleosts. Therefore, this study aimed to assess the ‘ecomorphology’ of brains (Kotrschal et al., 1998) from a selection of large pelagic sharks and teleosts. Both relative brain size (expressed as encephalization quotients, QE) and the relative development of five brain areas; two integration areas, the telencephalon and the cerebellum, and three sensory brain areas, the olfactory bulbs, optic tectum and octavolateralis area (which receive #
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primary projections from the olfactory epithelium, eye and octavolateralis senses, respectively) were investigated.
MATERIALS AND METHODS ANIMALS The brains from one individual from 10 species of pelagic fishes were analysed in this study: four species of shark [bigeye thresher shark Alopias superciliosus (Lowe), silky shark Carcharhinus falciformis (Bibron), blue shark Prionace glauca (L.) and crocodile shark Pseudocarcharias kamoharai (Matsubara)] and six species of teleost [common dolphinfish Coryphaena hippurus L., skipjack tuna Katsuwonus pelamis (L.), escolar Lepidocybium flavobrunneum (Smith), the shortbill spearfish Tetrapturus angustirostris Tanaka, striped marlin Tetrapturus audax (Philippi) and broadbill swordfish Xiphias gladius L.] (Table I). All of the teleosts and two of the shark species (A. superciliosus and P. glauca) were caught during a research longlining cruise aboard the U.S. National Atmospheric and Oceanographic Administration (NOAA) research vessel ‘Oscar Elton Sette’, around the Hawaiian Islands in December 2002. Of the two remaining shark species, the specimen of C. falciformis was collected at the Port Stephens Big Game Fishing Tournament, New South Wales, Australia, in February 2002, while the specimen of P. kamoharai was caught by a tuna long liner off the coast of Queensland, Australia, and was donated by researchers at the University of Queensland. All specimens were collected and sacrificed according to the ethical guidelines of the National Health and Medical Research Council of Australia. A minimum fork length (LF) was recorded for each specimen [as was the lower-jaw to fork length (LLJF) for the three billfish species T. angustirostris, T. audax and X. gladius] prior to dissection. The individuals of the four shark species and C. hippurus were also sexed. The brains were removed and fixed by immersion in 10% formalin in 01 M phosphate buffer or 4% paraformaldehyde in 01 M phosphate buffer. All brains were post-fixed for at least 5 months before further dissection and analysis, thereby avoiding the greatest fluctuations in brain mass due to fixation (Frontera, 1959; Bauchot, 1967; Lisney, 2004).
E N C E P H A L I Z A TI O N The meninges, blood vessels, choroid plexus and connective tissue were dissected away from each brain and the cranial and sensory nerves were transected at their base. Each brain was blotted and weighed to the nearest 001 g using an analytical balance. The sampling error of using this method was estimated to be 10, 10 and 1, and included five of the six shark species. Four of the sharks, P. kamoharai, C. longimanus, C. falciformis and A. superciliosus, had the highest QE of the species investigated (292, 266, 183 and 158, respectively). Of the teleosts, K. pelamis had the highest QE (131). Three billfish species, X. gladius, I. platypterus and T. argustirostris, had the lowest QE of 055, 034 and 032, respectively. Brain areas analysis The quantitative analysis of the relative volume of five brain areas (the olfactory bulbs, telencephalon, optic tectum, corpus cerebellum and the octavolateralis area) reflected the impressions given by visual inspection of the gross morphology, i.e. that there are substantial differences in gross brain morphology between pelagic sharks and teleosts (Tables II and III). The two integration areas, the telencephalon and the corpus cerebellum, were both relatively larger in the sharks in comparison to the teleosts. Relative to the ‘sensory brain’, the 100
Log10 brain mass (g)
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FIG. 4. The allometric relationship between brain mass and body mass for 14 species of pelagic fishes, six sharks (^) and eight teleosts (*) calculated using least squares regression. 1, Alopias superciliosus; 2, Isurus oxyrinchus; 3, Pseudocarcharias kamoharai; 4, Carcharhinus falciformis; 5, Carcharhinus longimanus; 6, Prionace glauca; 7, Coryphaena hippurus; 8, Lepidocybium flavobrunneum; 9, Katsuwonus pelamis; 10, Thunnus albacares; 11, Istiophorous platypterus; 12, Tetrapturus angustirostris; 13, Tetrapturus audax; 14, Xiphias gladius. The curve was fitted by: y ¼ 05301 x08735(r ¼ 0827).
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Tetrapturus argustirostris Istiophorous platypterus Xiphias gladius Thunnus albacres Coryphaena hippurus Lepidocybium flavobrunneum Isurus oxyrinchus Prionace glauca Tetrapturus audax Katsuwonus pelamis Alopias superciliosus Carcharhinus falciformis Carcharhinus longimanus Pseudocarcharias kamoharai 0
0·5
1
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QE FIG. 5. Encephalization quotients for 14 species of pelagic fishes, six sharks (&) and eight teleosts (&). Species with QE >10 have relatively larger brains.
volumes of the telencephalon and the corpus cerebellum in the sharks were 518 and 104%, respectively, whereas in the teleosts the volumes of these brain areas were much lower (59 and 31%, respectively). These differences were also reflected by the weighted factor analysis (Table II). The median relative size of the telencephalon was significantly larger in the sharks (Mann–Whitney U-test, n1 ¼ 4, n2 ¼ 6, P < 005), while the difference in the median relative size of the corpus cerebellum approached significance (Mann–Whitney U-test, n1 ¼ 4, n2 ¼ 6, P ¼ 0067). The ICF, which ranked the level of folding exhibited by the corpus cerebellum in each species on a scale of 1–5, revealed that this brain area was much more heavily foliated in the sharks (which had an average rank of 425) in comparison to the teleosts, whose average rank was 15 (Table II). The relative proportion of each of the three sensory brain areas, the olfactory bulbs, optic tectum and the octavolateralis area, was assessed as a proportion of the total ‘sensory brain’, and the relative volumes for each species were also normalized using a weighted factor (y) (Wagner, 2001a, b; Lisney, 2004), (Table II and Fig. 6). The olfactory bulbs were significantly larger in the sharks than in the teleosts (Mann–Whitney U-test, n1 ¼ 4, n2 ¼ 6, P < 005), accounting for, on average, nearly 40% of the total sensory brain volume (compared to
