Catherine M. Kemper

A review of heavy metal and organochlorine levels in marine mammals in Australia

Study of toxic contaminants in marine mammal specimens collected around Australia is currently uncoordinated and piecemeal. Most states collect samples but there is little or no financial support for their analysis. This study combines data, published or unpublished, from 13 sources. Heavy metals have been analysed in about 676 specimens; over 400 were for mercury levels in P. macrocephalus taken at a whaling station. The remaining samples were mostly from toothed whales, a few baleen whales (< 20), pinnipeds (41) and dugongs (49). The most consistently analysed metals were lead, mercury and cadmium. Liver and kidney lead levels ranged from < 1-3 ppm; levels in bone were 0-418 ppm, with most less than 10 ppm. Mercury levels in a large sample of P. macrocephalus muscle were < 12.2 ppm. Mercury levels in the small number of samples from other species were 0.51-143 ppm (kidney), 1.52-479 ppm (liver) and < 0.1-36 ppm (muscle). Cadmium levels in liver (0-52 ppm) and kidney (0-106 ppm) were extremely variable. Levels greater than 10 ppm were recorded in many species and were especially high in Hydrurga leptonyx, Dugong dugon, Mesoplodon layardii and Pseudorca crassidens. Adult Tursiops truncatus inhabiting the inshore gulfs of South Australia had considerably higher levels of cadmium compared with other regions. Information on organochlorine levels is sparse (approximately 39 specimens) and suggest low levels when compared to other parts of the world. Total DDT was highest (28.4 ppm) in a neonatal Orcinus orca. Some high levels of DDT were recorded in Tursiops truncatus, Delphinus delphis and Arctocephalus pusillus doriferus. PCBs ranged from < 0.05 to 3.87 ppm. A comprehensive pathological assessment of marine mammals is needed in order to evaluate the effects of toxic contaminants.

Heavy metal toxicity of kidney and bone tissues in South Australian adult bottlenose dolphins (Tursiops aduncus).

Metallothioneins (MT) concentration, renal damage, and bone malformations were investigated in 38 adult Tursiops aduncus carcasses to determine any associations with cadmium, copper, zinc, mercury, lead and selenium. Significantly higher concentrations of cadmium, copper, and zinc in the liver were observed in dolphins showing evidence of more advanced renal damage. No significant differences in metal or selenium concentrations in the liver were observed between groups differing in level of bone malformations. Some dolphins displayed evidence of toxicity and knowledge of metal toxicity pathways were used to elucidate the cause of these abnormalities. Two dolphins had high metal burdens, high MT concentrations, renal damage, and evidence of bone malformations, indicating possible severe and prolonged metal toxicity. One dolphin showed evidence of renal damage, but the lack of any other symptoms suggests that this was unlikely to be caused by metal toxicity. We recommend examining a range of metal toxicity symptoms simultaneously to aid in distinguishing metal toxicity from unrelated aetiologies.

Osteological variation and taxonomic affinities of bottlenose dolphins, Tursiops spp., from South Australia

Skulls and skeletons of 84 cranially mature bottlenose dolphins collected from South Australia were studied to distinguish morphological groups. The dataset comprised 38 skull measurements, 5 tooth counts/measurements, 6 coded skull features and 2 vertebral counts. There was no significant difference between sexes. Agglomerative, heirarchical cluster analyses performed on all variables and a dataset refined by eliminating those with high partial correlations produced two clear groups of skulls but with some differences in group membership between the statistical treatments. Size was an important factor in distinguishing groups, especially when categorical variables were excluded. Groups produced by cluster analysis of all variables were aligned with Tursiops truncatus and T. aduncus. In general, Tursiops truncatus was distinguished by a wide band (3-9 mm) of cancellous bone on the premaxillae, a distinct supraoccipital crest, raised naso-frontal complex, the almost complete lack of bone resorption on the pterygoid bones, a relatively wider rostrum, generally larger skull size (condylobasal length >465 mm versus <476 mm, except two skulls of 445 and 448 mm), and more than 60 vertebrae. This species was collected from open ocean coasts and sometimes stranded in groups. Tursiops aduncus generally had a narrow or no band of cancellous bone (0-5 mm), an indistinct or no supraoccipital crest, a naso-frontal complex that was not markedly raised, moderate to extensive bone resorption on the pterygoids, relatively narrow rostrum, fewer than 63 vertebrae and was collected mainly from the large gulfs. There was no significant difference between tooth diameter of T. aduncus and T. truncatus from South Australia.

Small mammals and habitat structure in lowland rain forest of Peninsular Malaysia

A method of assessing rain forest structure by ranking relative abundance of 41 habitat variables was used to describe habitat differences among six trapping sites (324 subsites). Variables included aspects of all vegetation layers but concentrated on those considered to be important to small mammal distribution. Ordination and classification methods resulted in similar analyses of the data. Differences in habitat structure were primarily related to the mois- ture conditions of the trapping sites and secondarily to their successional age (regenerating versus primary forest). The most important habitat variables for differentiating between sites were LITTER, CLEARING, SOILS, PIG DAMAGE, FLOODING, FAN PALM, EMERGENTS, CANOPY SURFACE and SEEDLINGS. Habitat structure also varied within sites with some suggestion of small-scale patterning. Small mammal captures were more likely in drier sites and subsites, but there was no dif- ference in trap success between regenerating sites and primary forest sites. Greater numbers of species were captured in sites containing a variety of habitats, a discrete layering of vegetation and an extensive understorey. Small mammal captures were positively associated with five habitat variables (EMERGENTS, LITTER, ROTTING LOGS, SEEDLINGS, ROUGH BARK) and negatively associated with five others (LAYERS, BERTAM, SEDGES, PIG DAMAGE, FLOODING). The destruction caused by pigs is thought to be a major factor since it reduces litter and food availability over wide areas. Leopoldamys sabanus was the most abundant small mammal captured (40/68 individuals) and trap success differences among sites (0.4-1.9%) reflect its preference for higher, well-drained habitats. The study demonstrates the usefulness of a simple method of ranking habitat features according to importance/abundance thus eliminating the all but impossible task of direct measurements in this complex system. This simple method of habitat description provides a basis for studying variables influencing faunal distribution patterns.

Niche differentiation of bottlenose dolphin species in South Australia revealed by stable isotopes and stomach contents

Context Animal species with overlapping ranges are common worldwide, but how these species coexist is less obvious. Dolphins are protected in Australia and yet little information is available on their resource use which is essential for successful management and conservation. Aim The aim of this study was to determine the degree of overlap in diet and feeding ecology of the two Tursiops spp. that have overlapping ranges in South Australia. Methods Stomach content (91 Tursiops sp. and 14 T. truncatus) and stable isotope (δ13C, δ15N) analyses (39 Tursiops sp. and 14 T. truncatus) were conducted. Carcasses of dolphins were opportunistically collected between 1974 and 2005. Diet was quantified by frequency of occurrence (FOO) and numerical abundance (NA) of prey. Key results Delta13C from teeth revealed distinct differences in primary source of carbon, corresponding to coastal (Tursiops sp. n = 39,  = –12.24, s.d. = 1.32) and offshore habitats (T. truncatus n = 14,  = –14.21, s.d. = 0.55). Differences in δ15N revealed Tursiops sp. ( = 11.66, s.d. = 0.58) feeds at a lower trophic level than T. truncatus ( = 14.29, s.d. = 0.88). Stomach content analyses for Tursiops sp. corroborated stable isotope results. There was a significant difference between the diets of Tursiops sp. from north Spencer Gulf and south Spencer Gulf (ANOSIM R = 0.249, P = 0.001). Prey were generally demersal in habit with the most important from the cephalopod families Octopodidae, Sepiidae and Loliginidae and fish families Carangidae, Clupeidae, Terapontidae and Apogonidae. For T. truncatus there were insufficient stomach contents for assessment. Conclusions South Australian bottlenose dolphin species exhibit distinct niche differentiation with clear evidence of regional variation in the diet of Tursiops sp. Implications The between and within species diet differentiation demonstrated, highlights the importance of regional management. Such results are internationally significant as coastal and offshore forms of Tursiops spp. occur worldwide.

The use of carcasses for the analysis of cetacean population genetic structure: a comparative study in two dolphin species

Advances in molecular techniques have enabled the study of genetic diversity and population structure in many different contexts. Studies that assess the genetic structure of cetacean populations often use biopsy samples from free-ranging individuals and tissue samples from stranded animals or individuals that became entangled in fishery or aquaculture equipment. This leads to the question of how representative the location of a stranded or entangled animal is with respect to its natural range, and whether similar results would be obtained when comparing carcass samples with samples from free-ranging individuals in studies of population structure. Here we use tissue samples from carcasses of dolphins that stranded or died as a result of bycatch in South Australia to investigate spatial population structure in two species: coastal bottlenose (Tursiops sp.) and short-beaked common dolphins (Delphinus delphis). We compare these results with those previously obtained from biopsy sampled free-ranging dolphins in the same area to test whether carcass samples yield similar patterns of genetic variability and population structure. Data from dolphin carcasses were gathered using seven microsatellite markers and a fragment of the mitochondrial DNA control region. Analyses based on carcass samples alone failed to detect genetic structure in Tursiops sp., a species previously shown to exhibit restricted dispersal and moderate genetic differentiation across a small spatial scale in this region. However, genetic structure was correctly inferred in D. delphis, a species previously shown to have reduced genetic structure over a similar geographic area. We propose that in the absence of corroborating data, and when population structure is assessed over relatively small spatial scales, the sole use of carcasses may lead to an underestimate of genetic differentiation. This can lead to a failure in identifying management units for conservation. Therefore, this risk should be carefully assessed when planning population genetic studies of cetaceans.

Cetacean café coronary

The carcass of a young adult male Indian Ocean Bottlenose dolphin (Tursiops cf aduncus) was found floating in an estuary near Adelaide, South Australia. An autopsy revealed that death had been caused by obstruction of the upper aerodigestive tract by a 660 mm Cobbler Carpetshark (Sutorectus tentaculatus). Similar airway obstruction in humans while feeding has been termed café coronary syndrome. Although death may have merely resulted from over-enthusiastic feeding, the possibility of neurological impairment was considered, and limited toxicological analyses of tissues was undertaken. No increase in organochlorine pesticides was found, however the possibility of heavy metal poisoning was not excluded. Formal neuropathology was unable to be undertaken. When sudden death in other mammal species mimics cases that are found in humans, similar underlying mechanisms may be present.

Unusual causes of fatal upper aerodigestive tract obstruction in wild bottlenose dolphins (Tursiops aduncus)

Necropsy examination of dolphins living in Gulf St Vincent, Australia is routinely undertaken to enable the evaluation of disease processes and to provide rapid medicolegal assessment of any inflicted and/or accidental injuries. Two Indo-Pacific Bottlenose Dolphins (Tursiops aduncus) are reported to demonstrate conditions that may result in unexpected death involving upper airway compromise by quite unusual mechanisms. In the first case an adult male was found with extensive soft tissue trauma suggesting human interaction. At necropsy, death was due instead to upper airway obstruction from an impacted Slender-spined Porcupine Fish (Diodon nichthemerus) in the posterior pharynx and upper esophagus. In the second case, an adult male dolphin was found to have died, following several weeks’ illness, from upper airway obstruction due to extensive respiratory tract papillomatosis within the blowhole. Given the infectious etiology of this condition the local population will be monitored for similar lesions. These cases demonstrate rare causes of upper airway obstruction in wild dolphins that were identifiable only after detailed necropsy examination. The possibility of human involvement in the deaths could be excluded.

Sexual maturity in male Indo-Pacific bottlenose dolphins (Tursiops aduncus): evidence for regressed/pathological adults

Abstract Age and sexual maturity have not previously been studied in Australian bottlenose dolphins. These were investigated in 57 male Indo-Pacific bottlenose dolphins (Tursiops aduncus) collected opportunistically in South Australia between 1989 and 2011. Age was estimated by counting growth layer groups in dentine tissue. Formalin-fixed testes plus epididymides were weighed, measured, and subsampled for histological analysis. Stage of spermatogenesis, presence of spermatozoa, testis tubule size, seminiferous tubule wall and tunica thickness, and relative amount of interstitial tissue were noted. Immature testis tubules contained only Sertoli cells and spermatogonia and had mean testis weights < 83 g, lengths < 190 mm, and tubule diameters < 98 μm. Testes of Active dolphins had spermatozoa, testis plus epididymis weights between 250 and 1,025 g, testis lengths between 164 and 292 mm, and mean tubule diameters > 84 μm. Regressed/pathological dolphins had testis weights (199–280 g), testis lengths (195–230 mm), and tubule diameters (59–130 μm) larger than Immature males and on average less than Active males. Seminiferous tubule wall thickness also separated Regressed/pathological male (X̄ = 14.9 μm) from Immature male (X̄ = 2.3 μm) testes. Sexual maturity in male Indo-Pacific bottlenose dolphins was attained between body lengths of 208 and 220 cm and body weights of 90 and 115 kg. Some males (20%) were sexually but not physically mature as determined by fusion of vertebral epiphyses. All physically mature males were sexually mature. The youngest sexually mature dolphin was 12 years old and the oldest immature male was 15 years, but samples were limited in the 8- to 12-year range. Testicular regression has not previously been reported in Tursiops spp. The 3 regressed males from South Australia had gross and histological evidence of organ pathology, including in the testes, suggesting that their reproductive status was related to ill health, rather than seasonal or individual cycling of function or senescence. The implications of heavy-metal toxicity on male Indo-Pacific bottlenose dolphin reproduction is discussed.

Cryptic grey-bellied dunnart (Sminthopsis griseoventer) discovered in South Australia: genetic, morphological and subfossil analyses show the value of collecting voucher material

The assumption that almost all mammal species are known to science has led to a recent trend away from collecting voucher specimens/tissues during field studies. Here we present a case study of a recently discovered cryptic marsupial (Sminthopsis griseoventer) in South Australia (SA) and show how such collections can contribute to rigorous biodiversity and biogeographic assessments. Morphological and genetic (allozyme and mitochondrial control region (CR) sequence data) analyses, including ancient DNA analyses of type material, were applied to 188 voucher specimens and 94 non-vouchered tissues of Sminthopsis held at the SA Museum. These data were used to confirm the presence of S. griseoventer in SA, validate means of identifying it morphologically and describe recent and pre-European distributions. Pelage differences between S. griseoventer and S. dolichura enabled their identification, but external measurements overlapped considerably. Subfossil S. griseoventer were identified from seven deposits and confirmed that in the past the species was more widespread in SA. CR divergences (>1.8%) among Western Australian and SA S. griseoventer suggested its long-term presence in SA. Discrepancies between the mitochondrial and allozyme affinities of S. aitkeni and S. griseoventer, coupled with the lack of obvious morphological differences, indicate that a taxonomic reappraisal of these species is warranted. The study strongly demonstrates an ongoing need for the routine collection of mammal voucher material in biological and environmental impact surveys.