Sexual dimorphism in striped dolphin (Stenella coeruleoalba) crania from South Africa

This study assessed the extent of sexual dimorphism in striped dolphin (Stenella coeruleoalba) cranial size and shape off the South African coast. Dorsal and ventral features of 60 striped dolphin crania from both the western and eastern coasts of South Africa were analyzed using landmark‐based geometric morphometrics. Although there was no evidence of dimorphism in cranial size, evidence for small, but significant, variation in both dorsal and ventral cranial shape was found between the sexes. The observed dimorphism was partly associated with changes in shape around the temporal fossa, occipital condyle and supraoccipital bone, the nasal bone, and the paraoccipital process and basiocciptal. The temporal fossa serves as an attachment point for the temporal muscle, which functions to close the lower jaw, and the occipital area serves as the anterior insertion of the epaxial muscles, which power the upstroke of the flukes during swimming. Both the paraoccipital process and basiocciptal are associated with the functioning of the hyoid apparatus, which serves as an attachment point for muscles and ligaments involved in feeding and sound production. These findings suggest the possibility of differences in diet, foraging behavior, vocalizations, and locomotion between the sexes of this species.     

Reproductive biology of female striped dolphin (Stenella coeruleoalba) from the western Mediterranean

Data on age and length at sexual maturity, calving interval, lactation period, and ovulation and pregnancy rates were analysed from 84 female striped dolphin collected during the Mediterranean morbillivirus epizootic. Age was determined by counting growth layer groups in tooth dentine, and reproductive status was determined by the macroscopic examination of the ovaries and the uterus. Age at sexual maturity (ASM) was estimated using two different methods; giving average estimates of 12 and 12.3 years. The average length at sexual maturity was 187 cm and the calving interval was four years. The annual pregnancy rate (APR) was calculated using two different criteria. In the first, only females that were pregnant at the time of death, as evidenced by the presence of a foetus, were incorporated in the calculations. This method gave an estimate of 8.9% as the apparent pregnancy rate of the dolphins killed by the epizootic. The second method incorporated in the calculations females that were pregnant at the time of death and females that had young corpus albicans in the ovaries and a distended uterus. This method is considered to reflect the true pregnancy rate of the population and gave an estimate of 25%. Estimates of ovulation rate (0.401) and lactation period (16 months) were considered to be potentially affected by the disease and, therefore, biased. These estimates reflect a peculiar situation of the diseased dolphins but are useful for comparative purposes. Estimates of ASM and APR, parameters which are not likely to be affected by the disease, differed markedly from those of other Stenella populations and could indicate a density-dependent response, possibly reflecting food limitations.     

Tetranucleotide microsatellite loci from the striped dolphin (Stenella coeruleoalba Meyen, 1833)

Five tetranucleotide microsatellite loci were isolated from the striped dolphin (Stenella coeruleoalba). Characterization of these loci revealed between three and 11 alleles at each locus and observed heterozygosity ranged from 0.192 to 0.775. All sets of primers amplified homologous loci when tested on four related species and showed polymorphisms in most locus–species combinations. A sixth microsatellite, which appeared to be monomorphic in the striped dolphin, was also shown to be polymorphic in three related species.     

Hepatic sarcocystosis in a striped dolphin (Stenella coeruleoalba) from the Spanish Mediterranean coast

Fatal hepatic sarcocystosis was diagnosed in a striped dolphin (Stenella coeruleoalba) from the northeastern Spanish Mediterranean coast based on pathologic findings and the microscopic and ultrastructural characteristics of the intralesional parasite. Main gross lesions were icterus, subcutaneous hemorrhages, and hepatic congestion. The most prominent microscopic lesions consisted of severe acute multifocal to coalescing necrotizing hepatitis with cholestasis and intralesional protozoa. There was severe chronic pancreatitis with generalized distension of pancreatic ducts by hyaline plugs and adult trematodes. Only asexual stages of the protozoa were found. The parasite in the liver divided by endopolygeny. Schizonts varied in shape and size. Mature schizonts had merozoites randomly arranged or budding peripherally around a central residual body. Schizonts were up to 22 microm long, and merozoites were up to 6 microm long. Ultrastructurally, merozoites lacked rhoptries. This parasite failed to react by immunohistochemistry with anti-Toxoplasma gondii, anti-Neospora caninum and anti-Sarcocystis neurona antibodies. The microscopic and ultrastructural morphologies of the parasite were consistent with Sarcocystis canis, so far described only from animals in the Unites States. The life cycle and source of S. canis are unknown. The present report of S. canis-like infection in a sea mammal from Spain indicates that the definitive host for this parasite also exists outside of the United States.     

A histological and NMR study of the melon of the striped dolphin (Stenella coeruleoalba)

The melon, the echolocation organ of the striped dolphin (Stenella coeruleoalba), was investigated by morphological and high-resolution (13)C nuclear magnetic resonance (NMR) methods, in order to characterize structure and composition gradient at the histological and molecular level. Morphological analysis showed that the lipidic components are organized in an adipose tissue; moreover, a clear muscular component was observed. Age-related structural differences also were noted. Furthermore, NMR yielded detailed information at a qualitative-quantitative level on the lipid components.     

Isolation of Clostridium tertium from a striped dolphin (Stenella coeruleoalba) in the Adriatic Sea

Bacteriologic examination of an abscess found between blubber and musculature of a striped dolphin (Stenella coeruleoalba) found dead on 30 March 2002 in the Adriatic Sea, Croatia, was performed and an aerotolerant, nontoxogenic Clostridium tertium was isolated in pure culture. National Collections of Industrial Food and Marine Bacteria (NCIMB Ltd., Aberdeen, Scotland, UK) confirmed the results. Sequencing results showed it to be C. tertium with 100% similarity. The strain was named Clostridium tertium strain Zagreb, acceded to the culture collection and assigned the accession number NCIMB 13970. This is the first record of C. tertium in marine mammals.     

Spatio‐temporal patterns of genetic diversity in the Mediterranean striped dolphin (Stenella coeruleoalba)

Comparing the genetic composition of wild animals between geographic regions with distinct environments is common in evolutionary studies. However, genetic composition can also change through time in response to environmental changes but studies examining this are carried out less often. In this study, we characterize striped dolphin genetic composition in the Mediterranean Sea across both geography and time. We provide genotype data for 15 microsatellite loci and 919 bp of mtDNA control region, collected over 21 years across all main Mediterranean Sea basins. We investigated spatial genetic structure using both classical and Bayesian population structure methods, and compared it with temporal patterns of genetic change using time‐series statistics. We integrated the temporal datasets with known environmental pressures and data on social structure, to infer potential drivers of observed changes. Geographic analyses suggest weak differentiation for striped dolphin in the Mediterranean Sea, with evidence for a recent expansion. Temporal analyses show significant cyclical fluctuations in genetic composition over 21 years, which correspond well with recurrent morbillivirus epizootics. Similarly, social group composition shows changes in the relative number of juveniles and adults per group, and an overall increase in the number of adults per group relative to juveniles over the time period. We suggest that the observed changes in genetic and group composition could relate to specific dynamics of morbillivirus resistance. Overall, our study highlights the importance of tracking long‐term genetic variation and the potential for this species as a model in studying genetic adaptation to environmental stress.     

Social kin associations and genetic structuring of striped dolphin populations (Stenella coeruleoalba) in the Mediterranean Sea

We investigated hierarchical patterns of genetic subdivision, and assessed kinship within and between social groups of striped dolphins (Stenella coeruleoalba) in the Tyrrhenian Sea. A total of 165 samples were analysed at eight microsatellite DNA loci, including outgroup samples from the Adriatic, Scotland and Spain for population-level comparisons. We found population genetic structure within the Mediterranean basin, including small but significant differentiation between the Adriatic and Tyrrhenian Seas (FST=0.0047, P=0.008), and between putative 'inshore' and 'offshore' (FST=0.0217, P=0.005) populations in the Tyrrhenian Sea. Assessment of kinship within and among 12 association groups showed higher average kinship for females within than between groups, and smaller groups showed higher average kinship. Comparisons of relatedness for both sexes showed a significant difference between males and females, with females more likely to associate with adult kin. Together these data emphasize the importance of the social cohesion of kin in small groups to the structuring of striped dolphin populations in this environment.     

Selection of reference genes for quantitative RT-PCR studies in striped dolphin (Stenella coeruleoalba) skin biopsies

Background  

Odontocete cetaceans occupy the top position of the marine food-web and are particularly sensitive to the bioaccumulation of lipophilic contaminants. The effects of environmental pollution on these species are highly debated and various ecotoxicological studies have addressed the impact of xenobiotic compounds on marine mammals, raising conservational concerns. Despite its sensitivity, quantitative real-time PCR (qRT-PCR) has never been used to quantify gene induction caused by exposure of cetaceans to contaminants. A limitation for the application of qRT-PCR is the need for appropriate reference genes which allow the correct quantification of gene expression. A systematic evaluation of potential reference genes in cetacean skin biopsies is presented, in order to validate future qRT-PCR studies aiming at using the expression of selected genes as non-lethal biomarkers.     

Isolation and genetic characterization of Toxoplasma gondii from striped dolphin (Stenella coeruleoalba) from Costa Rica

Toxoplasma gondii infection in marine mammals is of interest because of mortality and mode of transmission. It has been suggested that marine mammals become infected with T. gondii oocysts washed from land to the sea. We report the isolation and genetic characterization of viable T. gondii from a striped dolphin (Stenella coeruleoalba), the first time from this host. An adult female dolphin was found stranded on the Pacific Coast of Costa Rica, and the animal died the next day. The dolphin had a high (1:6400) antibody titer to T. gondii in the modified agglutination test. Severe nonsuppurative meningoencephalomyelitis was found in its brain and spinal cord, but T. gondii was not found in histological sections of the dolphin. Portions of its brain and the heart were bioassayed in mice for the isolation of T. gondii. Viable T. gondii was isolated from the brain, but not from the heart, of the dolphin. A cat fed mice infected with the dolphin isolate (designated TgSdCol) shed oocysts. Genomic DNA from tachyzoites of this isolate was used for genotyping at 10 genetic loci, including SAG1, SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, and Apico, and this TgSdCo1 isolate was found to be Type II.     

Nasitrema sp.-associated encephalitis in a striped dolphin (Stenella coeruleoalba) stranded in the Gulf of Mexico.

An immature female striped dolphin (Stenella coeruleoalba) found dead on a northwestern Florida beach in 1988 exhibited severe inflammation bilaterally in the dorsal and mid-thalamus in association with adult trematodes (Nasitrema sp.) and trematode eggs. Numerous specimens of Nasitrema sp. also were present in the pterygoid sinuses. Pneumonia in association with a heavy growth of Vibrio damsela was observed also. This report confirms the occurrence of Nasitrema sp.-associated encephalitis in striped dolphins and in small cetaceans from the Gulf of Mexico.     

Genetic differentiation in the striped dolphin Stenella coeruleoalba from European waters according to mitochondrial DNA (mtDNA) restriction analysis

We used mitochondrial DNA (mtDNA) restriction analysis to study genetic variation in 98 striped dolphins (Stenella coeruleoalba) stranded on coasts from different European countries and from animals caught by fisheries. A total of 63 different restriction sites was mapped after digestion of mtDNA with 15 restriction endonucleases that yielded a total of 27 haplotypes. No haplotype was shared between Mediterranean and Atlantic areas. All the analyses indicate the existence of two different populations with a very limited gene flow across the Strait of Gibraltar.     

Formation of the pits with taste buds at the lingual root in the striped dolphin,Stenella coeruleoalba

The tongue of the striped dolphin, Stenella coeruleoalba, shows a V-shaped row of pits on its posterior dorsum. Their development is described on the basis of macroscopic and light microscopic observations on fetal, young, and adult stages. Four to eight pits occur, most often five in the adult. Anlagen of the pits first protrude as round epithelial thickenings which later increase in diameter and become thin. The circular primordia then sink, and grooves oriented both circularly and radially develop in the walls of the shallow pits thus formed. Pits and grooves deepen with development so that older pits become lined with conical projections. As pits grow further, they become elongated anterolaterally, retaining slit-like openings. Each pit in the adult is 2–8 mm long and about 1 mm wide. The pits are not derived from lingual gland ducts but develop independently. Taste buds resembling those of other mammalian tongues can be found in young dolphins but are few in number and limited to the thin epithelium of the pit projections and to that of the side wall of the pits. They first appear in the late prenatal period but degenerate in the adult. A rich nerve supply is observable in the lamina propria below taste buds in the calf. The pits and their projections in the dolphin correspond to the vallate papillae of other mammals, but whether each projection or a whole pit corresponds to a single vallate papilla is undecided.     

Cephalopods in the diet of the striped dolphin Stenella coeruleoalba from the western Mediterranean during an epizootic in 1990

Fifteen cephalopod species from 28 stomach contents of striped dolphins, Stenella coeruleoalba (Meyen, 1833), stranded during an epizootic on the western Mediterranean coast in summer 1990, were analysed.
Albraliopsis pfefferi, Onychoteuthis banksii, Todarodes sagittatus and Brachioteuthis riisei are species showing higher relative importance indices. Composition and characteristics of cephalopod preys were discussed and compared to the scarce literature for this cetacean. The data showed a mixed diet of muscular and gelatinous body squids, mainly consisting of oceanic and pelagic or bathypelagic species.     

Microtriches of tetraphyllidean metacestodes from Western Mediterranean striped dolphins (Stenella coeruleoalba)

The tegumental structures of two types of tetraphyllidean plerocercoids and two types of merocercoids (Phyllobothrium delphini and Monorygma grimaldii) from Mediterranean striped dolphins, Stenella coeruleoalba, are described for the first time using scanning electron microscopy. The tegument of all of the specimens was fully covered with microtriches. Four basic types were found: filitriches, blade-like spinitriches of different sizes and shapes, cone-shaped spinitriches (with two parallel small projections of equal length at the apex), and crowned cylindrical spinitriches (with 6-7 small papillae forming a crown at the apex); the two latter types are newly described. The two types of plerocercoids had a similar morphology and distribution of microtriches; in addition, cilium-like projections appeared interspersed among the microtriches on the apical sucker, accessory suckers, and distal bothridial loculus. Merocercoids exhibited a greater variety of tegumental structures, especially on the distal bothridial loculus. Both merocercoid types had regularly spaced papillae or "buttons" on the accessory suckers and the distal bothridial loculus that were composed of a central cilium-like projection surrounded by numerous filitriches. However, crowned cylindrical spinitriches were specific to P. delphini and cone-shaped spinitriches were specific to M. grimaldii. Differences in the morphology and distribution of scolex microtriches of adult cestodes have been considered useful for species identification. A previous molecular study has suggested that P. delphini and M. grimaldii are actually different congeneric species. Our study has shown that significant differences in the morphology and distribution of microtriches occur between these species at the merocercoid stage.     

Modeling the spatial distribution of the striped dolphin (Stenella coeruleoalba) and common bottlenose dolphin (Tursiops truncatus) in the Gulf of Taranto (Northern Ionian Sea,Central-eastern Mediterranean Sea)

Although the EU Marine Strategy Framework Directive (MSFD) is largely based on the establishment of environmental targets and associated proxies to achieve Good Environmental Status (GES), a full suite of ecological indicators for all the ecosystem components is not currently available for ongoing assessment and regular update of GES targets. This is because effective indicators and management actions aimed at preserving/rebuilding marine biodiversity should be found from the knowledge of the spatial distribution of target species and extension of critical habitats as well as their overlapping with human activities, pressure and impacts. In this regard, the spatial distributions of the striped dolphin Stenella coeruleoalba and the common bottlenose dolphin Tursiops truncatus in the Gulf of Taranto (Northern Ionian Sea, Central-eastern Mediterranean Sea) were investigated by means of a generalized additive model (GAM) and a Random Forest (RF) based on sighting data collected during standardized vessel-based surveys carried out from 2009 to 2015. Eight predictive variables were considered, taking into account both the local physiographic features and human activities existing in the investigated area, suggesting an innovative approach to habitat modeling. In particular, the explanatory variables depth, distance from industrial areas and distance from the coast proved to significantly influence the distribution of both dolphin species. In addition, the distribution of S. coeruleoalba and T. truncatus were also significantly shaped by the distance from the navy exercise areas and the fishing areas, respectively. On the contrary, the slope and the distance from the main commercial routes never provided any significant influence. The reliability of GAM and RF models in predicting the spatial distribution of both dolphins was tested by applying the Youden Index method to the ROC curves. The RF model allowed the projection of the expected presence/absence pattern of S. coeruleoalba and T. truncatus to produce the preference habitat versus non habitat map. In particular, the RF model predicted that the striped dolphin is widely present in the central and deeper part of the Gulf of Taranto. In contrast, the common bottlenose dolphin seems to be mainly distributed along the coasts in both the eastern and western sector of the basin. A clear overlapping of the preference habitats estimated for S. coeruleoalba and T. truncatus is shown north of Punta Alice and in front of Policoro as well as offshore from Ugento in the eastern and western parts of the investigated area, respectively. Finally, the critical habitats of S. coeruleoalba and T. truncatus are the outcome of both the influence of environmental conditions and anthropogenic pressures presently occurring in the Gulf of Taranto, basically indicating the need for conservation measures, especially considering that the area is expected to be considered for hydrocarbon prospecting. These results contribute to setting up a baseline reference for future assessment of environmental marine disturbances using cetaceans, which are considered a key group in the MSFD, as an ecological indicator.     

Effect of the 1990 die-off in the northern Italian seas on the developmental stability of the striped dolphin Stenella coeruleoalba (Meyen, 1833)

Developmental stability of the community of striped dolphins, Stenella coeruleoalba (Meyen, 1833), that died during the Mediterranean epizootic of 1990 was compared with that of the population prior to and after the epizootic, to assess whether animals that died were the developmentally less stable individuals in the population. Significantly higher levels of fluctuating asymmetry (FA) were found in those individuals that died. Tissue levels of organochlorine pesticide residues and PCBs were determined and the correlation between contaminant concentration and FA was tested. No correlations were found between the contaminant level and FA.