Determinants of lungworm specificity in five cetacean species in the western Mediterranean.

BACKGROUND: Current data about Pseudaliidae show contrasting patterns of host specificity between congeneric species. We investigated how both contact and compatibility between hosts and parasites contributed to the patterns of lungworm infection observed in a community of five species of cetaceans in the western Mediterranean. METHODS: The lungs of 119 striped dolphins Stenella coeruleoalba, 18 bottlenose dolphins Tursiops truncatus, 7 Risso's dolphins Grampus griseus, 7 long-finned pilot whales Globicephala melas, and 6 common dolphins Delphinus delphis were analysed for lungworms. Parasites were identified by morphology and analysis of ITS2 sequences using both maximum likelihood and Bayesian inference methods. Body length was used as a proxy for lungworm species fitness in different hosts and compared with Kruskal-Wallis tests. Infection parameters were compared between cetacean species using Fisher's exact tests and Kruskal-Wallis tests. Phylogenetic specificity was explored by collating the overall lungworm species prevalence values in hosts from previous surveys in various localities. To explore the relative importance of vertical and horizontal transmission, Spearman's rank correlation was used to look for an association between host size and lungworm burden. A Mantel test was used to explore the association between lungworm species similarity and prey overlap using dietary data. RESULTS: Halocercus delphini had higher infection levels in striped dolphins and common dolphins; Stenurus ovatus had higher infection levels in bottlenose dolphins; and Stenurus globicephalae had higher infection levels in long-finned pilot whales. These results are congruent with findings on a global scale. Morphometric comparison showed that the larger nematodes were found in the same host species that had the highest parasite burden. Lungworms were found in neonatal striped dolphins and a Risso's dolphin, and there was a weak but significant correlation between host size and parasite burden in striped dolphins and bottlenose dolphins. There was also a weak but significant association between prey overlap and lungworm species similarity. CONCLUSIONS: Data indicate that phylogenetic specificity has an important role in governing host-parasite associations, as indicated by the higher infection levels and larger nematode size in certain hosts. However, diet can also influence infection patterns in these preferred hosts and contribute to less severe infections in other hosts.

Photo-identification comparison of four Indo-Pacific humpback dolphin populations off southeast China.

Indo-Pacific humpback dolphins (Sousa chinensis) inhabit shallow coastal waters of the Indo-Pacific region including southeast China, with at least 6 putative populations identified to date in Chinese waters. However, the connectivity among these populations has not yet been fully investigated. In the present study, we compared and cross-matched photographic catalogs of individual dolphins collected to date in the Pearl River Delta region, Leizhou Bay, Sanniang Bay, and waters southwest of Hainan Island, a total of 3158 individuals, and found no re-sighting of individual dolphins among the 4 study areas. Furthermore, there was a notable difference in the pigmentation pattern displayed by individuals from these 4 regions. We suggest that this may be a phenotypical expression of fine-scale regional differentiation among humpback dolphin groups, possibly distinct populations. Given the considerable conservation management implications it may carry (e.g. definition of management units), further research is much needed.

Early divergence and differential population histories of the Indo-Pacific humpback dolphin in the Pacific and Indian Oceans.

The currently recognized Indo-Pacific humpback dolphin occurs in estuaries and surrounding shallow waters from the South China Sea to the Asian coast of the Indian Ocean. However, a recent study suggested that the humpback dolphin from the Bay of Bengal may represent a distinct phylogenetic species. In this study, we sequenced 915-bp mtDNA segments from five geographic populations in both Chinese and Thai waters; together with previously published sequences, these data revealed that the ancestral Indo-Pacific humpback dolphin might have split during the transition from the Oligocene to Miocene (23.45 Mya, 95% HPD: 16.65-26.55 Mya), and then dispersed along the Pacific and Indian Ocean coasts of Asia. Genetic differentiation was detected between most of the examined populations, except for only a few pairwise populations in the northern South China Sea. Genetic differentiation/distance between the humpback dolphins from the northern and southern South China Sea met the sub-species threshold value proposed for marine mammals, whereas that between the humpback dolphins in the Pacific and the Indian Ocean was above the species threshold. Bayesian inference of historic gene flow indicated low but constant northward gene flow along the Indian Ocean coast; however, there was a recent abrupt increase in gene flow in the Pacific region, likely due to the shortening coastline at the low stand of sea level. Our results revealed that the current taxonomic classification of Indo-Pacific humpback dolphins may not reflect their phylogeography.

Complete mitogenome of Ganges river dolphin, Platanista gangetica gangetica and its phylogenetic relationship with other cetaceans.

The Ganges river dolphin, Platanista gangetica gangetica is one of the endangered cetaceans. Due to increasing anthropogenic activities, it has faced a significant reduction in distribution range since the late 1800s and has even gone extinct from most of the early localities. The investigation of complete mitogenome holds significant relevance for identifying evolutionary relationships and monitoring the endangered species. Herein, we report and characterize for the first time the 16,319 bp complete mitochondrial genome of P. g. gangetica. It comprises 13 protein-coding genes, 22 transfer RNA (tRNA) genes, two ribosomal RNA genes, and one control region (CR). The genome composition was A + T biased (59.6%) and exhibited a positive AT-skew (0.104) and negative GC-skew (- 0.384). All the genes were encoded on the heavy strand, except eight tRNAs and the ND6 gene. In the CR, an 18 bp tandem repeat sequence was observed. Our Bayesian Inference (BI) and Maximum Likelihood (ML) based phylogenetic analysis indicated that studied river dolphins were polyphyletic and the placement of Platanista was to be more basal than other river dolphins (Lipotes, Inia and Pontoporia). The pairwise genetic distance of Platanista with other cetaceans was varied, with an overall close affinity with whales. The model-based BI and ML phylogenetic analysis indicated that Platanista clustering with Ziphiidae with high to moderate supportive values (PP/BP = 98/68). The results of this study provide insights important for the conservation genetics and further evolutionary studies of the freshwater river dolphins.

Phylogenomics of the genus Tursiops and closely related Delphininae reveals extensive reticulation among lineages and provides inference about eco-evolutionary drivers.

Phylogeographic inference has provided extensive insight into the relative roles of geographical isolation and ecological processes during evolutionary radiations. However, the importance of cross-lineage admixture in facilitating adaptive radiations is increasingly being recognised, and suggested as a main cause of phylogenetic uncertainty. In this study, we used a double digest RADseq protocol to provide a high resolution (~4 Million bp) nuclear phylogeny of the Delphininae. Phylogenetic resolution of this group has been especially intractable, likely because it has experienced a recent species radiation. We carried out cross-lineage reticulation analyses, and tested for several sources of potential bias in determining phylogenies from genome sampling data. We assessed the divergence time and historical demography of T. truncatus and T. aduncus by sequencing the T. aduncus genome and comparing it with the T. truncatus reference genome. Our results suggest monophyly for the genus Tursiops, with the recently proposed T. australis species falling within the T. aduncus lineage. We also show the presence of extensive cross-lineage gene flow between pelagic and European coastal ecotypes of T. truncatus, as well as in the early stages of diversification between spotted (Stenella frontalis; Stenella attenuata), spinner (Stenella longirostris), striped (Stenella coeruleoalba), common (Delphinus delphis), and Fraser's (Lagenodelphis hosei) dolphins. Our study suggests that cross-lineage gene flow in this group has been more extensive and complex than previously thought. In the context of biogeography and local habitat dependence, these results improve our understanding of the evolutionary processes determining the history of this lineage.

Molecular footprints of inshore aquatic adaptation in Indo-Pacific humpback dolphin (Sousa chinensis).

The Indo-Pacific humpback dolphin, Sousa chinensis, being a member of cetaceans, had fully adapted to inshore waters. As a threatened marine mammal, little molecular information available for understanding the genetic basis of ecological adaptation. We firstly sequenced and obtained the draft genome map of S. chinensis. Phylogenetic analysis in this study, based on the single copy orthologous genes of the draft genome, is consistent with traditional phylogenetic classification. The comparative genomic analysis indicated that S. chinensis had 494 species-specific gene families, which involved immune, DNA repair and sensory systems associated with the potential adaption mechanism. We also identified the expansion and positive selection genes in S. chinensis lineage to investigate the potential adaptation mechanism. Our study provided the potential insight into the molecular bases of ecological adaptation in Indo-Pacific humpback dolphin and will be also valuable for future understanding the ecological adaptation and evolution of cetaceans at the genomic level.

Population Structure of Riverine and Coastal Dolphins Sotalia fluviatilis and Sotalia guianensis: Patterns of Nuclear and Mitochondrial Diversity and Implications for Conservation.

Coastal and freshwater cetaceans are particularly vulnerable due to their proximity to human activity, localized distributions, and small home ranges. These species include Sotalia guianensis, found in the Atlantic and Caribbean coastal areas of central and South America, and Sotalia fluviatilis, distributed in the Amazon River and tributaries. We investigated the population structure and genetic diversity of these 2 species by analyses of mtDNA control region and 8-10 microsatellite loci. MtDNA analyses revealed strong regional structuring for S. guianensis (i.e., Colombian Caribbean vs. Brazilian Coast, FST = 0.807, ΦST = 0.878, P < 0.001) especially north and south of the Amazon River mouth. For S. fluviatilis, population structuring was detected between the western and eastern Amazon (i.e., Colombian Amazon vs. Brazilian Amazon, FST = 0.085, ΦST = 0.277, P < 0.001). Haplotype and nucleotide diversity were higher for S. fluviatilis. Population differentiation was supported by analysis of the microsatellite loci (S. guianensis, northern South America vs. southern South America FST = 0.275, Jost's D = 0.476, P < 0.001; S. fluviatilis, western and eastern Amazon FST = 0.197, Jost's D = 0.364, P < 0.001). Most estimated migration rates in both species overlapped with zero, suggesting no measurable migration between most of the sampling locations. However, for S. guianensis, there was measurable migration in neighboring sampling locations. These results indicate that the small home ranges of these species may act to restrict gene flow between populations separated by relatively short distances, increasing the risk of extirpation of some localized populations in the future if existing threats are not minimized.

The Influence of Selection on MHC DQA and DQB Haplotypes in the Endemic New Zealand Hector's and Maui Dolphins.

Strong balancing selection on the major histocompatibility complex (MHC) can lead to different patterns in gene frequencies and neutral genomic variation within species. We investigated diversity and geographic structure of MHC genes DQA and DQB, as well as their inferred functional haplotypes, from 2 regional populations (East and West Coast) of the endangered Hector's dolphin (Cephalorhynchus hectori hectori) and the critically endangered Maui dolphin (Cephalorhynchus hectori maui) (West Coast, North Island), and contrasted these results with patterns from neutral microsatellites. The Maui had the lowest number of alleles for DQA (2) and DQB (3), consistent with strong genetic drift acting on this remnant population. However, the 2 retained DQA alleles are among the most divergent combinations of all 4 alleles found across the Hector's metapopulation, potentially reflecting the retention of divergent alleles due to balancing selection. The high frequency of the divergent DQB*04 allele also gave this population the highest nucleotide diversity for DQB. Strong differentiation was evident for DQA, DQB, and DQA-DQB haplotypes between the regional populations of Hector's dolphins (FST > 0.213) and both subspecies (FST > 0.311). Differentiation was generally greater than observed at neutral microsatellite loci, suggesting the influence of selection between geographically proximate East and West Coast populations. This might be the result of spatial differences in directional selection on those opposite coastlines. In addition, measures of the ratio of nonsynonymous to synonymous substitutions (dN/dS) were consistent with balancing selection over evolutionary time. Together, these results suggest a complex interplay of balancing selection, directional selection, local fidelity, and genetic drift.

Examining the viability of dorsal fin pigmentation for individual identification of poorly-marked delphinids.

Dolphin photo-identification has traditionally relied only on distinctive markings on the dorsal fin-this is problematic for delphinids whose populations exhibit a low mark ratio. We used common dolphins (genus Delphinus) as a model species to assess the viability of using pigmentation for photo-identification. Using a photo-identification catalogue of 169 adult individuals collected between 2002 and 2013, we extracted features that quantified pigmentation in a manner that was robust to lighting artefacts and dorsal fin orientation. We determined the proportion of individuals which exhibited pigmentation and examined temporal stability by (i) visually examining individuals and (ii) testing for seriation. We found 88-91% of images could be manually matched to the correct individual in the catalogue based on pigmentation patterns alone. A linear discriminant analysis classifier correctly identified the correct individual 77% of the time. We found 95% common dolphins exhibited distinctive pigmentation-all of which were temporarily stable. Our work challenges the current thinking that pigmentation is an unreliable feature for delphinid photo-identification and suggests that this feature could be applied to common dolphins and other poorly-marked delphinids.

Echolocation click source parameters of Australian snubfin dolphins (Orcaella heinsohni).

The Australian snubfin dolphin (Orcaella heinsohni) is endemic to Australian waters, yet little is known about its abundance and habitat use. To investigate the feasibility of Passive Acoustic Monitoring for snubfin dolphins, biosonar clicks were recorded in Cygnet Bay, Australia, using a four-element hydrophone array. Clicks had a mean source level of 200 ± 5 dB re 1 µPa pp, transmission directivity index of 24 dB, mean centroid frequency of 98 ± 9 kHz, and a root-mean-square bandwidth of 31 ± 3 kHz. Such properties lend themselves to passive acoustic monitoring, but are comparable to similarly-sized delphinids, thus requiring additional cues to discriminate between snubfins and sympatric species.

Evolution of the alternative AQP2 gene: Acquisition of a novel protein-coding sequence in dolphins.

Taxon-specific de novo protein-coding sequences are thought to be important for taxon-specific environmental adaptation. A recent study revealed that bottlenose dolphins acquired a novel isoform of aquaporin 2 generated by alternative splicing (alternative AQP2), which helps dolphins to live in hyperosmotic seawater. The AQP2 gene consists of four exons, but the alternative AQP2 gene lacks the fourth exon and instead has a longer third exon that includes the original third exon and a part of the original third intron. Here, we show that the latter half of the third exon of the alternative AQP2 arose from a non-protein-coding sequence. Intact ORF of this de novo sequence is shared not by all cetaceans, but only by delphinoids. However, this sequence is conservative in all modern cetaceans, implying that this de novo sequence potentially plays important roles for marine adaptation in cetaceans.

A new tropical Oligocene dolphin from Montañita/Olón, Santa Elena, Ecuador.

A new small probable Oligocene dolphin from Ecuador represents a new genus and species, Urkudelphis chawpipacha. The new taxon is known from a single juvenile skull and earbones; it differs from other archaic dolphins in features including widely exposed frontals at the vertex, a dorsally wide open vomer at the mesorostral groove, and a strongly projected and pointed lateral tuberosity of the periotic. Phylogenetic analysis places it toward the base of the largely-extinct clade Platanistoidea. The fossil is one of a few records of tropical fossil dolphins.

Acoustic occurrence detection of a newly recorded Indo-Pacific humpback dolphin population in waters southwest of Hainan Island, China.

In 2014, Indo-Pacific humpback dolphins were recorded for the first time in waters southwest of Hainan Island, China. In this paper, the temporal occurrence of Indo-Pacific humpback dolphins in this region was detected by stationary passive acoustic monitoring. During the 130-day observation period (from January to July 2016), 1969 click trains produced by Indo-Pacific humpback dolphins were identified, and 262 ten-minute recording bins contained echolocation click trains of dolphins, of which 70.9% were at night and 29.1% were during the day. A diurnal rhythm with a nighttime peak in acoustic detections was found. Passive acoustic detections indicated that the Indo-Pacific humpback dolphins frequently occurred in this area and were detected mainly at night. This information may be relevant to conservation efforts for these dolphins in the near future.

A simulation of temperature influence on echolocation click beams of the Indo-Pacific humpback dolphin (Sousa chinensis).

A finite element method was used to investigate the temperature influence on sound beams of the Indo-Pacific humpback dolphin. The numerical models of a dolphin, which originated from previous computed tomography (CT) scanning and physical measurement results, were used to investigate sound beam patterns of the dolphin in temperatures from 21 °C to 39 °C, in increments of 2 °C. The -3 dB beam widths across the temperatures ranged from 9.3° to 12.6°, and main beam angle ranged from 4.7° to 7.2° for these temperatures. The subsequent simulation suggested that the dolphin's sound beam patterns, side lobes in particular, were influenced by temperature.

Categorizing click trains to increase taxonomic precision in echolocation click loggers.

Passive acoustic monitoring is an efficient way to study acoustically active animals but species identification remains a major challenge. C-PODs are popular logging devices that automatically detect odontocete echolocation clicks. However, the accompanying analysis software does not distinguish between delphinid species. Click train features logged by C-PODs were compared to frequency spectra from adjacently deployed continuous recorders. A generalized additive model was then used to categorize C-POD click trains into three groups: broadband click trains, produced by bottlenose dolphin (Tursiops truncatus) or common dolphin (Delphinus delphis), frequency-banded click trains, produced by Risso's (Grampus griseus) or white beaked dolphins (Lagenorhynchus albirostris), and unknown click trains. Incorrect categorization rates for broadband and frequency banded clicks were 0.02 (SD 0.01), but only 30% of the click trains met the categorization threshold. To increase the proportion of categorized click trains, model predictions were pooled within acoustic encounters and a likelihood ratio threshold was used to categorize encounters. This increased the proportion of the click trains meeting either the broadband or frequency banded categorization threshold to 98%. Predicted species distribution at the 30 study sites matched well to visual sighting records from the region.

Geographic variation in Risso's dolphin echolocation click spectra.

Discrimination of bioacoustic signals to the species or population level is critical for using passive acoustic monitoring to study cetacean ecology. Risso's dolphins off southern California have distinctive peaks and notches in their echolocation clicks, but it was unknown whether Risso's dolphins from other geographic areas have similarly distinctive click spectra and whether populations are acoustically distinct. This study investigates using clicks for species and population identification by characterizing the spectral structure of Risso's dolphin echolocation clicks recorded over wide-ranging geographic regions including the U.S. waters of the North Atlantic Ocean, Gulf of Mexico, and North Pacific Ocean; and international waters of the Eastern Tropical Pacific. All recordings with Risso's dolphin clicks exhibited the spectral peak and notch pattern described off southern California, indicating the presence of peak banding patterns is useful for species discrimination. Geographic regions were a significant explanatory factor for variability in the frequencies of click spectral peaks, with relatively higher frequency peaks and notches found off Hawaii compared to California waters and off the southeast U.S. compared to the Gulf of Mexico. In the North Atlantic Ocean, a latitudinal cline in frequencies was evident. Potential causes of acoustic variation within and among acoustic encounters are evaluated.

Limited trophic partitioning among sympatric delphinids off a tropical oceanic atoll.

Understanding trophic relationships among marine predators in remote environments is challenging, but it is critical to understand community structure and dynamics. In this study, we used stable isotope analysis of skin biopsies to compare the isotopic, and thus, trophic niches of three sympatric delphinids in the waters surrounding Palmyra Atoll, in the Central Tropical Pacific: the melon-headed whale (Peponocephala electra), Gray's spinner dolphin (Stenella longirostris longirostris), and the common bottlenose dolphin (Tursiops truncatus). δ15N values suggested that T. truncatus occupied a significantly higher trophic position than the other two species. δ13C values did not significantly differ between the three delphinds, potentially indicating no spatial partitioning in depth or distance from shore in foraging among species. The dietary niche area-determined by isotopic variance among individuals-of T. truncatus was also over 30% smaller than those of the other species taken at the same place, indicating higher population specialization or lower interindividual variation. For P. electra only, there was some support for intraspecific variation in foraging ecology across years, highlighting the need for temporal information in studying dietary niche. Cumulatively, isotopic evidence revealed surprisingly little evidence for trophic niche partitioning in the delphinid community of Palmyra Atoll compared to other studies. However, resource partitioning may happen via other behavioral mechanisms, or prey abundance or availability may be adequate to allow these three species to coexist without any such partitioning. It is also possible that isotopic signatures are inadequate to detect trophic partitioning in this environment, possibly because isotopes of prey are highly variable or insufficiently resolved to allow for differentiation.

A toothless dwarf dolphin (Odontoceti: Xenorophidae) points to explosive feeding diversification of modern whales (Neoceti).

Toothed whales (Odontoceti) are adapted for catching prey underwater and possess some of the most derived feeding specializations of all mammals, including the loss of milk teeth (monophyodonty), high tooth count (polydonty), and the loss of discrete tooth classes (homodonty). Many extant odontocetes possess some combination of short, broad rostra, reduced tooth counts, fleshy lips, and enlarged hyoid bones-all adaptations for suction feeding upon fishes and squid. We report a new fossil odontocete from the Oligocene (approx. 30 Ma) of South Carolina (Inermorostrum xenops, gen. et sp. nov.) that possesses adaptations for suction feeding: toothlessness and a shortened rostrum (brevirostry). Enlarged foramina on the rostrum suggest the presence of enlarged lips or perhaps vibrissae. Phylogenetic analysis firmly places Inermorostrum within the Xenorophidae, an early diverging odontocete clade typified by long-snouted, heterodont dolphins. Inermorostrum is the earliest obligate suction feeder within the Odontoceti, a feeding mode that independently evolved several times within the clade. Analysis of macroevolutionary trends in rostral shape indicate stabilizing selection around an optimum rostral shape over the course of odontocete evolution, and a post-Eocene explosion in feeding morphology, heralding the diversity of feeding behaviour among modern Odontoceti.

Burst pulses of Guiana dolphin (Sotalia guianensis) in southeastern Brazil.

Acoustic studies of Guiana dolphin have been focused on whistles, with little known about pulse signals in this species. This study characterized the temporal and spectral properties of Guiana dolphin burst pulses. Groups of 2 to 23 Guiana dolphins were recorded while feeding and socializing in shallow waters in Guanabara Bay, southeastern Brazil, in 2013 and 2014. Burst pulse analysis involved two steps: signal detection and acoustic parameter analysis. Eight variables were analyzed for 197 total burst pulses: number of clicks, burst pulse duration, interclick interval, click duration, peak frequency, center frequency, -3 dB bandwidth, and -10 dB bandwidth. Mean burst pulse duration was 108.6 ms [standard deviation (SD) = 91.3] with a mean of 168 clicks (SD = 137.3). Burst pulses had short interclick interval (0.7 ms, SD = 0.3) and mean click duration of 300 µs (SD = 100). Mean peak frequency and center frequency were 28 kHz (SD = 11.6) and 29 kHz (SD = 11.0), respectively. Mean -3 dB bandwidth was 15 kHz (SD = 7.5) and mean -10 dB bandwidth was 40.5 kHz (SD = 14.3). The quantitative characterization of Guiana dolphin burst pulses is an important step in describing the full acoustic repertoire of this species.

Automatic classification of whistles from coastal dolphins of the southern African subregion.

Passive acoustic monitoring (PAM) is commonly used to generate information on the distribution, abundance, and behavior of cetacean species. In African waters, the utilization of PAM lags behind most other continents. This study examines whether the whistles of three coastal delphinid species (Delphinus delphis, Tursiops truncatus, and Tursiops aduncus) commonly encountered in the southern African subregion can be readily distinguished using both statistical analysis of standard whistle parameters and the automated detection and classification software PAMGuard. A first account of whistles recorded from D. delphis from South Africa is included. Using PAMGuard, classification to species was high with an overall mean correct classification rate of 87.3%. Although lower, high rates of correct classification were also found (78.4%) when the two T. aduncus populations were included separately. Classification outcomes reflected patterns observed in standard whistle parameters. Such acoustic discrimination may be useful for confirmation of morphologically similar species in the field. Classification success was influenced by training and testing the classifier with data from different populations, highlighting the importance of locally collected acoustic data to inform classifiers. The small number of sampling populations may have inflated the classification success, therefore, classification trials using a greater number of species are recommended.