Leszek Karczmarski

Rolling stones and stable homes: social structure, habitat diversity and population genetics of the Hawaiian spinner dolphin (Stenella longirostris)

Spinner dolphins (Stenella longirostris) exhibit different social behaviours at two regions in the Hawaiian Archipelago: off the high volcanic islands in the SE archipelago they form dynamic groups with ever‐changing membership, but in the low carbonate atolls in the NW archipelago they form long‐term stable groups. To determine whether these environmental and social differences influence population genetic structure, we surveyed spinner dolphins throughout the Hawaiian Archipelago with mtDNA control region sequences and 10 microsatellite loci (n = 505). F‐statistics, Bayesian cluster analyses, and assignment tests revealed population genetic separations between most islands, with less genetic structuring among the NW atolls than among the SE high islands. The populations with the most stable social structure (Midway and Kure Atolls) have the highest gene flow between populations (mtDNA ΦST < 0.001, P = 0.357; microsatellite FST = −0.001; P = 0.597), and a population with dynamic groups and fluid social structure (the Kona Coast of the island of Hawai’i) has the lowest gene flow (mtDNA 0.042 < ΦST < 0.236, P < 0.05; microsatellite 0.016 < FST < 0.040, P < 0.001). We suggest that gene flow, dispersal, and social structure are influenced by the availability of habitat and resources at each island. Genetic comparisons to a South Pacific location (n = 16) indicate that Hawaiian populations are genetically depauperate and isolated from other Pacific locations (mtDNA 0.216 < FST < 0.643, P < 0.001; microsatellite 0.058 < FST < 0.090, P < 0.001); this isolation may also influence social and genetic structure within Hawai’i. Our results illustrate that genetic and social structure are flexible traits that can vary between even closely‐related populations.

Integrating multiple lines of evidence to better understand the evolutionary divergence of humpback dolphins along their entire distribution range: a new dolphin species in Australian waters?

The conservation of humpback dolphins, distributed in coastal waters of the Indo‐West Pacific and eastern Atlantic Oceans, has been hindered by a lack of understanding about the number of species in the genus (Sousa) and their population structure. To address this issue, we present a combined analysis of genetic and morphologic data collected from beach‐cast, remote‐biopsied and museum specimens from throughout the known Sousa range. We extracted genetic sequence data from 235 samples from extant populations and explored the mitochondrial control region and four nuclear introns through phylogenetic, population‐level and population aggregation frameworks. In addition, 180 cranial specimens from the same geographical regions allowed comparisons of 24 morphological characters through multivariate analyses. The genetic and morphological data showed significant and concordant patterns of geographical segregation, which are typical for the kind of demographic isolation displayed by species units, across the Sousa genus distribution range. Based on our combined genetic and morphological analyses, there is convincing evidence for at least four species within the genus (S. teuszii in the Atlantic off West Africa, S. plumbea in the central and western Indian Ocean, S. chinensis in the eastern Indian and West Pacific Oceans, and a new as‐yet‐unnamed species off northern Australia).

Molecular ecology meets remote sensing: environmental drivers to population structure of humpback dolphins in the Western Indian Ocean

Genetic analyses of population structure can be placed in explicit environmental contexts if appropriate environmental data are available. Here, we use high-coverage and high-resolution oceanographic and genetic sequence data to assess population structure patterns and their potential environmental influences for humpback dolphins in the Western Indian Ocean. We analyzed mitochondrial DNA data from 94 dolphins from the coasts of South Africa, Mozambique, Tanzania and Oman, employing frequency-based and maximum-likelihood algorithms to assess population structure and migration patterns. The genetic data were combined with 13 years of remote sensing oceanographic data of variables known to influence cetacean dispersal and population structure. Our analyses show strong and highly significant genetic structure between all putative populations, except for those in South Africa and Mozambique. Interestingly, the oceanographic data display marked environmental heterogeneity between all sampling areas and a degree of overlap between South Africa and Mozambique. Our combined analyses therefore suggest the occurrence of genetically isolated populations of humpback dolphins in areas that are environmentally distinct. This study highlights the utility of molecular tools in combination with high-resolution and high-coverage environmental data to address questions not only pertaining to genetic population structure, but also to relevant ecological processes in marine species.

The evolving male: spinner dolphin (Stenella longirostris) ecotypes are divergent at Y chromosome but not mtDNA or autosomal markers

The susceptibility of the Y chromosome to sexual selection may make this chromosome an important player in the formation of reproductive isolating barriers, and ultimately speciation. Here, we investigate the role of the Y chromosome in phenotypic divergence and reproductive isolation of spinner dolphin (Stenella longirostris) ecotypes. This species contains six known ecotypes (grouped into four subspecies) that exhibit striking differences in morphology, habitat and mating system, despite having adjacent or overlapping ranges and little genetic divergence at previously studied mtDNA and autosomal markers. We examined the phylogeographic structure for all six ecotypes across the species range (n = 261, 17 geographic locations) using DNA sequences from three Y chromosome markers, two maternally inherited mitochondrial (mtDNA) markers, and a biparentally inherited autosomal intron. mtDNA and autosomal analyses revealed low divergence (most ΦST values <0.1) between ecotypes and geographic regions, concordant with previous studies. In contrast, Y intron analyses revealed fixed differences amongst the three most phenotypically divergent groups: S. l. longirostris vs. S. l. roseiventris vs. combined S. l. orientalis/S. l. centroamericana/Tres Marias ecotypes). Another ecotype (whitebelly), previously postulated to be a hybrid between the two phenotypically most divergent ecotypes, had Y haplotypes from both putative parent ecotypes, supporting a hybrid designation. Reduced introgression of the Y chromosome has previously been observed in other organisms ranging from insects to terrestrial mammals, and here we demonstrate this phenomenon in a marine mammal with high dispersal capabilities. These results indicate that reduced introgression of the Y chromosome occurs in a wide taxonomic range of organisms and support the growing body of evidence that rapid evolution of the Y chromosome is important in evolutionary diversification.

Indo-Pacific Humpback Dolphins: A Demographic Perspective of a Threatened Species

Indo-Pacific humpback dolphins inhabit shallow coastal waters within the tropics and subtropics of the Indian and Western Pacific Oceans. Their taxonomy remains unresolved, between a single widespread and highly variable species, two species, and three species being currently proposed. Their inshore distribution renders them highly susceptible to the adverse effects of many human activities; for most of the known remaining populations their continuous survival is a subject of major conservation concern. In this chapter, we describe the use of demographic analysis to quantify population trend and, more informatively, predict the risk (probabilities) of extinction. The results of demographic analyses provide valuable means of assessing conservation status. Using the population of humpback dolphins from the Pearl River Estuary as an example, we show the power of demographic analyses, predicting a significant population decline before it is directly documented by other standard techniques. Comparing our findings with known, albeit limited data from southeast Africa, and considering the current ambiguity of the taxonomic classification adopted by IUCN, we question the current listing of humpback dolphins under the IUCN Red List of Threatened Species. We urge that their conservation status classification be reconsidered as it likely understates, perhaps severely, the threats faced by many fragmented populations off Southeast Asia and the western Indian Ocean.

Spatiotemporal Trends of Heavy Metals in Indo-Pacific Humpback Dolphins (Sousa chinensis) from the Western Pearl River Estuary, China

We assessed the spatiotemporal trends of the concentrations of 11 heavy metals (HMs) in the liver and kidney of Indo-Pacific humpback dolphins (Sousa chinensis) from western Pearl River Estuary (PRE) during 2004-2015. The hepatic levels of Cr, As, and Cu in these dolphins were among the highest reported for cetaceans globally, and the levels of Zn, Cu, and Hg were sufficiently high to cause toxicological effects in some of the animals. Between same age-sex groups, dolphins from Lingdingyang were significantly more contaminated with Hg, Se, and V than those from the West-four region, while the opposite was true for Cd. Generalized additive mixed models showed that most metals had significant but dissimilar temporal trends over a 10-year period. The concentrations of Cu and Zn increased significantly in recent years, corresponding to the high input of these metals in the region. Body-length-adjusted Cd levels peaked in 2012, accompanied by the highest annual number of dolphin stranding events. In contrast to the significant decrease in HM levels in the dolphins in Hong Kong waters (the eastern reaches of the PRE), the elevated metal exposure in the western PRE raises serious concerns.

Phylogeography of the finless porpoise (genus Neophocaena ): testing the stepwise divergence hypothesis in the northwestern Pacific

We used 344 mitochondrial control region (717 bp) sequences from the finless porpoise (genus Neophocaena) from the northwestern Pacific to investigate the extent and manner in which past climatic oscillations may have shaped patterns of genetic diversity for this marine mammal. Both SplitsTree and Analysis of Molecular Variance (AMOVA) revealed the presence of a deep divergence among N. phocaenoides in subtropical waters compared with N. asiaeorientalis in temperate waters. Results from Migrate-n indicated that migration increased along the continent during the early Pleistocene period. Migration increased, although to a lesser extent than that during the Pleistocene, along the marginal shelf in the Yellow/Bohai Sea during the Last Glacial Maximum (LGM) due to a shortening coastline. Our results suggest that the current patterns of genetic diversity of Neophocaena vary at a hierarchy on a temporal and spatial scale, and phylogeographic history should be taken into account when examining species population structure and taxonomy.

Infanticide in the Indo-Pacific humpback dolphin (Sousa chinensis)

Infanticide has been observed in several mammalian taxa and studied in considerable detail in carnivores and primates. Although reported previously in cetaceans, known cases are few and their socio-behavioral context remains poorly understood. We report here on three cases of social coercion directed at mother-neonate pairs of Indo-Pacific humpback dolphins (Sousa chinensis) in the Pearl River Estuary, southeast China. Two of these cases resulted in confirmed infanticide. To aid the interpretation of our field observations, we refer to the results of necropsies of calf carcasses stranded and recovered in our research area between 2003 and 2012, which indicate that in several cases the main cause of death of stranded calves was asphyxia resulting from blunt-force trauma. This is consistent with the aggressive behaviors seen during our field observations. We conclude that male infanticide is the most plausible interpretation of the observed behaviors, never previously reported for the genus Sousa, while the calf-directed aggression is likely a result of socio-sexual harassment by males as part of their reproductive strategy.

Indo-Pacific humpback dolphins (Sousa chinensis) in Hong Kong: Modelling demographic parameters with mark-recapture techniques

Indo-Pacific humpback dolphins (Sousa chinensis) inhabiting Hong Kong waters are thought to be among the worlds most anthropogenically impacted coastal delphinids. We have conducted a 5-year (2010–2014) photo-ID study and performed the first in this region comprehensive mark-recapture analysis applying a suite of open population models and robust design models. Cormack-Jolly-Seber (CJS) models suggested a significant transient effect and seasonal variation in apparent survival probabilities as result of a fluid movement beyond the study area. Given the spatial restrictions of our study, limited by an administrative border, if emigration was to be considered negligible the estimated survival rate of adults was 0.980. Super-population estimates indicated that at least 368 dolphins used Hong Kong waters as part of their range. Closed robust design models suggested an influx of dolphins from winter to summer and increased site fidelity in summer; and outflux, although less prominent, during summer-winter intervals. Abundance estimates in summer (N = 144–231) were higher than that in winter (N = 87–111), corresponding to the availability of prey resources which in Hong Kong waters peaks during summer months. We point out that the current population monitoring strategy used by the Hong Kong authorities is ill-suited for a timely detection of a population change and should be revised.

Increased human occupation and agricultural development accelerates the population contraction of an estuarine delphinid

Over the past few thousand years, human development and population expansion in southern China have led to local extirpation and population contraction of many terrestrial animals. At what extent this early human-induced environmental change has also affected coastal marine species remains poorly known. We investigated the demographic history of the Indo-Pacific humpback dolphin (Sousa chinensis) in the Pearl River Delta (PRD); an obligatory inshore species known for its susceptibility to anthropogenic impacts in one of China’s most developed coastal regions. Although the deltaic evolution of PRD has been influenced by climate since the Holocene, ~74% reduction of the dolphin’s effective population size occurred within the last 2000 years, consistent with ~61% habitat contraction during this period. This considerable and recent population contraction may have been due to land use practices and deforestation in the upper/middle Pearl River region, all leading to increasing sedimentation rate in the estuarine area. As anthropogenic impacts within the drainage of Pearl River affected a vast area, coastal dolphins and large terrestrial mammals in southern China may share a similar demographic history, whilst the demographic and biogeographic history of the PRD humpback dolphins may be symptomatic of similar processes that this species may have undergone elsewhere in the region.