A field study of chemical senses in bottlenose dolphins and pilot whales.

For most marine vertebrates, chemical cues provide crucial information during navigation and foraging, but their use by cetaceans is still poorly understood. In contrast to baleen whales, toothed whales (odontocetes) are scarcely equipped for chemoreception: they lack the conventional anatomical structures (i.e., olfactory epithelium, nerves and bulbs) involved in olfaction and have reduced taste buds on the tongue. Several behavioral studies have however shown that captive dolphins can perceive chemical solutions, including odorants, in their oral cavity. To investigate whether odontocetes could use infochemicals in their foraging ecology, we implemented a behavioral response experiment in wild bottlenose dolphins and long-finned pilot whales. We tested dimethyl sulfide (DMS) as a potentially attractive stimulus since it is a chemical signature of highly productive marine areas, known to attract several marine predators including fishes and seabirds. We assessed cetacean responses to DMS exposure by analyzing their movements and surface behaviors recorded by onboard observers. In both species, results did not reveal any significant attraction or behavioral reaction toward DMS when compared to a control chemical stimulus, apart from a short-distance response in bottlenose dolphins. These results suggest that while odontocetes may perceive DMS in water, it apparently does not play a significant role in their foraging ecology. Testing potentially more attractive compounds such as prey extracts with the present method and analyzing surface, underwater and acoustic responses would provide further insights on odontocete feeding behavior. It would also provide valuable clues to studies on the anatomical structures involved in their chemosenses.

Wait your turn, North Atlantic fin whales share a common feeding ground sequentially.

Highly migratory marine species pose a challenge for the identification of management units due to the absence of clear oceanographic barriers. The population structure of North Atlantic fin whales has been investigated since the start of whaling operations but is still the subject of an ongoing scientific debate. Here we measured stable isotopes of carbon, nitrogen and oxygen in skin samples collected from 151 individuals from western Iceland, Galicia (NW Spain), the Azores archipelago and the Strait of Gibraltar (SoG). We found spatiotemporal differences in stable isotope ratios suggesting that fin whales sampled in these four areas may share a common feeding ground within the Northeast Atlantic at different times during the year. Our results also suggest that SoG whales use this common feeding ground in summer but exploit Mediterranean resources during the winter months, further supporting the existence of a limited but current exchange of individuals between these two basins.

Stable isotopes reveal winter feeding in different habitats in blue, fin and sei whales migrating through the Azores.

Knowing the migratory movements and behaviour of baleen whales is fundamental to understanding their ecology. We compared δ15N and δ13C values in the skin of blue (Balaenoptera musculus), fin (Balaenoptera physalus) and sei (Balaenoptera borealis) whales sighted in the Azores in spring with the values of potential prey from different regions within the North Atlantic using Bayesian mixing models to investigate their trophic ecology and migration patterns. Fin whale δ15N values were higher than those recorded in blue and sei whales, reflecting feeding at higher trophic levels. Whales' skin δ15N and δ13C values did not reflect prey from high-latitude summer foraging grounds; instead mixing models identified tropical or subtropical regions as the most likely feeding areas for all species during winter and spring. Yet, differences in δ13C values among whale species suggest use of different regions within this range. Blue and sei whales primarily used resources from the Northwest African upwelling and pelagic tropical/subtropical regions, while fin whales fed off Iberia. However, determining feeding habitats from stable isotope values remains difficult. In conclusion, winter feeding appears common among North Atlantic blue, fin and sei whales, and may play a crucial role in determining their winter distribution. A better understanding of winter feeding behaviour is therefore fundamental for the effective conservation of these species.

Fin whale (Balaenoptera physalus) mitogenomics: A cautionary tale of defining sub-species from mitochondrial sequence monophyly.

The advent of massive parallel sequencing technologies has resulted in an increase of studies based upon complete mitochondrial genome DNA sequences that revisit the taxonomic status within and among species. Spatially distinct monophyly in such mitogenomic genealogies, i.e., the sharing of a recent common ancestor among con-specific samples collected in the same region has been viewed as evidence for subspecies. Several recent studies in cetaceans have employed this criterion to suggest subsequent intraspecific taxonomic revisions. We reason that employing intra-specific, spatially distinct monophyly at non-recombining, clonally inherited genomes is an unsatisfactory criterion for defining subspecies based upon theoretical (genetic drift) and practical (sampling effort) arguments. This point was illustrated by a re-analysis of a global mitogenomic assessment of fin whales, Balaenoptera physalus spp., published by Archer et al. (2013), which proposed to further subdivide the Northern Hemisphere fin whale subspecies, B. p. physalus. The proposed revision was based upon the detection of spatially distinct monophyly among North Atlantic and North Pacific fin whales in a genealogy based upon complete mitochondrial genome DNA sequences. The extended analysis conducted in this study (1676 mitochondrial control region, 162 complete mitochondrial genome DNA sequences and 20 microsatellite loci genotyped in 380 samples) revealed that the apparent monophyly among North Atlantic fin whales reported by Archer et al. (2013) to be due to low sample sizes. In conclusion, defining sub-species from monophyly (i.e., the absence of para- or polyphyly) can lead to erroneous conclusions due to relatively "trivial" aspects, such as sampling. Basic population genetic processes (i.e., genetic drift and migration) also affect the time to the most recent common ancestor and hence the probability that individuals in a sample are monophyletic.

Behavioural responses of humpback whales to food-related chemical stimuli.

Baleen whales face the challenge of finding patchily distributed food in the open ocean. Their relatively well-developed olfactory structures suggest that they could identify the specific odours given off by planktonic prey such as krill aggregations. Like other marine predators, they may also detect dimethyl sulfide (DMS), a chemical released in areas of high marine productivity. However, dedicated behavioural studies still have to be conducted in baleen whales in order to confirm the involvement of chemoreception in their feeding ecology. We implemented 56 behavioural response experiments in humpback whales using two food-related chemical stimuli, krill extract and DMS, as well as their respective controls (orange clay and vegetable oil) in their breeding (Madagascar) and feeding grounds (Iceland and Antarctic Peninsula). The whales approached the stimulus area and stayed longer in the trial zone during krill extract trials compared to control trials, suggesting that they were attracted to the chemical source and spent time exploring its surroundings, probably in search of prey. This response was observed in Iceland, and to a lesser extend in Madagascar, but not in Antarctica. Surface behaviours indicative of sensory exploration, such as diving under the stimulus area and stopping navigation, were also observed more often during krill extract trials than during control trials. Exposure to DMS did not elicit such exploration behaviours in any of the study areas. However, acoustic analyses suggest that DMS and krill extract both modified the whales' acoustic activity in Madagascar. Altogether, these results provide the first behavioural evidence that baleen whales actually perceive prey-derived chemical cues over distances of several hundred metres. Chemoreception, especially olfaction, could thus be used for locating prey aggregations and for navigation at sea, as it has been shown in other marine predators including seabirds.

Diet of bottlenose dolphins (Tursiops truncatus) from the Gulf of Cadiz: Insights from stomach content and stable isotope analyses.

The ecological role of species can vary among populations depending on local and regional differences in diet. This is particularly true for top predators such as the bottlenose dolphin (Tursiops truncatus), which exhibits a highly varied diet throughout its distribution range. Local dietary assessments are therefore critical to fully understand the role of this species within marine ecosystems, as well as its interaction with important ecosystem services such as fisheries. Here, we combined stomach content analyses (SCA) and stable isotope analyses (SIA) to describe bottlenose dolphins diet in the Gulf of Cadiz (North Atlantic Ocean). Prey items identified using SCA included European conger (Conger conger) and European hake (Merluccius merluccius) as the most important ingested prey. However, mass-balance isotopic mixing model (MixSIAR), using δ13C and δ15N, indicated that the assimilated diet consisted mainly on Sparidae species (e.g. seabream, Diplodus annularis and D. bellottii, rubberlip grunt, Plectorhinchus mediterraneus, and common pandora, Pagellus erythrinus) and a mixture of other species including European hake, mackerels (Scomber colias, S. japonicus and S. scombrus), European conger, red bandfish (Cepola macrophthalma) and European pilchard (Sardina pilchardus). These contrasting results highlight differences in the temporal and taxonomic resolution of each approach, but also point to potential differences between ingested (SCA) and assimilated (SIA) diets. Both approaches provide different insights, e.g. determination of consumed fish biomass for the management of fish stocks (SCA) or identification of important assimilated prey species to the consumer (SIA).

Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic.

Despite no obvious barrier to gene flow, historical environmental processes and ecological specializations can lead to genetic differentiation in highly mobile animals. Ecotypes emerged in several large mammal species as a result of niche specializations and/or social organization. In the North-West Atlantic, two distinct bottlenose dolphin (Tursiops truncatus) ecotypes (i.e. 'coastal' and 'pelagic') have been identified. Here, we investigated the genetic population structure of North-East Atlantic (NEA) bottlenose dolphins on a large scale through the analysis of 381 biopsy-sampled or stranded animals using 25 microsatellites and a 682-bp portion of the mitochondrial control region. We shed light on the likely origin of stranded animals using a carcass drift prediction model. We showed, for the first time, that coastal and pelagic bottlenose dolphins were highly differentiated in the NEA. Finer-scale population structure was found within the two groups. We suggest that distinct founding events followed by parallel adaptation may have occurred independently from a large Atlantic pelagic population in the two sides of the basin. Divergence could be maintained by philopatry possibly as a result of foraging specializations and social organization. As coastal environments are under increasing anthropogenic pressures, small and isolated populations might be at risk and require appropriate conservation policies to preserve their habitats. While genetics can be a powerful first step to delineate ecotypes in protected and difficult to access taxa, ecotype distinction should be further documented through diet studies and the examination of cranial skull features associated with feeding.