Runs of homozygosity in killer whale genomes provide a global record of demographic histories.

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.

Cooperative feeding in common dolphins as suggested by ontogenetic patterns in δ15 N bulk and amino acids.

Understanding the effect of stage-specific traits on species feeding habits can reveal how natural selection shapes life strategies. Amino acid (AA) nitrogen stable isotopes (δ15 N) provide multiple proxies of habitat baseline values and diet that can improve our understanding of species feeding strategies relative to their animal metabolism. We evaluated the effect of body length as a proxy for life stage and sex on the feeding habits of the common dolphin Delphinus delphis delphis using δ13 C and δ15 N in bulk tissue and AAs δ15 N from skin samples collected for almost two decades. For bulk δ13 C and δ15 N data, we used SIBER analysis to compare isotopic niches by sex and life stage. For AA δ15 N data, we developed a hierarchical Bayesian model (HBM) to estimate indices of trophic status (Δ15 N and trophic position). The model reflected the natural hierarchical structure of AA data by partitioning variability into three sources: between laboratory replicates, within dolphins and among dolphins. Estimates of Δ15 N based on all trophic and source AAs were more precise for each dolphin, less variable among dolphins and on average 2.4‰ higher than indices based on single trophic (Glx) and source (Phe) AAs. Precision was further increased when information was shared among individuals through random effects or regression models. Estimates of trophic position showed similar patterns. Both Δ15 N and δ15 Nbulk isotopic niches showed no difference by sex, suggesting that males and females have similar feeding habits and may not segregate. However, lower Δ15 N values for weaning calves and smaller juveniles discriminate them from adults, whereas δ15 N bulk isotopic niches do not. A trophic discrimination factor (TDFTro-Src ) of 3.1‰ was required for reasonable estimates of trophic position for these dolphins. Together, the lack of δ15 N differences between sexes, low variation between juveniles and adults and knowledge of common dolphins' social organization support intraspecific feeding cooperation as an important strategy to feed in the highly dynamic marine environment. Our study also presents an efficient way to analyse complex AA δ15 N data using HBM to investigate foraging behaviour in long-lived marine species difficult to study in the wild.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Passive acoustic monitoring of the decline of Mexico's critically endangered vaquita.

The vaquita (Phocoena sinus) is the world's most endangered marine mammal with approximately 245 individuals remaining in 2008. This species of porpoise is endemic to the northern Gulf of California, Mexico, and historically the population has declined because of unsustainable bycatch in gillnets. An illegal gillnet fishery for an endangered fish, the totoaba (Totoaba macdonaldi), has recently resurged throughout the vaquita's range. The secretive but lucrative wildlife trade with China for totoaba swim bladders has probably increased vaquita bycatch mortality by an unknown amount. Precise population monitoring by visual surveys is difficult because vaquitas are inherently hard to see and have now become so rare that sighting rates are very low. However, their echolocation clicks can be identified readily on specialized acoustic detectors. Acoustic detections on an array of 46 moored detectors indicated vaquita acoustic activity declined by 80% between 2011 and 2015 in the central part of the species' range. Statistical models estimated an annual rate of decline of 34% (95% Bayesian credible interval -48% to -21%). Based on results from 2011 to 2014, the government of Mexico enacted and is enforcing an emergency 2-year ban on gillnets throughout the species' range to prevent extinction, at a cost of US$74 million to compensate fishers. Developing precise acoustic monitoring methods proved critical to exposing the severity of vaquitas' decline and emphasizes the need for continual monitoring to effectively manage critically endangered species.

Ecological metrics of biomass removed by three methods of purse-seine fishing for tunas in the eastern tropical Pacific Ocean.

An ecosystem approach to fisheries management is a widely recognized goal, but describing and measuring the effects of a fishery on an ecosystem is difficult. Ecological information on the entire catch (all animals removed, whether retained or discarded) of both species targeted by the fishery and nontarget species (i.e., bycatch) is required. We used data from the well-documented purse-seine fishery for tunas (Thunnus albacares, T. obesus, and Katsuwonus pelamis) in the eastern tropical Pacific Ocean to examine the fishery's ecological effects. Purse-seine fishing in the eastern tropical Pacific is conducted in 3 ways that differ in the amount and composition of target species and bycatch. The choice of method depends on whether the tunas are swimming alone (unassociated sets), associated with dolphins (dolphin sets), or associated with floating objects (floating-object sets). Among the fishing methods, we compared catch on the basis of weight, number of individuals, trophic level, replacement time, and diversity. Floating-object sets removed 2-3 times as much biomass as the other 2 methods, depending on how removal was measured. Results of previous studies suggest the ecological effects of floating-object sets are thousands of times greater than the effects of other methods, but these results were derived from only numbers of discarded animals. Management of the fishery has been driven to a substantial extent by a focus on reducing bycatch, although discards are currently 4.8% of total catch by weight, compared with global averages of 7.5% for tuna longline fishing and 30.0% for midwater trawling. An ecosystem approach to fisheries management requires that ecological effects of fishing on all animals removed by a fishery, not just bycatch or discarded catch, be measured with a variety of metrics.

Distribution of the acoustic occurrence of dolphins during the summers 2011 to 2015 in the Upper Gulf of California, Mexico.

Baseline knowledge of spatial and temporal distribution patterns is essential for cetacean management and conservation. Such knowledge is particularly important in areas where gillnet fishing occurs, as the Upper Gulf of California, which increases the probability of bycatch of cetaceans. In this area, the vaquita porpoise (Phocoena sinus) has been widely studied, but the knowledge of other cetaceans is scarce and based on traditional visual survey methods. We used data collected by an array of acoustic click detectors (C-PODs) during the summers 2011 to 2015 to analyze the distribution of dolphins in the Vaquita Refuge in the Upper Gulf of California. We recorded 120,038 echolocation click trains of dolphins during 12,371 days of recording effort at 46 sampling sites. Based on simultaneous visual and acoustic data, we estimated a false positive acoustic detection rate of 19.4%. Dolphin acoustic activity varied among sites, with higher activity in the east of the Vaquita Refuge. Acoustic activity was higher at night than during the day. We used negative binomial generalized linear models to study the count of clicks of dolphins in relation to spatial, temporal, physical, biological and anthropogenic explanatory variables. The best model selected for the response variable included sampling site, day-night condition, and vertical component of tide speed. Patterns in the spatial distribution of predicted acoustic activity of dolphins were similar to the acoustic activity observed per sampling season. Higher acoustic activity was predicted at night, but the tide speed variable was not relevant under this condition. Acoustic activity patterns could be related to the availability of prey resources since echolocation click trains are associated with foraging activities of dolphins. This is the first study of the distribution of dolphins in Mexico using medium-term systematic passive acoustic monitoring, and the results can contribute to better management to the natural protected area located in the Upper Gulf of California.

Temporal variation in pelagic food chain length in response to environmental change.

Climate variability alters nitrogen cycling, primary productivity, and dissolved oxygen concentration in marine ecosystems. We examined the role of this variability (as measured by six variables) on food chain length (FCL) in the California Current (CC) by reconstructing a time series of amino acid-specific δ15N values derived from common dolphins, an apex pelagic predator, and using two FCL proxies. Strong declines in FCL were observed after the 1997-1999 El Niño Southern Oscillation (ENSO) event. Bayesian models revealed longer FCLs under intermediate conditions for surface temperature, chlorophyll concentration, multivariate ENSO index, and total plankton volume but not for hypoxic depth and nitrate concentration. Our results challenge the prevalent paradigm that suggested long-term stability in the food web structure in the CC and, instead, reveal that pelagic food webs respond strongly to disturbances associated with ENSO events, local oceanography, and ongoing changes in climate.

Correction to 'Food limitation of sea lion pups and the decline of forage off central and southern California'.

[This corrects the article DOI: 10.1098/rsos.150628.].

Food limitation of sea lion pups and the decline of forage off central and southern California.

California sea lions increased from approximately 50 000 to 340 000 animals in the last 40 years, and their pups are starving and stranding on beaches in southern California, raising questions about the adequacy of their food supply. We investigated whether the declining sea lion pup weight at San Miguel rookery was associated with changes in abundance and quality of sardine, anchovy, rockfish and market squid forage. In the last decade off central California, where breeding female sea lions from San Miguel rookery feed, sardine and anchovy greatly decreased in biomass, whereas market squid and rockfish abundance increased. Pup weights fell as forage food quality declined associated with changes in the relative abundances of forage species. A model explained 67% of the variance in pup weights using forage from central and southern California and 81% of the variance in pup weights using forage from the female sea lion foraging range. A shift from high to poor quality forage for breeding females results in food limitation of the pups, ultimately flooding animal rescue centres with starving sea lion pups. Our study is unusual in using a long-term, fishery-independent dataset to directly address an important consequence of forage decline on the productivity of a large marine predator. Whether forage declines are environmentally driven, are due to a combination of environmental drivers and fishing removals, or are due to density-dependent interactions between forage and sea lions is uncertain. However, declining forage abundance and quality was coherent over a large area (32.5-38° N) for a decade, suggesting that trends in forage are environmentally driven.

Patterns of cetacean sighting distribution in the Pacific exclusive economic zone of Costa Rica based on data collected from 1979-2001.

Nineteen species of cetaceans (families Balaenopteridae, Kogiidae, Physeteridae, Ziphiidae and Delphinidae) occur in the Costa Rican Pacific Exclusive Economic Zone (EEZ). Based on data recorded from the EEZ by the Southwest Fisheries Service Center, Cascadia Research Collective, and CIMAR between 1979-2001, we mapped the distribution of 18 cetacean species. Our results suggest that the majority of the cetacean species use primarily oceanic waters, particularly those species within the families Balaenopteridae, Kogiidae. Physeteridae and Ziphiidae. Members of the family Delphinidae showed a wide variety of distribution patterns: seven species are widespread throughout the EEZ, four appear to be exclusively pelagic, and two are primarily coastal. Overall, three cetacean species appear to have populations concentrated in coastal waters: Stenella attenuata graffmani. Tursiops truncatus, and Megaptera novaeangliae. These three may be more susceptible to human activities due to the overlap of their ranges with fishery areas (tuna and artisanal fisheries), and an uncontrolled increase of touristic whale watching activities in several parts of their range. The distribution maps represent the first comprehensive representation of cetacean species that inhabit Costa Rican Pacific waters. They provide essential base-line information that may be used to initiate conservation and management efforts of the habitats where these animals reproduce and forage.

Inferring cetacean population densities from the absolute dynamic topography of the ocean in a hierarchical Bayesian framework.

We inferred the population densities of blue whales (Balaenoptera musculus) and short-beaked common dolphins (Delphinus delphis) in the Northeast Pacific Ocean as functions of the water-column's physical structure by implementing hierarchical models in a Bayesian framework. This approach allowed us to propagate the uncertainty of the field observations into the inference of species-habitat relationships and to generate spatially explicit population density predictions with reduced effects of sampling heterogeneity. Our hypothesis was that the large-scale spatial distributions of these two cetacean species respond primarily to ecological processes resulting from shoaling and outcropping of the pycnocline in regions of wind-forced upwelling and eddy-like circulation. Physically, these processes affect the thermodynamic balance of the water column, decreasing its volume and thus the height of the absolute dynamic topography (ADT). Biologically, they lead to elevated primary productivity and persistent aggregation of low-trophic-level prey. Unlike other remotely sensed variables, ADT provides information about the structure of the entire water column and it is also routinely measured at high spatial-temporal resolution by satellite altimeters with uniform global coverage. Our models provide spatially explicit population density predictions for both species, even in areas where the pycnocline shoals but does not outcrop (e.g. the Costa Rica Dome and the North Equatorial Countercurrent thermocline ridge). Interannual variations in distribution during El Niño anomalies suggest that the population density of both species decreases dramatically in the Equatorial Cold Tongue and the Costa Rica Dome, and that their distributions retract to particular areas that remain productive, such as the more oceanic waters in the central California Current System, the northern Gulf of California, the North Equatorial Countercurrent thermocline ridge, and the more southern portion of the Humboldt Current System. We posit that such reductions in available foraging habitats during climatic disturbances could incur high energetic costs on these populations, ultimately affecting individual fitness and survival.

Current and future patterns of global marine mammal biodiversity.

Quantifying the spatial distribution of taxa is an important prerequisite for the preservation of biodiversity, and can provide a baseline against which to measure the impacts of climate change. Here we analyse patterns of marine mammal species richness based on predictions of global distributional ranges for 115 species, including all extant pinnipeds and cetaceans. We used an environmental suitability model specifically designed to address the paucity of distributional data for many marine mammal species. We generated richness patterns by overlaying predicted distributions for all species; these were then validated against sightings data from dedicated long-term surveys in the Eastern Tropical Pacific, the Northeast Atlantic and the Southern Ocean. Model outputs correlated well with empirically observed patterns of biodiversity in all three survey regions. Marine mammal richness was predicted to be highest in temperate waters of both hemispheres with distinct hotspots around New Zealand, Japan, Baja California, the Galapagos Islands, the Southeast Pacific, and the Southern Ocean. We then applied our model to explore potential changes in biodiversity under future perturbations of environmental conditions. Forward projections of biodiversity using an intermediate Intergovernmental Panel for Climate Change (IPCC) temperature scenario predicted that projected ocean warming and changes in sea ice cover until 2050 may have moderate effects on the spatial patterns of marine mammal richness. Increases in cetacean richness were predicted above 40° latitude in both hemispheres, while decreases in both pinniped and cetacean richness were expected at lower latitudes. Our results show how species distribution models can be applied to explore broad patterns of marine biodiversity worldwide for taxa for which limited distributional data are available.

Patterns of cetacean sighting distribution in the Pacific Exclusive Economic Zone of Costa Rica based on data collected from 1979-2001

Nineteen species of cetaceans (families Balaenopteridae, Kogiidae, Physeteridae, Ziphiidae and Delphinidae) occur in the Costa Rican Pacific Exclusive Economic Zone (EEZ). Based on data recorded from the EEZ by the Southwest Fisheries Service Center, Cascadia Research Collective, and CIMAR between 1979- 2001, we mapped the distribution of 18 cetacean species. Our results suggest that the majority of the cetacean species use primarily oceanic waters, particularly those species within the families Balaenopteridae, Kogiidae, Physeteridae and Ziphiidae. Members of the family Delphinidae showed a wide variety of distribution patterns: seven species are widespread throughout the EEZ, four appear to be exclusively pelagic, and two are primarily coastal. Overall, three cetacean species appear to have populations concentrated in coastal waters: Stenella attenuata graffmani, Tursiops truncatus, and Megaptera novaeangliae. These three may be more susceptible to human activities due to the overlap of their ranges with fishery areas (tuna and artisanal fisheries), and an uncontrolled increase of touristic whale watching activities in several parts of their range. The distribution maps represent the first comprehensive representation of cetacean species that inhabit Costa Rican Pacific waters. They provide essential base-line information that may be used to initiate conservation and management efforts of the habitats where these animals reproduce and forage

Diecinueve especies de cetáceos distribuídos en cinco familias (Balaenopteridae, Kogiidae, Physeteridae, Ziphiidae and Delphinidae) habitan en la Zona Económica Exclusiva del Pacífico de Costa Rica (ZEEP). Con base a datos tomados en esta zona por el Southwest Fisheries Service Center, Cascadia Research Collective y CIMAR entre 1979 y 2001 construímos mapas de distribución de avistamientos para 18 especies. Nuestros resultados sugieren que la mayoría de las especies de cetáceos habitan en aguas oceánicas, particularmente miembros de las familias Balaenopteridae, Kogiidae, Physeteridae y Ziphiidae. Miembros de la familia Delphinidae mostraron una variedad de patrones de distribución, siete mostraron una distribución amplia en el ZEEP, cuatro parecen ser exclusivamente oceánicas y dos principalmente costeras. Adicionalmente, tres especies de cetáceos tienen poblaciones concentradas en la costa: Stenella attenuata graffmani, Tursiops truncatus y Megaptera novaeangliae. Estas tres especies son por lo tanto más suceptibles debido a que su hábitat traslapa considerablemnte con áreas importantes para la pesca artesanal y atunera, y áreas de observación de ballenas (las cuales a incrementado considerablemente en los últimos años). Los mapas de distribución de avistamientos de cetáceos presentados en este trabajo son los primeros en su tipo para Costa Rica. Estos aportan información esencial y básica para iniciativas de conservación y manejo de estos animals y los habitats donde estos se reproducen y alimentan