Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo-identification data with high-resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource- and/or mate-defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until approximately 15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.     

Uncertain recovery of the North Atlantic right whale in a changing ocean

Human activities have placed populations of many endangered species at risk and mitigation efforts typically focus on reducing anthropogenic sources of mortality. However, failing to recognize the additional role of environmental factors in regulating birth and mortality rates can lead to erroneous demographic analyses and conclusions. The North Atlantic right whale population is currently the focus of conservation efforts aimed at reducing mortality rates associated with ship strikes and entanglement in fishing gear. Consistent monitoring of the population since 1980 has revealed evidence that climate‐associated changes in prey availability have played an important role in the population's recovery. The considerable interdecadal differences observed in population growth coincide with remote Arctic and North Atlantic oceanographic processes that link to the Gulf of Maine ecosystem. Here, we build capture‐recapture models to quantify the role of prey availability on right whale demographic transitional probabilities and use a corresponding demographic model to project population growth rates into the next century. Contrary to previous predictions, the right whale population is projected to recover in the future as long as prey availability and mortality rates remain within the ranges observed during 1980–2012. However, recent events indicate a northward range shift in right whale prey, potentially resulting in decreased prey availability and/or an expansion of right whale habitat into unprotected waters. An annual increase in the number of whale deaths comparable to that observed during the summer 2017 mass mortality event may cause a decline to extinction even under conditions of normal prey availability. This study highlights the importance of understanding the oceanographic context for observed population changes when evaluating the efficacy of conservation management plans for endangered marine species.     

Dangerous dining: surface foraging of North Atlantic right whales increases risk of vessel collisions

North Atlantic right whales are critically endangered and, despite international protection from whaling, significant numbers die from collisions with ships. Large groups of right whales migrate to the coastal waters of New England during the late winter and early spring to feed in an area with large numbers of vessels. North Atlantic right whales have the largest per capita record of vessel strikes of any large whale population in the world. Right whale feeding behaviour in Cape Cod Bay (CCB) probably contributes to risk of collisions with ships. In this study, feeding right whales tagged with archival suction cup tags spent the majority of their time just below the water's surface where they cannot be seen but are shallow enough to be vulnerable to ship strike. Habitat surveys show that large patches of right whale prey are common in the upper 5 m of the water column in CCB during spring. These results indicate that the typical spring-time foraging ecology of right whales may contribute to their high level of mortality from vessel collisions. The results of this study suggest that remote acoustic detection of prey aggregations may be a useful supplement to the management and conservation of right whales.     

Postcopulatory selection for dissimilar gametes maintains heterozygosity in the endangered North Atlantic right whale

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long‐term implications have received little attention. Here, we combined over 25 years of field data with high‐resolution genetic data to assess the long‐term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long‐term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.     

Simulation of the entanglement of a North Atlantic right whale (Eubalaena glacialis) with fixed fishing gear

Population estimates of the critically endangered North Atlantic right whale (Eubalaena glacialis) put the number of individuals at 458 with the actual number likely being lower due to a recent unusual mortality event. Entanglement with fixed fishing gear is the most significant cause of mortality of North Atlantic right whales. There remains little documentation of how North Atlantic right whales become enwrapped during an encounter with fixed fishing gear. In order to gain a better understanding of how entanglements might occur, an interactive simulator was developed that allows the user to swim a virtual whale model using a standard game controller through a gear field in an attempt to re‐create an entanglement. The morphologically accurate right whale model produces realistic swimming motions and is capable of pectoral fin motions in response to user input. Using the simulator, gear entanglements involving the pectoral flippers including ropes wrapping around the body and entanglements involving the tailstock were re‐created. Entanglements involving the pectoral flippers with body wraps were more easily generated than entanglements involving the tailstock only. The simulator should aid scientists, fisheries experts, fishing gear designers, and bycatch reduction scientists in understanding entanglement dynamics and testing potential new gear configurations.     

Passive acoustic monitoring predicts daily variation in North Atlantic right whale presence and relative abundance in Roseway Basin,Canada

North Atlantic right whale monitoring in Roseway Basin, Canada, is primarily based on short‐term (<14 d) visual surveys conducted during August–September. Variability in survey effort has been the biggest limiting factor to studying changes in the population's occurrence and habitat use. Such efforts could be enhanced considerably using passive acoustic monitoring (PAM). We sought to determine if variation in whale presence, relative abundance, demography, and/or behavior (estimated through visual surveys) could be explained by variation in three right whale call types in this habitat. A generalized linear model was fit to 23 d of concurrent PAM and visual monitoring during four summers within the Roseway Basin Right Whale Critical Habitat boundaries. The model revealed significant positive relationships between relative abundance, call counts and presence of surface‐active group behavior. PAM can refine daily right whale presence estimates. While visual observations (n = 23 d) implied a 40% decline in right whale presence during 2014–2015 relative to 2004–2005, PAM data (n = 211 d) showed right whales were present between 71%–85% of survey days throughout all years analyzed. We demonstrate that PAM is a useful tool to extend periods of right whale monitoring, especially in areas where visual monitoring efforts may be limited.     

Visual and acoustic surveys for North Atlantic right whales,Eubalaena glacialis,in Cape Cod Bay,Massachusetts, 2001–2005: Management implications

North Atlantic right whales, Eubalaena glacialis, remain endangered, primarily due to excessive anthropogenic mortality. Current management protocols in US waters are triggered by identifying the presence of at least one right whale in a management area. We assessed whether acoustic detection of right whale contact calls can work as an alternative to visual aerial surveys for establishing their presence. Aerial survey and acoustic monitoring were conducted in Cape Cod Bay, Massachusetts, in 2001–2005 and used to evaluate and compare right whale detections. Over the 58 d with simultaneous aerial and acoustic coverage, aerial surveys saw whales on approximately two-thirds of the days during which acoustic monitoring heard whales. There was no strong relationship between numbers of whales seen during aerial surveys and numbers of contact calls detected on survey days. Results indicate acoustic monitoring is a more reliable mechanism than aerial survey for detecting right whales. Because simple detection is sufficient to trigger current management protocols, continuous, autonomous acoustic monitoring provides information of immediate management utility more reliably than aerial surveillance. Aerial surveys are still required to provide data for estimating population parameters and for visually assessing the frequency and severity of injuries from shipping and fishing and detecting injured and entangled right whales.     

Estimated absorbance spectra of the visual pigments of the North Atlantic right whale (Eubalaena glacialis)

To assess the spectral sensitivities of the retinal visual pigments from the North Atlantic right whale (Eubalaena glacialis), we have cloned and sequenced two exons from the rod opsin gene and two exons from the middle‐wavelength sensitive (MWS) cone opsin gene in order to determine the amino acids at positions known to be key regulators of the spectral location of the absorbance maximum (λ_max). Based on previous mutagenesis models we estimate that the right whale possesses a rod visual pigment with a λ_max of 499 nm and a MWS cone visual pigment with a λ_max of 524 nm. Although the MWS cone visual pigment from the right whale is blue‐shifted in its spectral sensitivity like those from odontocetes, the spectral sensitivity of the right whale rod visual pigment is similar to those from terrestrial mammals.     

Computational fluid dynamics of flow regime and hydrodynamic forces generated by a gliding North Atlantic right whale (Eubalaena glacialis)

Accurate estimates of drag on marine animals are required to investigate the locomotive cost, propulsive efficiency, and the impacts of entanglement if the animal is carrying fishing gear. In this study, we performed computational fluid dynamics analysis of a 10 m (length over all) right whale to obtain baseline measurements of drag on the animal. Swimming speeds covering known right whale speed range (0.125 m/s to 8 m/s) were tested. We found a weak dependence between drag coefficient and Reynolds number. At a swimming speed of 2 m/s, we analyzed the boundary layer thicknesses, the flow regimes, and drag components. We found the thickest boundary layer at the lateral sides of the peduncle, whereas the boundary layer thickness over the outer part of the flukes was less than 1.7 cm. Laminar flow occurred over the anterior ~0.6 LoA and turbulent flow from ~0.8 LoA to the fluke notch. On the surfaces of the flukes outside of the body wake region, flow was laminar. Our most significant finding is that the drag coefficient (0.0071–0.0059) of a right whale for swimming speeds ranging from 0.25 m/s to 2 m/s is approximately twice that of many previous estimates for cetaceans.     

Changes in North Atlantic right whale (Eubalaena glacialis) cow–calf association times and use of the calving ground: 1993–2005

Like most mysticetes, North Atlantic right whale cows generally separate from their calves on their feeding grounds within a year. Right whale life history data from 1993 to 2005 were analyzed to determine the duration of cow/calf associations and where the pair separated. A change occurred with the 2001 cows; 71% of those available stayed with their calves into the second year and this behavior remained elevated for several years. Less experienced cows, independent of their age, were more likely to extend their associations. The occurrence of cow/yearling associations was not related to the length of the cow's previous interbirth interval, used as a proxy for cow condition, but the hypothesis that body condition impacts how long cows nurse their young could not be adequately tested. Seventy-seven percent of the observed cow/yearling pairs also returned to the calving ground, a substantial physiological investment given the 1,450 km plus migration and the fact that they fast there, indicating that factors other than nutrition also influenced the cow's behavior. The concurrent increase in juveniles in the shallow waters of the winter calving grounds may afford naive whales greater protection from predators or provide a social benefit that improves their overall fitness.     

Quantification and genetic profiling of DNA isolated from free-floating feces of the North Atlantic right whale (Eubalaena glacialis)

Fecal analysis from the highly endangered North Atlantic right whale provides valuable information about health and reproductive parameters of individual animals. Genetically profiling the feces facilitates this connection when the sample originator is unknown. Although genetic analysis of feces collected in terrestrial systems has become well established, genetic studies of cetacean DNA are rare. Here, the use of free‐floating feces as a source of right whale DNA and the reliability of the genotypes produced are examined. On average, fecal extracts yielded 25 ng of DNA/mg dry weight, but less than 1% was right whale DNA. Although all samples were amplified using genus‐specific mitochondrial control region primers, the quantity of right whale DNA present was over estimated when compared to amplifications using nuclear primers. No correlation was found between the quantity of right whale DNA recovered and the duration the sample sat in the water. Composite microsatellite profiles from multiple amplifications of 28 fecal samples of known origin were consistent with profiles of the same individuals obtained from skin biopsies, however, the rate of allelic dropout varied depending on the amount of right whale DNA added. A screening and genotyping protocol for reliable genetic profiling based on fecal DNA quantification is presented.     

Rope trauma,sedation, disentanglement,and monitoring‐tag associated lesions in a terminally entangled North Atlantic right whale (Eubalaena glacialis)

A chronically entangled North Atlantic right whale, with consequent emaciation was sedated, disentangled to the extent possible, administered antibiotics, and satellite tag tracked for six subsequent days. It was found dead 11 d after the tag ceased transmission. Chronic constrictive deep rope lacerations and emaciation were found to be the proximate cause of death, which may have ultimately involved shark predation. A broadhead cutter and a spring‐loaded knife used for disentanglement were found to induce moderate wounds to the skin and blubber. The telemetry tag, with two barbed shafts partially penetrating the blubber was shed, leaving barbs embedded with localized histological reaction. One of four darts administered shed the barrel, but the needle was found postmortem in the whale with an 80º bend at the blubber‐muscle interface. This bend occurred due to epaxial muscle movement relative to the overlying blubber, with resultant necrosis and cavitation of underlying muscle. This suggests that rigid, implanted devices that span the cetacean blubber muscle interface, where the muscle moves relative to the blubber, could have secondary health impacts. Thus we encourage efforts to develop new tag telemetry systems that do not penetrate the subdermal sheath, but still remain attached for many months.     

The use of machine learning to detect foraging behaviour in whale sharks: a new tool in conservation

In this study we present the first attempt at modelling the feeding behaviour of whale sharks using a machine learning analytical method. A total of eight sharks were monitored with tri-axial accelerometers and their foraging behaviours were visually observed. Our results highlight that the random forest model is a valid and robust approach to predict the feeding behaviour of the whale shark. In conclusion this novel approach exposes the practicality of this method to serve as a conservation tool and the capability it offers in monitoring potential disturbances of the species.     

Small changes in timing of breeding among subarctic passerines over a 32‐year period

Many bird populations in temperate regions have advanced their timing of breeding in response to a warming climate in recent decades. However, long‐term trends in temperature differ geographically and between seasons, and so do responses of local breeding populations. Data on breeding bird phenology from subarctic and arctic passerine populations are scarce, and relatively little data has been recorded in open‐nesting species. We investigated the timing of breeding and its relationship to spring temperature of 14 mainly open‐nesting passerine species in subarctic Swedish Lapland over a period of 32 years (1984–2015). We estimated timing of breeding from the progress of post‐juvenile moult in mist‐netted birds, a new method exploring the fact that the progress of post‐juvenile moult correlates with age. Although there was a numerical tendency for earlier breeding in most species (on average ?0.09 days/year), changes were statistically significant in only three species (by ?0.16 to ?0.23 days/year). These figures are relatively low compared with what has been found in other long‐term studies but are similar to a few other studies in subarctic areas. Generally, annual hatching dates were negatively correlated with mean temperature in May. This correlation was stronger in long‐distance than in short‐distance migrants. Although annual temperatures at high northern latitudes have increased over recent decades, there was no long‐term increase in mean temperature in May over the study period at this subarctic site. This is probably the main reason why there were only small long‐term changes in hatching dates.     

Phenological overlap of interacting species in a changing climate: an assessment of available approaches

Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long‐term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long‐term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate‐induced phenological shifts has focused on terrestrial pairwise resource–consumer interactions, especially those between plants and insects.     

Estimated calf and perinatal mortality in western North Atlantic right whales (Eubalaena glacialis)

Reduced reproductive success has contributed to lack of recovery of the endangered western North Atlantic right whale (Eubalaena glacialis). Here we examined the specific life history period from just before birth through the first year to estimate calf and perinatal losses between 1989 and 2003. The lower bound estimate (17 mortalities from 208 calving events) included documented calf mortalities and presumed deaths from serious injury or disappearance from the sighting record. The upper bound estimated potential calf losses from females with delayed first parturition (>10 yr) and shortened (2 yr) or lengthened (≥4 yr) calving intervals, if the female migrated to the calving ground during these intervals. Because cows were sighted in the calving ground predominantly in years when they were available to calve, adult females sighted there in a possible calving year without a calf were assumed to have experienced a perinatal loss. Twenty-eight potential perinatal losses were detected, bringing the upper bound of calf and perinatal mortality to 45 (3.0 calves/yr). The high frequency of lengthened calving intervals in E. glacialis suggests that abortion and neonatal losses are contributing to lower reproductive success compared to Southern Hemisphere right whales (Eubalaena australis).     

Long‐term mark‐and‐recapture study of a freshwater mussel reveals patterns of habitat use and an association between survival and river discharge

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