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Unravelling the complex reproductive tactics of male humpback whales: an integrative analysis of paternity, age, testosterone, and genetic diversity
Abstract
How the underlying forces of sexual selection impact reproductive tactics including elaborate acoustic displays in cetaceans remains poorly understood. Here, I combined 26 years (1995-2020) of photo-identification, behavioural, (epi)genetic, and endocrine data from an endangered population of humpback whales (New Caledonia), to explore male reproductive success, age, physiology, and population dynamics over almost a third of the lifespan of a humpback whale. First, I conducted a paternity analysis on 177 known mother-offspring pairs and confirmed previous findings of low variation in reproductive success in male humpback whales. Second, epigenetic age estimates of 485 males revealed a left-skewed population age structure in the first half of the study period that became more balanced in the second half. Further, older males (> 23 years) more often engaged in certain reproductive tactics (singing and escorting) and were more successful in siring offspring once the population age structure stabilised, suggesting reproductive tactics and reproductive success in male humpback whales may be age-dependent. Third, using enzyme immunoassays on 457 blubber samples, I observed a seasonal decline in male testosterone in the population over the breeding season. Testosterone levels appeared highest during puberty, then decreased and levelled off at the onset of maturity, yet were highly variable at any point during the breeding season and across males of all ages. Lastly, I investigated the influence of genetic diversity at the major histocompatibility complex (MHC) class I and class IIa (DQB and DRB-a) on patterns of male reproductive success in humpback whales. Mating pairs shared fewer alleles than expected under random mating at MHC class I and IIa, thus, providing evidence of an MHC-mediated female mate choice in humpback whales. This thesis provides novel, critical insights into the evolutionary consequences of commercial whaling on the demography, patterns of reproduction and sexual selection of exploited populations of baleen whales.
Humpback whale song is a culturally transmitted behavior. Human language, which is also culturally transmitted, has statistically coherent parts whose frequency distribution follows a power law. These properties facilitate learning and may therefore arise because of their contribution to the faithful transmission of language over multiple cultural generations. If so, we would expect to find them in other culturally transmitted systems. In this study, we applied methods based on infant speech segmentation to 8 years of humpback recordings, uncovering in whale song the same statistical structure that is a hallmark of human language. This commonality, in two evolutionarily distant species, points to the role of learning and cultural transmission in the emergence of properties thought to be unique to human language.
The major histocompatibility complex (MHC) is a highly polymorphic gene family that is crucial in immunity, and its diversity can be effectively used as a fitness marker for populations. Despite this, MHC remains poorly characterised in non‐model species (e.g., cetaceans: whales, dolphins and porpoises) as high gene copy number variation, especially in the fast‐evolving class I region, makes analyses of genomic sequences difficult. To date, only small sections of class I and IIa genes have been used to assess functional diversity in cetacean populations. Here, we undertook a systematic characterisation of the MHC class I and IIa regions in available cetacean genomes. We extracted full‐length gene sequences to design pan‐cetacean primers that amplified the complete exon 2 from MHC class I and IIa genes in one combined sequencing panel. We validated this panel in 19 cetacean species and described 354 alleles for both classes. Furthermore, we identified likely assembly artefacts for many MHC class I assemblies based on the presence of class I genes in the amplicon data compared to missing genes from genomes. Finally, we investigated MHC diversity using the panel in 25 humpback and 30 southern right whales, including four paternity trios for humpback whales. This revealed copy‐number variable class I haplotypes in humpback whales, which is likely a common phenomenon across cetaceans. These MHC alleles will form the basis for a cetacean branch of the Immuno‐Polymorphism Database (IPD‐MHC), a curated resource intended to aid in the systematic compilation of MHC alleles across several species, to support conservation initiatives.
Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella, an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.
Sperm whales’ reproductive strategies are centered around their extreme sexual dimorphism, both in morphology and behavior. Females are much smaller than males and are highly social. Females live in stable, matrilineally based social units with communal care of calves, including cooperative defense and allonursing. In contrast, male sperm whales are large nearly solitary nomads. Males disperse from their natal social unit and move toward the poles, where they eat and grow almost three times larger than females. Males’ great ranges span across and between ocean basins, allowing global genetic connectivity. As they rove the warm waters where females concentrate, mature males avoid each other; physical aggression on the breeding grounds is rarely observed. Instead, males may rely on powerful acoustic displays to establish dominance over potential competitors and provide females with an honest quality signal. Associations between sexually mature males and groups of females tend to be transitory. Disproportionate mating success of some males is suggested by evidence of paternal relatedness within female social units. Sperm whale mothers provide a substantial investment of time and energy to calves, resulting in the slowest reproductive rate among cetaceans. The peculiar characteristics of sperm whale mating systems reflect the evolutionary interplay between habitat structure, predation risk, sociality, and reproduction. A convergence of reproductive biology between sperm whales and African elephants likely results from similarities in these ecological pressures. Despite sperm whales being one of the most studied cetaceans, much remains unknown about their reproductive strategies. Most of what we know comes from whaling data and long-term observational and modeling studies. The rapid advances in technology for behavioral and physiological studies at sea can refine our understanding of these elusive deep-diving animals’ social, mating, and caring systems and the extent to which these vary across oceans.
While a variety of reproductive tactics are readily witnessed in odontocetes, such behaviors can be far more elusive in baleen whales and in some cases are yet to be observed. This leads researchers to study the reproductive behaviors in mysticetes using a variety of research methods which have improved greatly in recent years. Genetics and genomics tools can provide valuable information on maternity, paternity, age, diversity, and kinship, while acoustic tools can provide new insights into the function of sexual displays such as song. In this chapter, we explore what is known about reproductive strategies and tactics of baleen whales, with a particular focus on the comparatively well-studied right whales ( Eubalaena spp.) and humpback whale ( Megaptera novaeangliae ). Finally, we showcase that by integrating multiple data types, we can explore the interactions between anatomy, physiology, reproductive success, age, population dynamics, and acoustic displays to better understand the mating systems of baleen whales.
Non-conceptive sexual behavior (NCSB) is phylogenetically widespread, having been documented in 35 of the 87 extant cetacean species, but function and form of NCSB have not been studied in comparative manner. Many cetacean species engage in NCSB across a wide variety of settings and contexts (e.g., play, sexual, affiliative). NCSB includes both social and non-social sexual behaviors, such as non-social masturbation on the environment or social same-sex thrusting toward a conspecific, but importantly, none of the behavior described as NCSB affords reproduction. While these two general categories encompass all sexual actions, the behaviors are diverse depending on species, social structure, and sex of the individual being observed. Social sexual behavior presumably has individual or social benefits. This chapter organizes what is known about NCSB in cetaceans by summarizing NCSB repertoires from peer-reviewed literature and discussing proposed functions (e.g., practice for reproduction, attracting opposite-sex mates, reducing the reproductive opportunities of same-sex conspecifics, reinforcing dominance relationships, alliance formation, reconciliation, and social tension reduction). Further, the form or behavioral repertoire, the sex of the individuals engaging in NCSB, the environment observed in, and whether NCSB was present or absent in general are noted from each of the articles reviewed. Overall, NCSB behavior observed across species shares similar elements (e.g., thrusting, lateral presentations) in both Mysticeti and Odontoceti. NCSB tends to be more prevalent among sexually immature compared to sexually mature individuals. Additionally, NCSB is more prevalent between male conspecifics compared to females when animals engage in same-sex NCSB. Interspecific NCSB has also been reported for a number of species. While most reports come from toothed whales, the limited observations of baleen whales have also found that many species engage in NCSB, making it likely that NCSB is included in the behavioral repertoire of most cetacean species. NCSB likely aids in forming and maintaining social relations and/or in the development of sexual repertoires in cetaceans, not unlike what has been proposed for primates. We hope this chapter sparks interest in comparative studies of NCSB and sheds light on the similarities of NCSB across species.
Humpback whales (Megaptera novaeangliae) in Southeast Alaska have been studied for over 50 years, and are largely considered a recovery success since the cessation of commercial whaling. Reproductive physiology is an important factor to consider in studying population health and can provide important insights into the drivers contributing to population abundance fluctuations. Validated assays for progesterone and testosterone were used on blubber biopsies from humpback whales (N = 33 whales, 71 samples) near Juneau, Alaska, in 2020 and 2021. Long-term sighting histories were used to confirm detected pregnancies with calf sightings the following year. Blubber samples were divided into two seasonal bins (early and late summer). Pregnant females sampled in both early and late summer of both 2020 and 2021 showed elevated progesterone concentrations compared to other reproductive states (p
Aging, often considered a result of random cellular damage, can be accurately estimated using DNA methylation profiles, the foundation of pan-tissue epigenetic clocks. Here, we demonstrate the development of universal pan-mammalian clocks, using 11,754 methylation arrays from
our Mammalian Methylation Consortium, which encompass 59 tissue
types across 185 mammalian species. These predictive models estimate mammalian tissue age with high accuracy (r > 0.96). Age deviations correlate with human mortality risk, mouse somatotropic axis mutations and caloric restriction. We identified specific cytosines with methylation levels that change with age across numerous species. These sites, highly enriched
in polycomb repressive complex 2-binding locations, are near genes implicated in mammalian development, cancer, obesity and longevity. Our findings offer new evidence suggesting that aging is evolutionarily conserved and intertwined with developmental processes across all mammals.
Epigenetic approaches for estimating the age of living organisms are revolutionizing studies of long‐lived species. Molecular biomarkers that allow age estimates from small tissue biopsies promise to enhance studies of long‐lived whales, addressing a fundamental and challenging parameter in wildlife management. DNA methylation (DNAm) can affect gene expression, and strong correlations between DNAm patterns and age have been documented in humans and nonhuman vertebrates and used to construct “epigenetic clocks”. We present several epigenetic clocks for skin samples from two of the longest‐lived cetaceans, killer whales and bowhead whales. Applying the mammalian methylation array to genomic DNA from skin samples we validate four different clocks with median errors of 2.3–3.7 years. These epigenetic clocks demonstrate the validity of using cytosine methylation data to estimate the age of long‐lived cetaceans and have broad applications supporting the conservation and management of long‐lived cetaceans using genomic DNA from remote tissue biopsies.
Recent studies have shown behavioural plasticity in mating strategies can increase a population’s ability to cope with anthropogenic impacts. The eastern Australian humpback whale population was whaled almost to extinction in the 1960s (~200 whales) and has recovered to pre-whaling numbers (>20,000 whales). Using an 18-year dataset, where the population increased from approximately 3,700 to 27,000 whales, we found that as male density increased over time, the use of mating tactics shifted towards more males engaging in non-singing physical competition over singing. Singing was the more successful tactic in earlier post-whaling years whereas non-singing behaviour was the more successful tactic in later years. Together, our study uncovers how changes in both local, and population-level male density resulted in a shift in the frequency, and fitness pay-off, of alternative mating tactics in a wild animal. This individual-level plasticity in male humpback whale mating tactics likely contributed to minimising their risk of extinction following a dramatic change in their social landscape due to whaling.
The krill surplus hypothesis of unlimited prey resources available for Antarctic predators due to commercial whaling in the 20th century has remained largely untested since the 1970s. Rapid warming of the Western Antarctic Peninsula (WAP) over the past 50 years has resulted in decreased seasonal ice cover and a reduction of krill. The latter is being exacerbated by a commercial krill fishery in the region. Despite this, humpback whale populations have increased but may be at a threshold for growth based on these human‐induced changes. Understanding how climate‐mediated variation in prey availability influences humpback whale population dynamics is critical for focused management and conservation actions. Using an 8‐year dataset (2013–2020), we show that inter‐annual humpback whale pregnancy rates, as determined from skin‐blubber biopsy samples (n = 616), are positively correlated with krill availability and fluctuations in ice cover in the previous year. Pregnancy rates showed significant inter‐annual variability, between 29% and 86%. Our results indicate that krill availability is in fact limiting and affecting reproductive rates, in contrast to the krill surplus hypothesis. This suggests that this population of humpback whales may be at a threshold for population growth due to prey limitations. As a result, continued warming and increased fishing along the WAP, which continue to reduce krill stocks, will likely impact this humpback whale population and other krill predators in the region. Humpback whales are sentinel species of ecosystem health, and changes in pregnancy rates can provide quantifiable signals of the impact of environmental change at the population level. Our findings must be considered paramount in developing new and more restrictive conservation and management plans for the Antarctic marine ecosystem and minimizing the negative impacts of human activities in the region.
Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These ‘epigenetic clocks’ present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species‐specific epigenetic clock based on skin tissue samples for a population of Indo‐Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine‐guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long‐term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave‐One‐Out‐Cross‐Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi‐species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species‐specific clocks can have superior performance over those of multi‐species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long‐term observational data for free‐ranging Indo‐Pacific bottlenose dolphins worldwide.
The sperm whale lives in most deep ice-free waters of the globe. It was targeted during two periods of whaling peaking in the 1840’s and 1960’s. Using a habitat suitability model, we extrapolated estimates of abundance from visual and acoustic surveys to give a global estimate of 736,053 sperm whales (CV = 0.218) in 1993. Estimates of trends in the post-whaling era suggest that: whaling, by affecting the sex ratio and/or the social cohesion of females, reduced recovery rates well after whaling ceased; preferentially-targeted adult males show the best evidence of recovery, presumably due to recruitment from breeding populations; several decades post-whaling, sperm whale populations not facing much human impact are recovering slowly, but populations may be declining in areas with substantial anthropogenic footprint. A theta-logistic population model enhanced to simulate spatial structure and the non-removal impacts of whaling indicated a pre-whaling population of 1,949,698 (CV = 0.178) in 1710 being reduced by whaling, and then then recovering a little to about 844,761 (CV = 0.209) in 2022. There is much uncertainty about these numbers and trends. A larger population estimate than produced by a similar analysis in 2002 is principally due to a better assessment of ascertainment bias.
The use of song as a reproductive display is common in the animal kingdom; however, for many taxa, little is known of song ontogeny. Male humpback whales produce elaborate songs on low latitude breeding grounds in winter and begin to sing on high latitude feeding grounds in late summer, yet songs from the two locations are rarely compared. Seasonal song ontogeny in western North Atlantic humpback whales was explored by comparing songs recorded in high latitude feeding grounds (Canada in spring 2016 and fall 2016 to winter 2017) with songs recorded in a low latitude breeding ground (Dominican Republic in winter and spring 2017). High-quality song samples were selected, and every phrase annotated. Song theme order, song duration, and number of phrase repetitions were compared across samples. The most variability in theme order was found between November and December in the Canadian recordings, a phase in song ontogeny that may be important for learning. Song duration gradually increased, via an increase in phrase repetitions, through the breeding season, before peaking in the Dominican Republic between January and March. A comparison to oscine bird seasonal song ontogeny revealed many similarities, highlighting potentially similar physiological processes between humpback whales and songbirds.
The rapidly growing understanding of the Omura’s whale (Balaenoptera omurai) is an example of how the drive to explore and discover has been enhanced by advances in technology, particularly in bioacoustics. This combination of inspiration and technology has allowed exploration of topics that had been out of reach for many scientists. The Omura’s whale was first described in 2003 from a handful of specimens, and for a decade remained an enigmatic “ghost” species without confirmation of live sightings, let alone any understanding of its ecology. After the chance discovery of a population off northwest Madagascar, the stage was set for the exploration of a new species. In five short years, through the application of recent advancements in bioacoustics, molecular genetics, and satellite telemetry, we may have a better understanding of the Omura’s whale (or at least one of its populations) than of many other cetaceans. In this chapter, I describe new information gathered on Omura’s whales off Madagascar during 2013–2017, with a focus on its singing behavior. Combined with growing information from other sites around the world, I make inferences about the species’ behavioral patterns and describe the potential for innovative research that could be conducted on this enigmatic species.KeywordsOmura’s whale
Balaenoptera omurai
BalaenopteridaePassive acoustic monitoringSpatiotemporal distributionSongSinging behaviorGeographic variationBreeding ecology
The major histocompatibility complex (MHC) plays a central role in the vertebrate adaptive immune system and has been of long‐term interest in evolutionary biology. While several protocols have been developed for MHC genotyping, there is a lack of transparent and standardized tools for downstream analysis of MHC data. Here, we present the r package mhctools and demonstrate the use of its functions to (i) assist accurate MHC genotyping from high‐throughput amplicon‐sequencing data, (ii) infer functional MHC supertypes using bootstrapped clustering analysis, (iii) identify segregating MHC haplotypes from family data, and (iv) analyse functional and genetic distances between MHC sequences. We employed mhctools to analyse MHC class I (MHC‐I) amplicon data of 559 great reed warblers (Acrocephalus arundinaceus). We identified 390 MHC‐I alleles which clustered into 14 functional supertypes. A phylogenetic analysis and analyses of positive selection suggested that the MHC‐I alleles belong to several distinct functional groups. We furthermore identified 107 segregating haplotypes among 116 families, and found substantial variation in diversity with 4–21 MHC‐I alleles and 3–13 MHC‐I supertypes per haplotype. Finally, we show that the great reed warbler haplotypes harboured combinations of MHC‐I supertypes with greater functional divergence than observed in simulated populations of possible haplotypes, a result that is in accordance with the divergent allele advantage hypothesis. Our study demonstrates the power of mhctools to support genotyping and analysis of MHC in non‐model species, which we hope will encourage broad implementation among researchers in MHC genetics and evolution.
Climate change directly impacts the foraging opportunities of cetaceans (e.g. lower prey availability), leads to habitat loss, and forces cetaceans to move to other feeding grounds. The rise in ocean temperature, low prey availability and loss of habitat can have severe consequences for cetacean survival, particularly those species that are already threatened or those with a limited habitat range. In addition, it is predicted that the concentration of contaminants in aquatic environments will increase owing to Arctic meltwater and increased rainfall events leading to higher rates of land-based runoff in downstream coastal areas. These persistent and mobile contaminants can bioaccumulate in the ecosystem, and lead to ecotoxicity with potentially severe consequences on the reproductive organs, immune system and metabolism of marine mammals. There is a need to measure and assess the cumulative impact of multiple stressors, given that climate change, habitat alteration, low prey availability and contaminants do not act in isolation. Human-caused perturbations to cetacean foraging abilities are becoming a pervasive and prevalent threat to many cetacean species on top of climate change-associated stressors. We need to move to a greater understanding of how multiple stressors impact the metabolism of cetaceans and ultimately their population trajectory.
This article is part of the theme issue ‘Nurturing resilient marine ecosystems’.
Variation in individual demographic rates can have large consequences for populations. Female reproductive skew is an example of structured demographic heterogeneity where females have intrinsic qualities that make them more or less likely to breed. The consequences of reproductive skew for population dynamics are poorly understood in non-cooperatively breeding mammals, especially when coupled with other drivers such as poaching. We address this knowledge gap with population viability analyses using an age-specific, female-only, individual-based, stochastic population model built with long-term data for three Kenyan populations of the Critically Endangered eastern black rhino ( Diceros bicornis michaeli). There was substantial reproductive skew, with a high proportion of females not breeding or doing so at very low rates. This had a large impact on the projected population growth rate for the smaller population on Ol Jogi. Moreover, including female reproductive skew exacerbates the effects of poaching, increasing the probability of extinction by approximately 70% under a simulated poaching pressure of 5% offtake per year. Tackling the effects of reproductive skew depends on whether it is mediated by habitat or social factors, with potential strategies including habitat and biological management respectively. Investigating and tackling reproductive skew in other species requires long-term, individual-level data collection.
The cost of reproduction greatly affects a species’ life history strategy. Baleen whales exhibit some of the fastest offspring growth rates in the animal kingdom. We quantified the energetic cost of gestation for southern right whales (Eubalaena australis) by combining whaling catch records of pregnant females with photogrammetry data on southern right whale mothers and calves from two breeding grounds in Argentina and Australia. The relationship between calf birth size and maternal length was determined from repeated measurements of individual females before and after giving birth. Fetal growth was determined from generalized linear models fitted to fetal length data from whaling operations between 1961 and 1967. Fetal length was converted to volume and mass, using the volume‐to‐length relationship of newborn southern right whales calves, and published tissue composition and energy content estimates. Fetal maintenance costs (heat of gestation) and the energy content of the placenta were predicted from published relationships and added to the fetal growth cost to calculate the total cost of gestation. Our findings showed that fetal growth rates and birth size increased linearly with maternal length, with calves being born at ∼35% maternal length. Fetal length increased curvilinearly through gestation, which resulted in an exponential increase in fetal volume and mass. Consequently, the cost of gestation was very low during the first (0.1% of total cost) and second trimester (4.9%), but increased rapidly during the last trimester (95.0%). The heat of gestation incurred the highest cost for pregnant females (73.8%), followed by fetal growth (21.2%) and the placental energy content (5.0%).
Key points
Baleen whales exhibit some of the fastest fetal growth rates in the animal kingdom. Despite this, the energetic cost of gestation is largely unknown, as well as the influence of maternal body size on fetal growth rates and calf birth sizes.
We combined historical whaling records and drone photogrammetry data to determine fetal growth rates and birth sizes in southern right whales (Eubalaena australis), from which we estimated the cost of gestation.
Calf birth size, and consequent fetal growth rates, increased positively with maternal body size.
The cost of gestation was negligible for southern right whale females during the first two trimesters, but increased rapidly during the last trimester.
These results show that late gestation incurs a significant cost for baleen whale females, and needs to be accounted for in bioenergetic models.
Despite their enormous size, whales make their living as voracious predators. To catch their much smaller, more maneuverable prey, they have developed several unique locomotor strategies that require high energetic input, high mechanical power output and a surprising degree of agility. To better understand how body size affects maneuverability at the largest scale, we used bio-logging data, aerial photogrammetry and a high-throughput approach to quantify the maneuvering performance of seven species of free-swimming baleen whale. We found that as body size increases, absolute maneuvering performance decreases: larger whales use lower accelerations and perform slower pitch-changes, rolls and turns than smaller species. We also found that baleen whales exhibit positive allometry of maneuvering performance: relative to their body size, larger whales use higher accelerations, and perform faster pitch-changes, rolls and certain types of turns than smaller species. However, not all maneuvers were impacted by body size in the same way, and we found that larger whales behaviorally adjust for their decreased agility by using turns that they can perform more effectively. The positive allometry of maneuvering performance suggests that large whales have compensated for their increased body size by evolving more effective control surfaces and by preferentially selecting maneuvers that play to their strengths.
Unoccupied aerial system (UAS) technologies applied to health assessments of large whales can have positive implications for progressive management. We focused on the collection of cetacean respiratory blow samples for endocrine, DNA profiling, microbial metabarcoding, and metagenomics analyses, with the goal of improving management of large whale populations. Blow samples were collected from humpback ( Megaptera novaeangliae, n = 109 samples analyzed), blue ( Balaenoptera musculus, n = 21 samples analyzed), and killer whale ( Orcinus orca, n = 1 sample analyzed) species, as well as the responses of the whales to the collection of their blow by UAS. Endocrine analyses were validated for 5 steroid hormones in humpback whales and 4 hormones in blue whales. For DNA profiling, we attempted to extract and amplify nuclear and mitochondrial DNA, resulting in sequencing of mtDNA haplotypes for 54% of samples, identification of sex for 39%, and individual identification by microsatellite genotyping for 17%. The DNA profiles of 2 of the blow samples from humpback whales were matched to a DNA register for this regional population. Metagenomic and microbial metabarcoding classifications found a diverse number of bacteria, eukaryotes, and viruses in humpback whale blow. Although a significant portion of classifications were found in both seawater and blow, several of the most abundant organisms were present only in blow samples, suggesting they are true members of the respiratory microbiome. A comprehensive integration of laboratory‐based approaches using noninvasive UAS collection technologies could become an important management tool for health assessments of large cetaceans, especially for species listed as endangered. The addition of individual and population‐level health assessments to currently practiced stewardship of large whales, renders them as excellent sentinels of ocean health. © 2021 The Wildlife Society.
Humpback whale song is an extraordinary example of vocal cultural behaviour. In northern populations, the complex songs show long-lasting traditions that slowly evolve, while in the South Pacific, periodic revolutions occur when songs are adopted from neighbouring populations and rapidly spread. In this species, vocal learning cannot be studied in the laboratory, learning is instead inferred from the songs' complexity and patterns of transmission. Here, we used individual-based cultural evolutionary simulations of the entire Southern and Northern Hemisphere humpback whale populations to formalize this process of inference. We modelled processes of song mutation and patterns of contact among populations and compared our model with patterns of song theme sharing measured in South Pacific populations. Low levels of mutation in combination with rare population interactions were sufficient to closely fit the pattern of diversity in the South Pacific, including the distinctive pattern of west-to-east revolutions. Interestingly, the same learning parameters that gave rise to revolutions in the Southern Hemisphere simulations gave rise to evolutionary patterns of cultural evolution in the Northern Hemisphere populations. Our study demonstrates how cultural evolutionary approaches can be used to make inferences about the learning processes underlying cultural transmission and how they might generate emergent population-level processes.
This article is part of the theme issue ‘Vocal learning in animals and humans’.
Epigenetics, specifically DNA methylation, allows for the estimation of animal age from blood or remotely sampled skin. This multi-tissue epigenetic age estimation clock uses 110 longitudinal samples from 34 Navy bottlenose dolphins (Tursiops truncatus), identifying 195 cytosine-phosphate-guanine sites associated with chronological aging via cross-validation with one individual left out in each fold (R2 = 0.95). With a median absolute error of 2.5 years, this clock improves age estimation capacity in wild dolphins, helping conservation efforts and enabling a better understanding of population demographics.
Most of our knowledge on reproductive biology of gray whales dates back to scientific research conducted during commercial whaling in the late 1950s and 1960s. The goal of the present study was to provide updated insights on reproductive physiology of gray whales, using progesterone and testosterone as biomarkers. We measured hormone concentrations using enzyme immunoassay (EIA) techniques in blubber biopsies collected from 106 individual whales from March to November over a span of 12 years (2004–2016) between California and Alaska. We found testosterone concentrations in males to increase significantly with age (P = 0.03). Adult males showed significantly elevated testosterone concentrations when sampled in the fall compared to the summer (P = 0.01), likely indicating physiological preparation for mating. We measured testosterone concentrations in females of different age classes, but no statistical differences were found. We found significantly higher progesterone concentrations in pregnant females compared to non-pregnant females and adult males (P< 0.001), indicating progesterone is a valid biomarker for pregnancy in gray whales. Both female and male calves had elevated progesterone concentrations, suggesting maternal transfer via lactation. We fit a mixture of two normal distributions to progesterone data from all non-calf females to identify clusters of high and low progesterone and estimated the probability of being pregnant for whales of unknown reproductive status. With this approach we identified likely pregnant and non-pregnant animals. This study represents an important milestone on reproductive profiles in this population, that can be used to estimate more accurate and precise reproductive parameters to be used for better understanding population dynamics of gray whales.
Age is a fundamental parameter in wildlife management as it is used to determine the risk of extinction, manage invasive species, and regulate sustainable harvest. In a broad variety of vertebrates species, age can be determined by measuring DNA methylation. Animals with known ages are initially required during development, calibration, and validation of these epigenetic clocks. However, wild animals with known ages are frequently difficult to obtain. Here, we perform Monte‐Carlo simulations to determine the optimal sample size required to create an accurate calibration model for age estimation by elastic net regression modelling of cytosine‐phosphate‐guanine methylation data. Our results suggest a minimum calibration population size of 70, but ideally 134 individuals or more for accurate and precise models. We also provide estimates to the extent a model can be extrapolated beyond a distribution of ages that was used during calibration. The findings can assist researchers to better design age estimation models and decide if their model is adequate for determining key population attributes.
The development of a precise blood or skin tissue DNA Epigenetic Aging Clock for Odontocete (OEAC) would solve current age estimation inaccuracies for wild odontocetes. Therefore, we determined genome-wide DNA methylation profiles using a custom array (HorvathMammalMethyl40) across skin and blood samples (n = 446) from known age animals representing nine odontocete species within 4 phylogenetic families to identify age associated CG dinucleotides (CpGs). The top CpGs were used to create a cross-validated OEAC clock which was highly correlated for individuals (r = 0.94) and for unique species (median r = 0.93). Finally, we applied the OEAC for estimating the age and sex of 22 wild Norwegian killer whales. DNA methylation patterns of age associated CpGs are highly conserved across odontocetes. These similarities allowed us to develop an odontocete epigenetic aging clock (OEAC) which can be used for species conservation efforts by provide a mechanism for estimating the age of free ranging odontocetes from either blood or skin samples.
The bowhead whale is the only baleen whale endemic to the Arctic and is well adapted to this environment. Bowheads live near the polar ice edge for much of the year and although sea ice dynamics are not the only driver of their annual migratory movements, it likely plays a key role. Given the intrinsic variability of open water and ice, one might expect bowhead migratory plasticity to be high and linked to this proximate environmental factor. Here, through a network of underwater passive acoustic recorders, we document the first known occurrence of bowheads overwintering in what is normally their summer foraging grounds in the Amundsen Gulf and eastern Beaufort Sea. The underlying question is whether this is the leading edge of a phenological shift in a species' migratory behaviour in an environment undergoing dramatic shifts due to climate change.
Monitoring the body condition of free-ranging marine mammals at different life-history stages is essential to understand their ecology as they must accumulate sufficient energy reserves for survival and reproduction. However, assessing body condition in free-ranging marine mammals is challenging. We cross-validated two independent approaches to estimate the body condition of humpback whales ( Megaptera novaeangliae ) at two feeding grounds in Canada and Norway: animal-borne tags ( n = 59) and aerial photogrammetry ( n = 55). Whales that had a large length-standardized projected area in overhead images (i.e. whales looked fatter) had lower estimated tissue body density (TBD) (greater lipid stores) from tag data. Linking both measurements in a Bayesian hierarchical model to estimate the true underlying (hidden) tissue body density (uTBD), we found uTBD was lower (−3.5 kg m ⁻³ ) in pregnant females compared to adult males and resting females, while in lactating females it was higher (+6.0 kg m ⁻³ ). Whales were more negatively buoyant (+5.0 kg m ⁻³ ) in Norway than Canada during the early feeding season, possibly owing to a longer migration from breeding areas. While uTBD decreased over the feeding season across life-history traits, whale tissues remained negatively buoyant (1035.3 ± 3.8 kg m ⁻³ ) in the late feeding season. This study adds confidence to the effectiveness of these independent methods to estimate the body condition of free-ranging whales.
Introduction
DNA methylation data facilitate the development of accurate molecular estimators of chronological age, or ‘epigenetic clocks.’ We present a robust epigenetic clock for the beluga whale, Delphinapterus leucas, developed for an endangered population in Cook Inlet, Alaska, USA.
Methods and Results
We used a custom methylation array to measure methylation levels at 37,491 cytosine‐guanine sites (CpGs) from skin samples of dead whales (n = 67) whose chronological ages were estimated based on tooth growth layer groups. Using these calibration data, a penalized regression model selected 23 CpGs, providing an R² = 0.92 for the training data; and an R² = 0.74 and median absolute age error = 2.9 years for the leave one out cross‐validation. We applied the epigenetic clock to an independent data set of 38 skin samples collected with a biopsy dart from living whales between 2016 and 2018. Age estimates ranged from 11 to 27 years. We also report sex correlations in CpG data and describe an approach of identifying the sex of an animal using DNA methylation.
Discussion
The epigenetic estimators of age and sex presented here have broad applications for conservation and management of Cook Inlet beluga whales and potentially other cetaceans.
Since the first studies on bowhead whale singing behaviour, song variations have been consistently reported. However, there has been little discussion regarding variability in bowhead whale singing display and its ecological significance. Unlike the better studied humpback whales, bowhead whales do not appear to share songs at population level, but several studies have reported song sharing within clusters of animals. Over the winter season 2013–2014, in an unstudied wintering ground off Northeast Greenland, 13 song groups sharing similar hierarchical structure and units were identified. Unit types were assessed through multidimensional maps, showing well separated clusters corresponding to manually labelled units, and revealing the presence of unit subtypes. Units presented contrasting levels of variability over their acoustic parameters, suggesting that bowhead whales keep consistency in some units while using a continuum in values of frequency, duration and modulation parameters for other unit types. Those findings emphasise the need to account for variability in song analysis to better understand the behavioural ecology of this endangered species. Additionally, shifting from song toward units or phrase-based analysis, as it has been suggested for humpback whales, offers the opportunity to identify and track similarities in songs over temporal and geographical scales relevant to population monitoring.
Climate change has resulted in physical and biological changes in the world's oceans. How the effects of these changes are buffered by top predator populations, and therefore how much plasticity lies at the highest trophic levels, are largely unknown. Here endocrine profiling, longitudinal observations of known individuals over 15 years between 2004 and 2018, and environmental data are combined to examine how the reproductive success of a top marine predator is being affected by ecosystem change. The Gulf of St. Lawrence, Canada, is a major summer feeding ground for humpback whales (Megaptera novaeangliae) in the North Atlantic. Blubber biopsy samples (n = 185) of female humpback whales were used to investigate variation in pregnancy rates through the quantification of progesterone. Annual pregnancy rates showed considerable variability, with no overall change detected over the study. However, a total of 457 photo‐identified adult female sightings records with/without calves were collated, and showed that annual calving rates declined significantly. The probability of observing cow–calf pairs was related to favourable environmental conditions in the previous year; measured by herring spawning stock biomass, Calanus spp. abundance, overall copepod abundance and phytoplankton bloom magnitude. Approximately 39% of identified pregnancies were unsuccessful over the 15 years, and the average annual pregnancy rate was higher than the average annual calving rate at ~37% and ~23% respectively. Together, these data suggest that the declines in reproductive success could be, at least in part, the result of females being unable to accumulate the energy reserves necessary to maintain pregnancy and/or meet the energetic demands of lactation in years of poorer prey availability rather than solely an inability to become pregnant. The decline in calving rates over a period of major environmental variability may suggest that this population has limited resilience to such ecosystem change.
Animals use acoustic signals for communication, implying that the properties of these signals can be under strong selection. The acoustic adaptation hypothesis predicts that species in dense habitats emit lower‐frequency sounds than those in open areas because low‐frequency sounds propagate further in dense vegetation than high‐frequency sounds. Signal frequency may also be under sexual selection because it correlates with body size and lower‐frequency sounds are perceived as more intimidating. Here, we evaluate these hypotheses by analysing variation in peak song frequency across 5,085 passerine species (Passeriformes). A phylogenetically informed analysis revealed that song frequency decreases with increasing body mass and with male‐biased sexual size dimorphism. However, we found no support for the predicted relationship between frequency and habitat. Our results suggest that the global variation in passerine song frequency is mostly driven by natural and sexual selection causing evolutionary shifts in body size rather than by habitat‐related selection on sound propagation.
Male fin whales sing by producing 20 Hz pulses in regular patterns of inter-note intervals. While singing, fin whales may also alternate the frequency ranges of their notes. Different song patterns have been observed in different regions of the world's oceans. New song patterns suddenly emerging in an area have been hypothesized to either be indicators of new groups of whales in the area or signs of cultural transmission between groups. Since the status of fin whales around Hawaii is unknown and visual surveys are expensive and difficult to conduct in offshore areas, passive acoustic monitoring has been proposed as a way to monitor these whales. We used passive acoustic recordings from an array of 14 hydrophones to analyze the song patterns of 115 fin whale encounters made up of 50,034 unique notes off Kauai, Hawaii from 2011 to 2017. Fin whale singing patterns were more complicated than previously described. Fin whales off Hawaii sang in five different patterns made of two 20 Hz note types and both singlet and doublet inter-note interval patterns. The inter-note intervals present in their songs were 28/33 s for the lower frequency doublet, 30 s for the lower frequency singlet, 17/24 s for the higher frequency doublet, 17 s for the higher frequency singlet, and 12/20 s for the doublet that alternated between both note types. Some of these song patterns were unique to these fin whales in Hawaiian waters, while others were similar to song patterns recorded from fin whales off the U.S. west coast. Individual fin whales often utilized several different song patterns which suggests that multiple song patterns are not necessarily indicators of different individuals or groups. The dominant song pattern also changed over these years. Cultural transmission may have occurred between fin whales in Hawaiian waters and off the U.S. west coast, which has resulted in similar songs being present at both locations but on lagged timescales. Alternatively, groups occupying the Hawaiian waters could shift over time resulting in different song patterns becoming dominant. This work has implications for the population structure and behavior of Hawaii fin whales.
Between 1991 and 1997 right whales were studied on their wintering grounds on the southern coastline of Australia, predominantly at theHead of the Great Australian Bight, where over 350 individuals have been identified. The observed mean inter-calf interval for females was3.33±0.10 years (±SE, n = 57) at the Head of the Bight and 3.64±0.13 years (±SE, n = 117) in the wider Australian population. Wheninter-calf intervals of six or more years were excluded, the mean intervals became 3.28±0.09 years (±SE, n = 56) and 3.28±0.06 years (±SE,n = 107), respectively. Inter-calf intervals of two years were recorded following the early death of a neonate on two separate occasions andthe implications of these ‘shortened’ intervals and of calvings that were not observed are discussed. The mean age at which yearlings wereobserved to be fully weaned was calculated to be 365±8 days (±SE, n = 18) from the estimated birth dates of individual calves andsubsequent associations, or lack of them, between the yearlings and their cows the following year. A total of 108 movements greater than200km in length were made by individual whales. The mean within-year movement was 730±84 km, made over 34±4 days (±SE, n = 18),whilst the mean between-year movement was 1,036±45km (±SE, n = 87), made over a mean interval of 3.3±0.3 years (±SE, n = 90). Thenumber and direction of coastal movements observed suggest that the right whales off southern Australia comprise a single populationwhich may undertake an almost circular, anti-clockwise migration to the south of the Australian continent. A significantly greaterproportion of females displayed a level of between-year fidelity to the Head of the Bight aggregation area (92%, n = 61) than did males(68%, n = 19) or whales of unknown sex (63%, n = 8).
Culture, defined as shared behavior or information within a community acquired through some form of social learning from conspecifics, is now suggested to act as a second inheritance system. Cultural processes are important in a wide variety of vertebrate species. Birdsong provides a classic example of cultural processes: cultural transmission, where changes in a shared song are learned from surrounding conspecifics, and cultural evolution, where the patterns of songs change through time. This form of cultural transmission of information has features that are different in speed and form from genetic transmission. More recently, culture, vocal traditions, and an extreme form of song evolution have been documented in cetaceans. Humpback whale song “revolutions,” where the single population-wide shared song type is rapidly replaced by a new, novel song type introduced from a neighboring population, represents an extraordinary example of ocean basin-wide cultural transmission rivaled in its geographic extent only by humans. In this review, we examine the cultural evolutions and revolutions present in some birdsong and whale song, respectively. By taking a comparative approach to these cultural processes, we review the existing evidence to understand the similarities and differences for their patterns of expression and the underlying drivers, including anthropogenic influences, which may shape them. Finally, we encourage future studies to explore the role of innovation vs. production errors in song evolution, the fitness information present in song, and how human-induced changes in population sizes, trajectories, and migratory connections facilitating cultural transmission may be driving song revolutions.
The acoustic behavior of minke whaleMinke whale populations worldwide has been a mystery for the better part of the twentieth century. Several likely biological sound sources such as the ‘boing’‘boing’ recorded in the North Pacific, or the ‘bio-duck’‘bioduck’ with its ubiquitous distribution in the Southern Ocean, had been described by seafarers since the middle of the twentieth century. However, the origin of these sounds could only be revealed once technological advances allowed scientists to simultaneously acoustically and visually track the elusiveElusive species producing them. The current data show that, like other baleen whales, most minke whaleMinke whale populations produce long song sequences presumably in a reproductive contextReproductive context. Over the past two decades, by extending our listening efforts into remote habitats, we have learned much about minke whalesMinke whale and can assume that many more mysteries are waiting to be unlocked.
Right whales have a long history of interactions with humans, being arguably the first commercially hunted species of whale. There are currently three recognized species of right whales including the North Pacific right whale (Eubalaena japonica), the North Atlantic right whale (Eubalaena glacialis), and the southern right whale (Eubalaena australis). The conservation status of these three species varies. Both of the northern hemisphere species are endangered and have only a few hundred individuals remaining, while the southern hemisphere species have multiple growing breeding populations that include thousands of individuals. Studies of right whale behavioral ecology and acoustic communication started in the 1960s and 1970s with studies off Massachusetts for North Atlantic right whales, and off Argentina for southern right whales. Behavioral studies of the less accessible North Pacific right whales have lagged behind, with most information on their behavior being published in the past 20 years. All right whale species share similarities in their acoustic repertoires, with a stereotyped contact call, the upcall and a loud broadband impulsive sound, the gunshot, being described for all species. Beyond these stereotyped sound types, right whales all share a graded repertoire of signals that range from pulsive to tonal in structure. Sound type usage varies by the behavioral context of the communication, and sound types appear to serve similar behavioral roles in all three species. Studies across species suggest that there are differences in sound production that reflect the sex and age class of the signaling individual. Additional studies have demonstrated behavioral responses of right whales to exposure from noise in their environments. Emerging areas for future research include the expansion of the use of passive acoustic monitoring to aid in the conservation of these whales.KeywordsRight whale
Eubalaena
Baleen whaleBehaviorEndangered speciesAcousticsPassive acoustic monitoring
Baleen whale migration emerges as a foundational theme of cetacean behavioral ecology and the relationships that bind humans and whales together. From facilitating the culmination of the great human migration many centuries ago, to their roles as ecosystem service providers, baleen whales have influenced the path of human history. With a focus on modern technologically enabled insights, we provide an overview of what scientists currently know about the spatial and temporal distribution of baleen whales and their migratory behaviors. Although a coarse model of seasonally paced north–south migration generally applies, a deeper analysis reveals the remarkable diversity of baleen whale migrations. Some species, including gray whales (Eschrichtius robustus), migrate relatively close to shore; others, including humpback whales (Megaptera novaeangliae), tend to migrate across ocean basins. Some species, including Bryde’s whales (Balaenoptera edeni), appear to largely reside in middle to low-latitude ecosystems, relatively removed from cold, high-latitude water. In contrast, bowhead whales (Balaena mysticetus) remain within Arctic ecosystems all year, and others, including Omura’s whales (Balaenoptera omurai), may not migrate at all. The scientific focus to date has largely been on population-specific studies of where whales go, what their behaviors are, and when they undertake their migrations. Thus, there remains much to be learned, particularly regarding why baleen whales migrate and how they navigate during their long-distance migrations. Technological innovations such as satellite tags and passive acoustics have revolutionized our understanding of baleen whale behavioral ecology and ethology, and technology will continue to play a critical role in advancing the science of baleen whale migration.KeywordsBaleen whaleMigrationTelemetrySatellite trackingPassive acousticsMigratory behaviorMovement behaviorAcoustic behaviorOrientationNavigation
Baleen whalesBaleen whales are specialized to find and exploit preyPrey that form dense patches seasonally within broad ocean areas. Most populations have an annual reproductive cycleAnnual reproductive cycle that separates their breeding seasonBreeding season from their feeding seasonFeeding season, often with long-distance migrationsMigrationsbetween feedingFeedingand breedingBreeding areas. The longest bond we know of for most baleen whale species is the mother-calf bondMother-calf bond. CalvesCalve suckle for five to seven months in most species and wean by the next feeding seasonFeeding season. The species whose social behavior has been most studied is the humpback whaleHumpback whale, enabled by their distribution, which often is near shore, and their individually distinctive natural markings. Some humpback whalesHumpback whalefeedingFeeding on mobile prey form stable groupsStable group where each individual learnsLearn specific roles to perform coordinated group foragingGroup foraging. Aside from these groups, which may last for many years, most baleen whale groups are reported to be fluid with few strong associations between individuals other than mother and calfCalf. However, most researchers define whale groups in terms of the number of whales that are close enough to be sighted within a certain distance of one another. Sound propagates so well underwater that whale sounds can be heardHeard at distances of tens to hundreds of kilometers away. This means that whales may be able to maintain contact over much greater ranges than are usually assessed by human observers—they may form long-range “heards”Heard in addition to shorter range “herdsHerd.” The social organization of whales during the breeding seasonBreeding season is structured in part by songsSong—acoustic reproductive advertisement displays. The potential scale of “heards”Heard is indicated by the ability of scientists to track one singingSingingblue whaleBlue whale for 43 days as it swam > 1700 km. Scientists will start to develop a fuller understanding of the social organization of baleen whales when they apply methods that can make observations and test hypotheses over the temporal and spatial scales at which baleen whales move and communicate.
Understanding reproductive physiology in mysticetes has been slowed by the lack of repeated samples from individuals. Analysis of humpback whale baleen enables retrospective hormone analysis within individuals dating back 3-5 years before death. Using this method, we investigated differences in four steroid hormones involved in reproduction and mating during confirmed pregnant and non-pregnant periods in two female humpback whales (Megaptera novaeangliae) with known reproductive histories based on sightings and necropsy data. Cortisol, corticosterone, testosterone, and estradiol concentrations were determined via enzyme immunoassay using subsamples of each baleen plate at 2 cm intervals. There were no significant differences in cortisol or corticosterone during pregnancy when compared to non-pregnancy (inter-calving interval), but there were significant differences between the two whales in average glucocorticoid concentrations, with the younger whale showing higher values overall. For testosterone, levels for the younger female peaked at parturition in one pregnancy, but also had spikes during non-pregnancy. The older female had three large spikes in testosterone, one of which was associated with parturition. Estradiol had large fluctuations in both whales but had generally lower concentrations during non-pregnancy than during pregnancy. There were peaks in estradiol before each pregnancy, possibly coinciding with ovulation, and peaks coinciding with the month of parturition. Both estradiol and testosterone could be useful for determining ovulation or impending birth. Using baleen to investigate retrospective steroid hormone profiles can be used for elucidating long-term patterns of physiological change during gestation.
Lay summary:
Case studies of two pregnant humpback whales whose hormones were analyzed in baleen may illuminate when humpback whales ovulate, gestate, and give birth. These physiological metrics could assist in accurate population growth assessments and conservation of the species. This study shows that baleen hormone analysis can be a useful tool for understanding whale reproductive physiology.
In order to exploit seasonally favourable habitats for feeding and breeding, humpback whales Megaptera novaeangliae undertake one of the longest migrations in the animal kingdom. Stored energy is crucial for a successful migration, but few studies have investigated the relationship between migration timing and body condition in baleen whales. Using unmanned aerial vehicles, we quantified the body condition of east Australian humpback whales. We collected data on 513 individuals (48 calves, 166 juveniles, 251 adults, and 48 lactating females) during their northbound and southbound migrations between June and October 2020. For adults and juveniles, we explored the loss of body condition between migration direction (north versus south) as well as the relationship of migration timing (day of year) and body condition. We found a significant loss in body condition between the northbound and southbound migrations for both adults (9.8%) and juveniles (18.3%). However, migration timing did not influence body condition for either reproductive class. Cow/calf pairs were analysed using relative calf length (percentage of maternal length) as a proxy for days postpartum. We found a positive curvilinear relationship between migration timing and calf body condition. However, lactating females showed no relationship between migration timing and body condition. Whilst body condition is important for capital breeding whales, the lack of a correlation found for adults and juveniles suggests that body condition is not the main driver of migration timing from feeding or breeding grounds. However, calf body condition may be a significant factor for the migration timing of cow/calf pairs.
Animal body size and growth patterns play important roles in shaping the life history of species. Baleen whales include the largest animals on the planet, with somatic growth costs expected to be substantial. We used unmanned aerial vehicle photogrammetry and long-term
individual sighting histories from photo identification (1991−2019) to estimate the cost of somatic growth for southern right whales (SRWs) Eubalaena australis. A Richards length-at-age growth model was developed, based on 161 calves, 20 yearlings, 1 juvenile and 23 adults, ranging in age from newborn to 27 yr. Predicted lengths were 4.7 m at birth, 12.5 m at minimum age of first parturition (6 yr) and an asymptotic length of 14.3 m. A volume-at-age curve was estimated from the body volume versus length relationship, and converted to a mass-at-age curve, using data on body tissue composition of North Pacific right whales E. japonica (n = 13). The energetic cost of
growth was estimated using published estimates of tissue lipid and protein concentrations. The cost of growth for SRWs (in MJ d−1) was 2112 at birth, 544 at 4 mo, 314 at 1 yr (~weaning age), 108 at 5 yr (minimum age of sexual maturity), 51.5 at 10 yr and 5.2 at 30 yr. The cumulative cost to age 30 was 764.3 GJ, but varied widely (458−995 GJ) depending on the tissue energy content. Our estimates represent a healthy SRW population, and provide a baseline to investigate individual and population level impacts of anthropogenic disturbance (including climate change).
Darwin's theory of sexual selection fundamentally changed how we think about sex and evolution. The struggle over mating and fertilization is a powerful driver of diversification within and among species. Contemporaries dismissed Darwin's conjecture of a "taste for the beautiful" as favoring particular mates over others, but there is now overwhelming evidence for a primary role of both male and female mate choice in sexual selection. Darwin's misogyny precluded much analysis of the "taste"; an increasing focus on mate choice mechanisms before, during, and after mating reveals that these often evolve in response to selection pressures that have little to do with sexual selection on chosen traits. Where traits and preferences do coevolve, they can do so whether fitness effects on choosers are positive, neutral, or negative. The spectrum of selection on traits and preferences, and how traits and preferences respond to social effects, determine how sexual selection and mate choice influence broader-scale processes like reproductive isolation and population responses to environmental change.
Creating a baseline understanding of communicative signals and perceptual abilities is imperative for gaining insight into a species' life history. This is especially relevant for at-risk species, as it can aid in monitoring and conservation efforts. Marine mammals communicate predominately through acoustic modalities for a variety of functions, including foraging and reproduction. The acoustic signals produced by marine mammals, and their ability to perceive signals produced by conspecifics, are directly impacted by the level of ambient noise in the underwater environment in which they inhabit. Modern ocean noise levels are considerably louder than historical levels, and noise is therefore considered to be a threat to acoustically communicating marine mammal species. This review summarizes the documented acoustic signals, hearing abilities, and responses to sound of a critically endangered baleen whale, the North Atlantic right whale (Eubalaena glacialis), highlights gaps in the current body of literature, and identifies priorities for future research.
Polygynous mating systems are common among terrestrial mammals, and are typically characterized by a skewed operational sex ratio, competition among males for females, variation in reproductive success (RS) among males and the evolution of alternative mating tactics. Little is known about mating systems of marine taxa due to difficulty of observing individual behavior and determining paternity. Humpback whales are thought to be polygynous with differences in reproduction among males related to alternative mating tactics. However, there is currently a lack of data on male RS. I tested predictions regarding male RS in humpback whales using the molecular assessment of paternity in a population in the Mexican Pacific. Parentage analysis for 125 mother-calf pairs and a sample of 297 males, genotyped for 13 polymorphic microsatellite loci, resulted in putative paternities for 30--50% of calves. The distribution of male RS deviated significantly from a random mating model. However, reproductive skew was not severe: most fathers sired only one calf and no male was assigned more than three calves. Most current measures of skew report a single value that describes variance but not the underlying statistical distribution of RS. I describe a procedure to estimate reproductive skew in terms of the population-wide distribution of RS using a simple simulation of mating, specifically for datasets with incomplete sampling of offspring and males. For my humpback whale data, I found that the best-fit mating model was an approximation of a gamma distribution, only slightly skewed beyond a Poisson distribution. Therefore I conclude that this population has a polygynous mating system, but without the large variation in male RS typical of some systems of this type. Successful males employed diverse mating tactics, with significant variation among the proportions of four alternative tactics used by fathers. Most fathers were observed to employ all tactics to varying degrees, although some appeared to favor specific tactics such as physically competing for females or escorting mothers. The latter, a tactic generally considered low pay-off, may in fact contribute significantly to overall male RS. Implications of these new findings are discussed in relation to the current understanding of this mating system.
The goal of the present study was to complement existing data of testosterone and progesterone in blue whale (Balaenoptera musculus) blubber from the eastern North Pacific Ocean to evaluate effects of seasonality and location on these hormones, and to better assess reproductive status of individuals. Physiological parameters regarding reproduction are fundamental for describing population dynamics, and hormones can be a valid tool to estimate those for wildlife populations. In this study, blubber tissue was validated for testosterone and progesterone assays. Hormone concentrations were measured in 69 (35 males and 34 females) blubber samples from live (n= 66) and stranded (n= 3) animals collected between 2002 and 2016 from a known winter reproductive ground in the Gulf of California (GoC) and summer feeding areas along the United States West Coast (USWC), specifically off the states of California and Oregon. Results were combined with sighting histories as a tool to determine reproductive status of individual whales. Testosterone concentrations in adult male blue whales were significantly higher (p< 0.05) in blubber biopsies sampled off the USWC between the months of June and November compared to those sampled in the GoC between February and April. Elevated testosterone concentrations likely indicate physiological preparation for reproductive activity while the animals were present off the USWC. Progesterone concentrations were significantly elevated in pregnant females, confirming progesterone as an indicator of pregnancy in blue whales. Probabilities of being pregnant were estimated for adult females with unknown sighting histories based on progesterone concentrations. Testosterone in females was detected and measured only in pregnant whales suggesting its biosynthesis or metabolism is altered during gestation. These results provide updated and new information on the reproductive cycle of blue whales in the eastern North Pacific, posing new milestones to better estimate the timing of the mating season for this endangered population.
Recovery rates for baleen whales that were decimated by exploitation vary between species and populations. Age determination is critical for the understanding of recovery trends and population structure, but determining age in free‐ranging individuals remains challenging. Recent research has suggested that the methylation level of some genes in skin samples may provide age determinations with accuracy. We selected nine CpG sites from three genes (TET2, CDKN2A, and GRIA2) and analyzed them in 40 skin samples from known‐age individuals pertaining to two different populations of fin whales from the North Atlantic. We observed significant correlations with age in five CpG sites. We used three of these CpG sites to perform an epigenetic age estimation. Predictions had a standard deviation of 2.94, but regression between observed and predicted ages showed a clear underestimation for older fin whales. For further development, we suggest: (1) screening for new CpG sites associated with age that exhibit higher variability between individuals, and (2) including older animals whenever the sampling allows it. We also observed subtle, but significant differences between the two populations studied in one of the CpG sites (TET2_CpG + 21). We attributed these differences to genetic differences or to the dissimilar environments that affect both populations.
An understanding of the functional morphology of the bowhead whale continues to have significance for population management. This chapter first examines the anatomical features of the bowhead whale reproductive system, with an emphasis on the female. This is followed by a consideration of the functional parameters of the female reproductive cycle, testicular function in the male, and the age at sexual maturity in both sexes.