Another method that may increase understanding of gray whale reproduction is assessment of reproductive hormones. In other baleen whale species, reproductive hormone assays of blubber biopsies and fecal samples have been used to determine pregnancy rates (e.g., Atkinson et al. 2020), better understand the physiological stress levels associated with different reproductive states (e.g., Valenzuela-Molina et al. 2018), and infer patterns of male reproductive seasonality based on trends in testosterone levels over time (e.g., Vu et al. 2015; Carone et al. 2019). Reproductive hormones have also been measured in whale blow samples (e.g., Burgess et al. 2018). In addition, analysis of reproductive hormones in baleen, while only attainable from dead whales, provides the opportunity to track the recent reproductive histories of individuals, increasing understanding of calving intervals, age of sexual maturity, and timing of the breeding season (Hunt et al. 2016, 2022; Lowe et al. 2021). In gray whales, analysis of reproductive hormone concentrations in fecal samples and blubber biopsies have focused on evaluating how reproductive hormones vary with age, reproductive status, season, and life history stage (Lemos et al. 2020, Melica et al. 2021). Although analysis thus far has been limited to a single sample, Hunt et al. (2017) demonstrated that reproductive hormones can be detected in gray whale baleen. These studies highlight the potential utility of reproductive hormone assessments to provide insight into gray whale reproduction.

#### 21.5.2 Linking Reproductive and Acoustic Behavior

Bioacoustic tags, capable of collecting acoustic data as well as information on acceleration and depth, and unoccupied aerial vehicles (UAVs or drones) equipped with video, photographic, and other sensors (e.g., thermal) are examples of rapidly developing technologies that can further expand the understanding of reproductive behavior in gray whales (Ramos et al. 2023, this book). When paired together, underwater calls of gray whales that are linked to their behavior at the surface can be collected simultaneously, including data from breeding and other social-sexual groups. Alternatively, a recent study using two drones, one capable of landing on the water near whales to collect acoustic recordings and the other for obtaining aerial imagery of whale behavior, demonstrated the feasibility and utility of this research approach (Frouin-Mouy et al. 2020).

Acoustic communication plays a vital role in the social interactions of many marine mammal species, but gray whale acoustic behavior and vocalizations are just beginning to be evaluated. While the S1 call described in Sect. 21.4.2 above seems associated with gray whale reproduction, its specific role has yet to be determined. The statistical approach taken by Ponce et al. (2012) could be designed to count the number of S1 calls detected, not only in relation to the total number of whales but to the two demographic classes: single whales and female–calf pairs. If the S1 call is indeed a social contact call used mostly by single whales that are actively trying to breed, its presence should be correlated with the presence of single whales but uncorrelated with the presence of female–calf pairs, when observed across multiple seasons.

# 21.5.3 Role of Wintering Lagoon Entrance Aggregations in Reproduction

Whalers in the nineteenth century first reported aggregations of gray whales at the wintering lagoon entrances off the Pacific coast of the Baja California peninsula, Mexico, leading to the eventual discovery and exploitation of the high concentrations of whales inside of the lagoons proper. In recent decades, reports from scientists and observations of local fishers and eco-tourism operators confirm that gray whales actively enter and leave the winter lagoon interiors and form aggregations at the entrance points (Jones and Swartz 1984; Jones 1990). These entrance point aggregations of whales are difficult to observe due to their distance from the shore and high surf where they occur, precluding detailed study and evaluation of the importance of these areas to gray whale reproductive behavior in the winter. A new generation of affordable "fixed-wing" and "hovering" drones have good potential to serve as effective and safe platforms to observe gray whale sexual and mating behavior in these portions of their winter range.

Acknowledgments We express our thanks to Dara Orbach and Bernd Würsig for providing the opportunity to contribute information on gray whale reproduction to this volume. We also thank Jim Darling for his review and constructive comments that improved an earlier draft. We all have those that inspired and encouraged us to pursue marine science, and on whose shoulders we will always gratefully stand. Collectively we acknowledge and thank our teachers, mentors, and colleagues, past and present, for fueling our desire to better understand the natural history and behavior of cetaceans, and particularly of the gray whale. We are hopeful that our endeavors will inspire new generations of marine scientists to follow and carry out novel lines of investigation and that they will be as fortunate as we have been to experience the exhilaration of discovery and the satisfaction of sharing their findings with their colleagues and with the world. Finally, we are grateful to the gray whales for providing the opportunity to learn from these most remarkable cetaceans of their lives in the ocean environment.

#### References

maturity in Eastern Gray Whales. Presented to the International Whaling Commission Scientific Committee Paper SC/62/BRG2. Available from http://www.iwcoffice.org/

eastern North Pacific gray whales, despite previous detection of mitochondrial differences. J Cetacean Res Manag 13(2):97–104

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# Chapter 22 Bowhead Whale Reproductive Strategies

William R. Koski, J. Craig George, and Bernd Würsig

Abstract Bowhead whales (Balaena mysticetus) have adopted growth and reproductive strategies to survive in a challenging environment where no other mysticete whales reside. They grow slowly, become sexually mature at around 25 years (later than other mammals), and do not give birth until they have sufficient energy reserves for the best possible chance of survival of the calf to weaning and long-term survival of the mother. To compensate for late maturity and long inter-birth intervals, some seem to have the capability to live to 200+ years of age, making them the longestlived mammal known to date. Bowhead whale males have large testes per body size, and it is hypothesized that the basic polygynandrous system of females and males mating with multiple partners per estrous cycle allows for males to not compete violently against each other. Instead, they use sperm competition by volume of sperm for enhanced capability to father as many offspring as possible.  Details of sperm volume, potential variabilities of sperm viabilities, and actual paternities are unknown, but some patterns can be inferred from the closely related right whales with similar morphologies.

Keywords Birthing period · Calf dependency · Calving · Calving intervals · Gestation · Growth rates · Mating behavior · Sexual maturity · Sperm competition · Surface-active groups

J. C. George Department of Wildlife Management, North Slope Borough, Utqiaġvik, AK, USA

B. Würsig Texas A&M University at Galveston, Galveston, TX, USA

https://doi.org/10.1007/978-3-031-35651-3\_22 © The Author(s) 2023 B. Würsig, D. N. Orbach (eds.), Sex in Cetaceans,

W. R. Koski (✉) LGL Limited, King City, ON, Canada e-mail<EMAIL_ADDRESS>
#### 22.1 Introduction

Living entities have evolved to maximize their long-term survival including selecting and specializing in niches where they can effectively compete with other species in their habitats. Bowhead whales (Balaena mysticetus) have taken this specialization to an extreme level by living year-round in a challenging geographic region where no other closely related species reside. To ensure survival of individuals in this isolated and unpredictable environment, bowhead whales have adopted conservative reproductive and growth strategies. They can live to be 200+ years old, and sexual and physical maturity is delayed compared to other species. They delay raising a calf for decades, producing young only when their energy reserves are sufficient to maximize survival of a calf and its mother (George et al. 2021b). Growth in young whales emphasizes the head and feeding apparatus at the expense of postcranial skeletal structures. The size of the head relative to the body and the length of baleen plates is greater than most other mysticetes so that they can efficiently feed on small low-density invertebrates. This chapter describes what we currently know about the above strategies with respect to reproduction in this slowgrowing and long-lived mammal.

#### 22.2 Age and Length at Sexual Maturity

Bowhead whale growth is slow compared to other cetaceans (Koski et al. 1993; George et al. 2011). They appear to forgo growth in favor of storing energy reserves that allow them to survive long periods with a negative energy balance (i.e., during periods when they use more energy for normal activities than they obtain from feeding) (George et al. 2021a, b). Male bowhead whales mature at a length of 12–13 m when they are about 25 years old (O'Hara et al. 2002; Tarpley et al. 2016). Female bowhead whales become sexually mature at 14.2 m when they are estimated to be about 25 years old (Koski et al. 1992) based on samples from harvested whales collected up to 1992 (Tarpley et al. 2016). More recent harvest data, however, have identified sexually mature females 12.6–13.9 m, suggesting that there may be a trend toward sexual maturity at a younger age in recent years (Tarpley et al. 2021). The appearance of smaller sexually mature females in the harvest at Utqiaġvik (formerly Barrow), Alaska, was thought to be due to more favorable feeding conditions that have resulted from increases in productivity with longer and more extensive areas of open water each year. However, young female bowhead whales migrate past Utqiaġvik later than older females (Koski et al. 1993). Thus, the appearance of small sexually mature female bowhead whales in the harvest in recent years may be due to the migration being earlier. Koski et al. (1993) identified bowhead whales as small as 12.3 m with calves in the Eastern Beaufort Sea during summer in the early to mid-1980s when the smallest pregnant females harvested at Utqiaġvik were 14.2 m (Tarpley et al. 2016). For comparison with bowhead whales, North Atlantic right whales (Eubalaena glacialis) become sexually mature much earlier at about 10 years (Knowlton et al. 1994; Rolland et al. 2005; NMFS 2022), blue whales (Balaenoptera musculus) at 10 years for females and 12 years for males (Sears 2002; NAMMCO 2020a), fin whales (Balaenoptera physalis) at 7–12 years for females and 6–10 for males (Aguilar 2002; NAMMCO 2022a), humpback whales (Megaptera novaeangliae) at 5–15 years (Clapham 2002, 2018; Gabriele et al. 2007; Best 2011), sei whales (Balaenoptera borealis) at 8–10 years (Horwood 2002; NAMMCO 2020b), and gray whales (Eschrichtius robustus) at 6–12 years (Jones and Swartz 2002; Swartz et al. 2023, this book).

George et al. (2011) examined the question of whether corpora accumulation is, on average, the same for left and right ovaries. They found no significant difference in the number of corpora in each ovary; however, they did find large variation where the number of corpora could vary by up to 12 scars. Ohsumi (1964) examined corpora-accumulation curves and noted baleen whales were "Type 1" ovulators where right and left ovaries attained maturity at the same time and overall accumulation rates were similar. Bowheads appear to be consistent with Ohsumi's characterization of baleen whales. George et al. (2021b) examined sex differences in the maximum body lengths of bowhead whales. They noted that among several hundred whales harvested since 1972, the 10 longest were females. The maximum reliable lengths for females were about 19 m while the maximum lengths for males were 16–17 m. However, maximum lengths of whales measured photogrammetrically are about 8.2% shorter than those of hunter-harvested whales, as there appears to be some "stretching" when whales are hauled onto shore (George et al. 2004). The longest whale measured in photographs was 17.57 m (Koski et al. 2006).

Reproductive senescence is poorly understood for bowhead whales, mainly because relatively few whales over 100 years have been aged. The current method of aging old bowhead whales relies on aspartic acid racemization (AAR; Wetzel et al. 2017), with exact age estimates insecure. There is no evidence for reproductive senescence in males.  There is, however, information on possible senescence in female bowhead whales based on examination of reproductive tracts and age estimates using AAR (Wetzel et al. 2017). The oldest female that has been harvested with a fetus was estimated to be 121 years old. The three oldest female bowhead whales that were harvested had AAR age estimates of 133, 139, and 149. They all had small, regressed corpora albicantia and no corpora lutea, suggesting that they were reproductively quiescent or senescent (George et al. 2021b). Although these age estimates are not precise, they suggest that at least some female bowhead whales might be able to produce calves over a period of about 100 years.

#### 22.2.1 Mating Period and Location

Bowhead whale behaviors associated with mating have been seen throughout the year, but a recent study (Fortune et al. 2017) found that some of this behavior is associated with stimulation of the epidermis during the molt, and therefore is not a reproductive activity (Würsig and Koski 2021). In particular, close physical presence and rubbing with pectoral appendages seem to assist with removal of dead skin and stimulation of new skin. Most calves are born over a very short period from late April to late May (Koski et al. 1993, 2008), suggesting that most successful mating occurs over a short time as well. On April 13 and 14, 2005, hundreds to perhaps one thousand or more bowhead whales were seen and photographed mating in the Bering Sea north of St. Lawrence Island (Figs. 22.1 and 22.2; Koski et al. 2005). Activities associated with mating have also been reported in autumn (Koski et al. 1993; Würsig and Clark 1993), but it is unknown how much of this behavior might be non-procreative. This behavior may have been rubbing relative to sloughing skin stimulation or it may have been non-reproductive mating attempts (Würsig and Koski 2021; Ham et al. 2023, this book; Würsig et al. 2023, this book). Several

Fig. 22.1 Mating behavior in a group of bowhead whales photographed on April 13 and 14, 2005, ~50 km north of St Lawrence Island, Bering Sea. The female (upside down at the top of image) is being aggressively pursued by several males. The resting whales on the lower right are probably males "catching their breath."  However, integration of variable lines of observational information and information below on gestation suggests that the main mating period is in late March to mid-April when most Bering, Chukchi, and Beaufort seas (BCB) bowhead whales are in the Bering Sea (Reese et al. 2001; Koski et al. 2005). Data from examination of ovaries suggest that female bowhead whales may ovulate up to three times during a reproductive cycle if the first and second ovulations do not result in a pregnancy (Tarpley et al. 2016). This likely explains observations of smaller numbers of whales engaged in mating activities during mid-April to late May than in early-to-mid April.

In addition to an overall decline in the number of whales seen engaged in mating activities later in the spring, the group sizes of whales engaged in mating behaviors have declined from early April to late May. Carroll and Smithhistler (1980) described mating behavior during May near Utqiaġvik and typical group sizes have been 4–6 animals. Similarly, during the many years of ice-based whale census observations west of Utqiaġvik, mating behavior was described by observers on several occasions and group size has been 4–6 animals as seen from the ice edge. The smaller group sizes seen during May (4–6 animals) than during April (up to 24+; Koski et al. 2005) could be due to waning sexual behavior because most ovulating sexually mature female bowhead whales have become pregnant during their first ovulation, which appears to be in early-to-mid April.

#### 22.2.2 Mate Selection

A hypothesis advanced by Kenagy and Trombulak (1986) and summarized for mammals in general by Clutton-Brock (2016) relates large testis size (generally by weight) to body size/weight in polygynous/polygynandrous (multi-mate) mating systems. This hypothesis is likely operating in bowhead whales. Males need a large volume of sperm to mate with as many females as possible during a proscribed mating season. In multi-mate systems, where the females are inseminated by more than one sexual partner, a higher volume of sperm also enhances the likelihood of paternity (Lüpold 2013). This relationship of sperm competition by volume was further advanced for gray whales, right whales, and bowhead whales by Brownell and Ralls (1986; see Gerber and Krützen 2023; Würsig et al. 2023, this book, for a summary for cetaceans); all of these species have large testes relative to their body size. Tarpley et al. (2021) mention that the largest single testis measured so far for a bowhead whale weighed 211 kg and was 1.5 m long. The estimated body mass of that whale was about 54,000 kg, making the testes/body weight 0.0078 (combined testis weight 422/per body weight 54,000). A relatively small number of harvested male bowhead whales had a combined testicular weight over 150 kg (n = 9) and only 5 had combined testes weights over 200 kg. The largest combined weight was 422 kg in a 14.6 m whale. A sexually mature male bowhead whale from the Eastern Canada-West Greenland (EC-WG) stock that was 14.1 m long had a single testis size of 42 kg (Heide-Jørgensen et al. 2012). Spermatozoa volume is massive due to the large size of the epididymis that can rival the testis (Haldiman and Tarpley 1993). Sperm competition can also be at sperm viability level; that is, some sperm will survive longer in the uterus making them more likely to impregnate their mate (Lüpold 2013); this has not been explored in bowhead whales, to our knowledge. In the closely related North Pacific right whale (Eubalaena japonica) the largest combined testes weight of 972 kg was in a 16.3 m whale and the next largest combined weight was 955 kg in a 17.0 m whale. Both whales were from the western North Pacific (Omura et al. 1969).

Very little has been published of the penis of the bowhead, but it is fibroelastic type like that found in most artiodactyls. From our field observations of a few large males, the penis is long (to 3.0 m) and slender (see also Fig. 22.2). As in right whales, penis length in bowheads, as a percentage of total body length, appears to be greater than that of balaenopterids. Little information is available on the morphology of spermatozoa in baleen whales. Tarpley et al. (2021) provide a photograph of spermatozoa from a 16.6 m adult male bowhead whale, but the morphology and size are not provided. The apparently strong physical sperm competition by volume may mean that male bowhead whales are rather indiscriminate in their choice of mates, but aspects of mate selection for both sexes are unknown. We explore mate selection further in the following section on mating behavior.

#### 22.2.3 Mating Behavior

Bowhead whale sexual behavior entails much scramble competition, with males maneuvering to gain access to females, possibly almost always near the surface (Würsig and Clark 1993). In the Bering Sea and near Utqiaġvik, where the water is clear, we saw chasing well below the surface (perhaps to 20–30 m), but we do not know how much farther below the surface it may occur. Similar to observations of right, gray, and humpback whale sexual interactions, there can be many whales involved (mostly males; Figs. 22.1 and 22.2) with at least one female, and much white water being created, making observations by humans as to specifics particularly difficult (Würsig et al. 1993). These interactions are generally termed surfaceactive groups (SAGs), following a definition for humpback whales (Clapham 1996). However, in humpback whales, testes to body size ratios are much smaller than in the apparent sperm competing bowhead whales, and in humpbacks there are very aggressive male–male interactions, termed contest competition Clapham 1996, 2018). In the apparent sperm competitors, while there is swift action, males appear to attempt to outmaneuver each other without much overt aggression (Dines et al. 2015). There is even the (unproven) provocative suggestion that males at times help each other to gain access to females, by one male pushing down on a ventrum (belly)-up female and another attempting to insert his penis (as shown for southern right whales, Eubalaena australis, Payne 1995). If true, this also makes sense for apparent strong sperm competitors; if only by helping each other, each male receives a better chance at inseminating the female.

While males are jostling for position, females tend to hold their breath while ventrum-up, making it difficult for males to mate with them (Würsig et al. 1993). That female inverted behavior is likely to represent a form of female choice, where perhaps the most adroit, experienced, largest, longer-lasting male has a better chance to inseminate the female. When the female needs to breathe, she rolls dorsum-up while rapidly surging ahead and diving, again appearing to evade the males. Würsig et al. (1993) provide several sequential line drawings of SAG activities; also see Figs. 22.1 and 22.2). It is not clear how often female bowhead whales mate with different males, but in southern right whales, the same female has been seen multiple times in different SAGs (Payne 1995; Brown and Sironi 2023, this book); it is unknown whether she is physiologically reproductively active throughout this time. At any rate, sperm competition does not negate the probability of polygynandry in these animals with super-large testes and can presently be hypothesized for bowhead whales. SAGs may also consist at times of bowhead whale male homosexual activity (Finley 1990), as in other whales (Darling 1977 for gray whales; Kraus and Hatch 2001 for northern right whales (Eubalaena glacialis); and Sironi 2004 for southern right whales; see also Brown and Sironi 2023, this book).

Surface-active groups (SAGs) of many males and one to several females (Würsig and Clark 1993; Koski et al. 2005) are "commonly" seen in spring in the Beaufort Sea, but also occur at other times of the year (e.g., Everitt and Krogman 1979; Würsig et al. 1993). It is not known for what reason extra-seasonal apparent matings

Fig. 22.3 Sizes of bowhead whales observed engaged in presumed sexual activity during behavior studies conducted in the Central Beaufort Sea on September 20, 1998. Lengths were determined by aerial photogrammetry conducted using the methods of Koski et al. (1993). Figure prepared by William R. Koski, and used here with permission

or mating attempts occur, but it has been hypothesized that while some of it is homosexual, it may also represent especially young animals learning mating patterns and physical maneuvering needs (Würsig et al. 2023, this book; Fig. 22.3). Not all apparent mating attempts occur in SAGs, and at times (and reported infrequently, probably as it is difficult for humans to witness), apparent mating has been reported for only two or three animals in much more leisurely rolling and touching activities than in SAGs (Würsig et al. 1985). While it is very likely that female bowhead whales mate with multiple males during estrus, this has been confirmed for right whales (Brown and Sironi 2023, this book). In right whales, two males with penises inside one female at the same time have even been reported (Mate et al. 2005 for northern right whales; Würsig 2000 for southern right whales), with strong evidence for competition being at sperm volume level, and perhaps with other physiological advantages. In Würsig (2000), the larger male seemed to be preferred by the female, as she tilted toward the larger male and thereby pulled the smaller male's penis out of her; the larger male went to apparent orgasm, with clear muscular contractions from base toward tip of penis. The gentle-seeming interactions, including caressing by flippers after the mating event, indicate that at least at times female choice may not be simply among several males in large aggregations, but may be more of a one-onone interaction of choice. While the above vignettes are of right whales, the similar large testes and apparent polygynandrous system of bowhead whales allow us to predict—with caution—that multiple mating strategies may also be involved in bowhead whales.

While detailed analyses of bowhead whale sounds and song have not been unequivocally linked with sexual behavior, it is likely that this link exists (Würsig and Clark 1993). Stafford et al. (2012) analyzed bowhead whale song recorded in Fram Strait between Greenland and Svalbard. Song-type calls were initiated in late October, with near-constant singing from late November until early March. Singing occurred somewhat intermittently through March-early April and ended abruptly in late April. While the number of new songs had decreased by March, the highest diversity of different song types occurred in March. It has been speculated that bowhead whale song is a male reproductive display similar to that of humpback whales (Stafford 2022; Eichenberger et al. 2023, this book). Peak singing coincides with the peak breeding/conception period in late March and April (see above) for BCB bowhead whales.

#### 22.2.4 Gestation

The bowhead whale gestation period appears to be slightly more than 1 year based on the main mating period in late March to mid-April and the peak of calving in late April to late May (Koski et al. 1993). This assertion is supported by small embryos (3 cm) and near-term fetuses (366–455 cm) having been found in harvested whales during the spring hunt at Utqiaġvik, Alaska (Tarpley et al. 2016, 2021). Reese et al. (2001) proposed a ~14-month gestation period like the 13.5-month gestation in gray whales (Dale Rice). However, bowhead and gray whale gestation is slightly longer than of blue (10–12 months; Sears 2002; NAMMCO 2020a), fin (11 months; Aguilar 2002; NAMMCO 2022a), and humpback whales (11–12 months; Clapham 2002; NAMMCO 2022b), and considerably longer than sei whales (7 months; Horwood 2002, 2018; NAMMCO 2020b).

#### 22.2.5 Birthing Period and Location

Bowhead whale calves are born in spring during the northward migration from the southwestern Bering Sea to the Eastern Beaufort Sea and mother and calf pass northern Alaska during the latter part of the migration in water with extensive ice cover that is <0 °C (Angliss et al. 1995; Koski et al. 2004, 2008). Although it seems like a stressful time to calve, bowhead whales avoid encounters with their main natural predator, the killer whale (Orcinus orca), and calving occurs a short time before the mothers arrive at prime feeding areas in the Eastern Beaufort Sea (Citta et al. 2015).

The question of how neonates withstand parturition into <0 °C sea water has not been investigated but does not appear to result in mortality of the calf. Based on between-day sightings of recently born calves in mother–calf pairs near Utqiaġvik, it appears that mothers interrupt their migration for a few days after they calve to recover from the stress of calving and to permit calves to become strong enough to migrate (Koski et al. 2004; Arnold Brower, Sr, pers comm to JCG). When mothers and newborn calves begin their journey toward summer feeding areas, the calf has at times been seen to ride on the back of the mother (Würsig et al. 1999). The calf sits on the lower back of the mother and appears to be able to maintain this position passively due at least in part to the Bernoulli effect. The riding behavior by very young calves is probably a method to reduce the energetic requirements of the calf during migration and hence to reduce the stress of migration on the young calf.

Most calves appear to be born in the Chukchi and Western Beaufort seas based on few sightings of calves in the Bering Sea, the relatively high occurrence of mature females 11/64 (17%) harvested at Utqiaġvik in spring carrying a full-term fetus (NSB unpublished data), and only one sighting of a young calf in the eastern Beaufort Sea during summer (Koski et al. 1988). However, some calves are born in the Bering Sea. Noongwook et al. (2007) reported that Saint Lawrence Island whale hunters have reported seeing migrating mother/calf pairs in April and May, but the frequency of such sightings was not quantified: "Mothers with calves travel as part of the large-whale group and are seen as early as April, but with greatest frequency in mid-May. Calves may be born as late as June. Hunters say they are harvesting pregnant females more frequently now than years ago, which is consistent with observations of increasing numbers of whales and particularly small whales" (Noongwook et al. 2007). In addition, Koski et al. (1993) estimated that 14% of calves were born before 1 April, when most whales are still in the Bering Sea, and 11% were born after 1 June, when most whales have passed Utqiaġvik. Some sexually mature females harvested at Utqiaġvik in May had near-term fetuses and these ranged in total length from 366 to 455 cm (Tarpley et al. 2016, 2021). It appears that first-time mothers calve late in the spring after they pass Utqiaġvik, based on a comparison of the sizes of mothers seen during the summer with those passing Utqiaġvik in late April to early June during the 1980s to early 1990s (Koski et al. 1993).

#### 22.2.6 Calf Size at Birth

There are limited data on the lengths of newborn calves, but the estimated near-term fetal lengths ranged from 400 to 450 cm in Nerini et al. (1984). Koski et al. (1993) suggested a mean size at birth of 430 cm based on the estimate of Nerini et al. (1984) and photogrammetric measurements of young calves photographed near Utqiaġvik. More recent data from near-term fetuses harvested from 29 April to 15 June had a mean size of 413 cm (George, field observations). Twelve of the 16 near-term fetuses were >400 cm (Tarpley et al. 2021) and the largest fetus was 455 cm. Based on photographic data from late spring and early summer, calves with their mothers had total lengths of around 4.4 m; however, most of these calves were more than a few days old so this overestimates the size of a newborn calf. The mean 4.4 m calf size is about 30% of the 14.7 m mean length of all photogrammetrically measured mothers (Fig. 22.4a; W Koski, unpubl data). Agbayani et al. (2020) reported that average size at birth of gray whales was 4.6 m, or 39% of the mean size of mature females (11.7 m; Rice and Wolman 1971).

Fig. 22.4 (a) A bowhead whale mother and newborn calf photographed near Utqiaġvik AK in spring 2004. Photo taken by W. Koski; (b) A bowhead whale mother with a 4–5-month-old calf photographed in Cumberland Sound during August 2019. Photo taken by Ricky Kilabuk

# 22.2.7 Calf Dependency

Bowhead whale calves remain with their mothers for about 10–11 months (Koski et al. 1993, 2004, 2008). Calves are primarily born during April to early June, and only a few yearlings have been seen with their mothers near Utqiaġvik in spring (Koski et al. 2012). The vast majority of yearlings are solitary when they pass Utqiaġvik toward the end of the spring migration, well after other immature whales (Koski et al. 2012). While few calves born the previous year are still with their mothers in spring, milk in the stomach of one yearling harvested in spring (it was probably born late in the previous year) indicates that it was still nursing (George and Suydam 2014; Tarpley et al. 2021). Stomach analyses of 12 calves of the year that were harvested in autumn found that nine had only milk in the stomach, two of them also had invertebrates, and one was empty. This indicates that calves begin to feed on invertebrates when 5–7 months old, but their main source of nourishment is milk (George and Suydam 2014; Sheffield and George 2021). Calf dependency is quite similar in related southern right whales, where females and their 1-year-old young return to the general winter-time mating area just before females and young separate (Taber and Thomas 1982). Other species of baleen whales are weaned at an earlier age than bowhead whales and after they arrive on their feeding grounds with their mothers (6–8 months for blue, fin, sei, gray, and humpback whales; Aguilar 2002; Clapham 2002; Horwood 2002, 2018; Jones and Swartz 2002; Sears 2002; NAMMCO 2020a, b, 2022a, b). Despite a longer period of dependency on their mothers, bowhead whale calves are generally less than half the length of their mother when weaned (Koski et al. 1993), while the other species of mysticetes are generally about two-third to three-quarter the length of their mothers at weaning (NAMMCO 2020a, b, 2022a, b). Gray whales, for instance, are weaned at about 8.7 m (Jones and Swartz 2002), which is about 74% of the average length of a mature female gray whale (Rice and Wolman 1971).

#### 22.2.8 Calving Intervals

Early photographic studies suggested that bowhead whale calving intervals were mostly 3 and 4 years (Miller et al. 1992; Rugh et al. 1992; Koski et al. 1993). Consistent with the calving intervals during those years were reproductive cycles of 2 years with very low calf production followed by 1 year with moderate calf production and 1 year with high calf production (Koski et al. 1993). Tarpley et al. (2021) summarized the considerable literature on bowhead whale calving intervals and calving rates for bowhead whales of the Bering–Chukchi–Beaufort (BCB) stock that was collected during post-mortem examination of harvested whales, aerial surveys, and progesterone spikes in baleen of mature females (Rolland et al. 2018). Tarpley et al. (2021) included data from more recent years (1993–2013) than Tarpley et al. (2016) and concluded that the average inter-birth interval is just over 3 years with an average pregnancy rate of about 0.32 calves/year. George et al. (2018) reported a positive and statistically significant trend in pregnancy rate during their study period; however, these findings are being reanalyzed. Right whale calving intervals are similar to bowhead whales (Davidson et al. 2018; Watson et al. 2021), but calving intervals for North Atlantic right whales have increased since the 1980s to about 5 years (Kraus et al. 2001, 2007). In comparison to bowhead and right whales, calving intervals of other baleen whales are generally 2 years (gray whales—Jones 1990; Jones and Swartz 2002; humpback whales—Clapham 2002; Baker et al. 1987; fin whales—Aguilar 2002) and are 2–3 years for blue whales (Sears 2002).

It is worthwhile to compare lactating bowhead whales with other migratory baleen species. Lactating gray whales in Mexican overwintering lagoons were in better body condition than other gray whales (Christiansen et al. 2021); however, it is not known whether the better body condition was maintained to weaning of the calf, which is several months later and after they leave the wintering lagoons. It is also not known whether females that had calves the previous year were more likely to die than other sexually mature gray whales during mass mortality events that periodically have occurred recently (Perryman et al. 2002, 2021). Survival of sexually mature bowhead whales is extremely high (98.4–99.6%, Zeh et al. 2002; Givens et al. 2017), so few bowhead whale mothers are likely to have died as a result of giving birth to a calf and raising it to weaning.

#### 22.2.9 Growth Rates

During the nursing period, bowhead whale calves grow rapidly (Fig. 22.4a, b; Koski et al. 1993), but between weaning and approximately year 5, bowhead whales display sustained baleen and head growth and an almost unprecedented pattern of limited growth in the rest of their bodies (i.e., the postcranial portions). Large autumn calves and small yearlings or even 2+-year-old bowhead whales can overlap in body length (Koski et al. 2012; George and Suydam 2014). During this period, they withdraw resources from the skeleton, in particular the ribs, which may lose 40% of bone mass (George et al. 2016). The body lengths of whales 2–5+ years old overlap, with little annual increase in body length (Lubetkin et al. 2008; Koski et al. 2012). This emphasis on baleen and head growth is unique among baleen whales and prepares the young whales for efficient feeding on tiny invertebrates in an environment with low densities and unpredictable presence of their primary prey. Following this hiatus in growth, bowhead whale growth becomes more rapid (Koski et al. 1992; Lubetkin et al. 2012) but is still slow compared to cetaceans inhabiting warmer waters (George et al. 2021b). Once growth resumes in year 6, it takes 13–20 years to grow to the age of sexual maturity (i.e., at about 25 years old) and another 30 years or more to attain physical maturity at an age of 50–60 (Koski et al. 1992; Lubetkin et al. 2012).

In other baleen whales, growth is rapid until they are weaned and then slows down or stops after they depart their feeding grounds. The second growth phase starts when they return to their feeding ground at about 1.5–2.5 years old, whereas in bowheads, the slow growth extends until they are 5+ years old. Sexual maturity in right whales is around 9 years (Hamilton et al. 1998), blue whales 8–10 years (Sears 2002), fin whales 6–8 years (Aguilar 2002), sei whales about 10 years (Horwood 2002), humpback whales about 5 years (Clapham 2002), and gray whales 6–12 years (Jones and Swartz 2002).

Bowhead whales store energy reserves in their blubber to ensure survival during periods of low food abundance rather than applying these reserves more immediately to growth as do other cetaceans (Burns 1993; George 2009). George et al. (2021a, b) speculated that these apparently conservative growth and reproductive strategies appear to be possible only for geographically isolated species such as the bowhead whale.

#### 22.3 Conclusions and Future Directions

Most of the information summarized above has come from harvest and photographic data collected from the BCB stock of bowhead whale. These data have been used for management of the EC-WG stock and should be validated by studies conducted on that latter stock. Estimates of growth rates and reproductive parameters rely heavily on accurate estimates of age. Calves and yearlings can be accurately identified in photographs based on their morphology (Koski et al. 1993, 2012), and whales up to about age 10 can be reliably aged based on the length of their baleen (Lubetkin et al. 2008). The latter information can only be obtained from harvested whales, which results in much smaller sample sizes for analyses and makes analyses impossible for stocks other than the BCB stock. Approximate age estimates for whales older than about 10 years come from AAR analyses (Wetzel et al. 2017). DNA methylation has been used to estimate the ages of a few EC-WG bowhead whales (Li et al. 2021; Parsons et al. 2023), and this method appears to provide more precise age estimates than AAR based on data from known age animals of other species in captivity. We recommend that tissues already aged using AAR and tissues from recently harvested whales be aged using DNA methylation. This will permit us to obtain better estimates of growth and reproduction parameters.

Biopsy samples from bowhead whales can be used to determine the age of sampled whales using DNA methylation (Parsons et al. 2023), the sex of sampled whales (Linsky et al. 2022), pregnancy rates for sexually mature whales (Pallin et al. 2018), and their diet (Marcoux et al. 2012; Pomerleau et al. 2018). From combinations of these data and with samples from a large number of whales, the ages at sexual maturity and senescence of female bowhead whales can more accurately be determined, and the population structure can be determined as well. Bowhead whales segregate by size class in the summer feeding areas (Koski et al. 1988) and so the diets of different size classes are expected to be different. Analysis of stable isotopes from biopsy samples will provide information on the differences in diet and energetics of different size classes of bowhead whales.

Genetic analyses of biopsy samples to determine the parents of bowhead whales will provide information on reproduction history of the parents. For example, if the age of a young animal is obtained and there is information for its mother about the years when she had calves, the information for the young animal could contribute to the sequence of years when the mother had or did not have calves. If a male bowhead is found to be the father of many animals, it would provide information on the existence of "super males" or males that father a disproportionately high proportion of the recruits to the population (Gerber and Krützen 2023, this book).

Drones have become a valuable tool for observing the behavior of animals while minimizing disturbance (Fortune et al. 2017; Ramos et al. 2023, this book). Recent studies of bowhead whales in eastern Canada have provided more detailed information on behavior than earlier studies from fixed wing aircraft because camera resolution has improved, and whales do not appear to be disturbed by batterypowered drones flying at low altitudes above them (W Koski, pers obs). During the same studies, accurate information on whale sizes and body condition can be obtained from still photographs.

Also, as noted by Brownell and Ralls (1986) there is still a need to collect additional anatomical data on harvested bowhead whales. Special attention should be given to the following: (1) size of testes and weights, (2) epididymides, (3) sperm morphology, (4) total length and girth of the penis, and (5) the size of the vagina and the number of vaginal folds (see also Orbach et al. 2023, this book). In addition, details are lacking on the morphology and viability of the sperm.

Bowhead whales have adopted many growth and reproductive strategies that have enabled them to survive in a challenging environment where no other mysticetes co-occur throughout their principal range. It appears that these strategies permit bowhead whales to survive long periods with negative energy balances by storing energy reserves in a thick layer of blubber. To obtain this energy in an environment with overall low annual productivity, they have developed an efficient feeding apparatus that can filter tiny organisms from the water column, as right whales of the related genus Eubalaena do. To ensure that they have adequate energy reserves to survive periods with low productivity, they delay reproduction until energy reserves are sufficient to successfully wean their young and at the same time enhance the survival of the mother. As a direct result of this cautious approach to using food resources for growth and raising a calf, females do not become sexually mature until they are in their mid-twenties, in comparison to other baleen whales which become sexually mature at 5–12 years (Hamilton et al. 1998; Aguilar 2002; Clapham 2002, 2018; Horwood 2002; Jones and Swartz 2002; Sears 2002). They counterbalance late sexual maturity and long periods between giving birth to calves with their extraordinary longevity. Bowhead whales are the longest living mammal discovered to date, apparently living to ages of 200 years or more and female bowheads may be capable of producing calves for 100 years, which is longer than other mysticetes are thought to live. Blue and fin whales, for instance, are believed to live to 80–90 (Aguilar 2002; Sears 2002; NAMMCO 2020a, 2022a), humpback and right whales to 70 (Hamilton et al. 1998; Clapham 2002, 2018), and sei whales to 50–70 years (Horwood 2002; NAMMCO 2020b).

Acknowledgments We thank the Alaska Eskimo Whaling Commission (AEWC) and the Barrow Whaling Captains' Association for their confidence, guidance, and support of our research. We gratefully acknowledge use of unpublished data and funding provided by the North Slope Borough Department of Wildlife Management and National Oceanic and Atmospheric Administration (through the AEWC) and the Coastal Impact Assessment Program. BOEM and their predecessor organizations, the National Marine Fisheries Service, the Canadian Government, and numerous oil companies funded or co-funded many of the early studies that contributed to our knowledge of bowhead whales. We thank the numerous biologists and field assistants who assisted with data collection during studies of bowhead whales over the past five decades. We also thank the external reviewers, Robert Brownell Jr., Franca Eichenberger, Ellen Garland, and Dara Orbach for their astute comments that helped to finalize this chapter. While he is also an author of this chapter, we dedicate this work to the memory of John Craighead ("Craig") George, a tireless scientist for bowhead and other Arctic life knowledge, and for honoring the ways of life of the Inuit People. Craig provided excellent chapter proof comments days before this book went to press, and short hours before he passed away in tragic unforeseen fashion. Thank you for all, Craig. Yours was a life well-lived.

#### References

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# Chapter 23 Right Whale Sexual Strategies and Behavior

Moira Wilding Brown and Mariano Sironi

Abstract North Atlantic and southern right whale social interactions and sexual behavior have been studied for decades. Understanding whale mating systems can inform about many aspects of their biology and even their anatomy. Right whales have a polygynandrous mating strategy where females and males mate with multiple partners within a breeding season. It is hypothesized that this promotes sperm competition among males and likely explains the large testis-to-body-size ratio in Eubalaenids. Surface active groups (SAGs) characterize mating behavior in North Atlantic and southern right whales, where two or more animals are at the surface with frequent physical contact. Observations of copulation in SAGs have led to the hypothesis that conception is the primary function, with females practicing a mating strategy where the chance of conception with the largest and likely healthiest male would be maximized. Right whales produce their entire acoustic repertoire of known calls while in SAGs and sounds are thought to serve a social communication function. In the North Atlantic, surface active behavior is seen in all habitat areas and in all months of the year in which right whales are sighted. SAGs tend to increase in size and vigor as the mating season approaches, resulting in spectacular and highly energetic courtship activity with group sizes numbering 30 animals and more; however, the whereabouts of any breeding ground is unknown. On southern right whale calving grounds, mother-calf pairs use relatively shallow waters along the coastline, and SAGs tend to occur farther from shore: calving and mating occur in winter in largely the same habitat areas. Analyses of seasonal timing and group composition of individually identified animals within SAGs suggest that they may serve multiple other roles, since conceptive and non-conceptive groups have been

Universidad Nacional de Córdoba, Córdoba, Argentina

Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/978-3-031-35651-3\_23.

M. W. Brown (✉)

Canadian Whale Institute, Welshpool, NB, Canada e-mail<EMAIL_ADDRESS>
M. Sironi Instituto de Conservación de Ballenas, Buenos Aires, Argentina

revealed. SAGs often include pregnant females, juveniles, and occasionally calves. Some groups consist of exclusively same sex individuals. It has been hypothesized that, in addition to conception, SAGs may also provide opportunities for right whales to socialize, play, learn, practice mating, and identify potential future mates.

Keywords Juvenile sexual behavior · Mating behaviors · Non-conceptive behavior · North Atlantic right whale · Polygynandrous mating · Sexual behavior · Southern right whale · Surface active groups

#### 23.1 Introduction

After one day at sea with North Atlantic right whales, colleague Malcolm Hunter wrote in his journal "Half a century of witnessing wildlife spectacles on every continent, including dozens featuring lions, tigers, and bears, but nothing can compare with August 8, 1995 on the Bay of Fundy Canada, watching male North Atlantic right whales thrashing about to position themselves next to a lone female."

When the editors invited us to contribute a chapter to this text, our thoughts went to the many hours of many days spent watching and puzzling over groups of so-called thrashing right whales in the North Atlantic (Eubalaena glacialis) and Southern Hemisphere (E. australis). Not all assemblages are equally energetic, some are relatively calm unions of two or three animals. Larger gatherings can be seen from a distance of one mile or more, the air above heavy with fountains of mist. As we approach, we notice the sounds of explosive blows and the churning of their surprisingly agile bodies – at times their tails were almost touching their heads. Meanwhile, the inverted focal female, with her genital slit in the air, apparently incites competition among attendant males who jockey for position beside her for an opportunity to mate when she rolls upright to breathe. This is the social behavior named courtship in right whales.

Garnering insights about whale behavior is challenging, with observations often confined to a few moments when the whales surface to breathe. But there are those times when researchers come across a pair or more, sometimes many more, whales remaining at the surface for minutes to hours. At times the whales are engaged in seemingly calm interactions (Fig. 23.1a). At other times, there is a confusing, at least to the observer, melee of heads, bodies, and tails maneuvering around each other at the surface (Fig. 23.1b).

We present a synthesis of what is known and hypothesized about social interactions and sexual behavior of right whales in the North Atlantic and southern hemisphere species. This chapter is illustrated with previously unpublished images and video clips from boats, airplanes, drones and shore. The status of North Pacific right whales (E. japonica) remains precarious, robust life history data are lacking, calving grounds remain a mystery, and the poor understanding of even broad scale movements despite visual and acoustic surveys over the past 20 years (Harcourt et al. 2019) precludes including this species.

Fig. 23.1 (a) Three North Atlantic right whales in a small surface active group (SAG) unusually close to shore in the Bay of Fundy; (b) a high-energy SAG in the Grand Manan Basin, North Atlantic right whale critical habitat, lower Bay of Fundy, Canada. The white-bellied animal is the focal female belly-up and surrounded by several males. One of the males to the left of the female is about to lay his flipper on her belly. Moira Brown, Canadian Whale Institute

North Atlantic and southern right whales are tracked over time using photo and video images of natural markings called callosities, unique patterns of keratinstructured raised skin tissue on the top and sides of their heads, lips and chins, and lip crenulations and by pigmentation patterns that are used to distinguish individuals over time (Payne et al. 1983; Kraus et al. 1986, Hamilton et al. 2007). Scarring from their encounters with human activities including fishing gear entanglement and to a lesser extent vessel strike (Knowlton and Kraus 2001; Knowlton et al. 2012; Sironi et al. 2021) and in southern right whales from Argentina kelp gull (Larus dominicanus) wounding (Marón et al. 2015a) provide additional marks to differentiate individuals that in some cases may be temporary. The ability to tell individuals apart is important for describing all behaviors. Modern drone technology (Ramos et al. 2023, this book) has allowed for rapid and rather inexpensive photo and video imagining of right whales, providing images of unprecedented levels of detail to understand who is who and who does what in the midst of the surface active groups (SAGs).

Cetacean social behavior is typically derived from observations of whales at or just below the surface (Sironi 2004; Brown et al. 2007). Behaviors are described by distance between individuals (usually in body lengths) and the relative positioning of animals in the association (i.e., head-to-head, belly-to-belly) (Kraus and Hatch 2001). Images and video footage of right whale movements (Azizeh et al. 2021), associations, and unique identifiers have permitted researchers to hypothesize individual strategies of social behavior (Lonati et al. 2022). Data on age, sex, reproductive state, and relatedness of individuals from genetic profiles derived from skin biopsy samples can be integrated to interpret social interactions and speculate on roles and strategies (i.e., Frasier et al. 2007, 2013). This is more feasible in relatively small populations, such as with the North Atlantic right whale, while in the larger southern right whale populations, less is known about each individual, but there are more individuals to learn from. Detailed right whale life history data make it possible to learn about why right whales display such elaborate sexual behavior to maximize their individual fitness.

#### 23.2 Mating Behavior, Gestation, and Parturition

Donnelly (1967) provided the first account of mating behavior in southern right whales from observations during a month-long period in late August and September 1965, in Algoa Bay, South Africa. He adopted the term courting pairs of whales for a social grouping of two whales rolling and splashing together, detectable from a great distance with "flukes and flippers waving above the surface," engaged in apparent mating behavior albeit with apparent tenderness and grace (Donnelly 1967). The courtship events were divided into pre-copulatory (female horizontal, male caressing), copulatory approach (female horizontal and dorsum up, male rolls under and positions belly-to-belly), and post coitus behavior (female returns to dorsal side up posture which was assumed to be the normal responsive behavior; Donnelly 1969). The admittedly difficult-to-detect sequences of behaviors were described as a female horizontal at the surface with head and "forequarters" exposed while the male actively dove, circled, and caressed the female for at least 4 h, often resting his chin on her hindquarters (Donnelly 1967). Group size was usually two whales, although polygamous events of three and four whales were seen. The term "polygamous" was used by Donnelly (1967) to indicate a mating system where a single male is able to obtain reproductive access to a number of females either simultaneously or serially. Males were identified as such when they surfaced and rolled on their back after a horizontal belly-to-belly position with the female; coitus was estimated to be rapid, taking no longer than one-half minute, occurring about every one-half hour and likely not always successful (Donnelly 1967). Body positioning was head-to-head and side-to-side. In some events, an unresponsive female lay on her side away from the male and occasionally on her back with the male attempting to turn her over (Donnelly 1969). Donnelly (1967) estimated the measure of male coital success by a "flurry of fluke movements" after which the male surfaced and rolled belly-up for about 20 s.

Donnelly (1969) reviewed the seasonality of southern right whale arrival in coastal calving areas and courtship behaviors for a first approximation of ten-month gestation with calving occurring at least in alternate years. Early efforts to calculate the gestation period of southern right whales based on mating behavior seen in coastal waters roughly coincided with the winter calving period were not substantiated, at least in Argentine waters because calving females were rarely seen in the year preceding a calving (Donnelly 1969; Payne et al. 1983). Three explanations were proposed: (1) gestation may be longer, up to two years, (2) there is delayed implantation occurring, and (3) female occupancy in coastal waters the year before calving is brief (Payne 1986).

Reproduction and gestation were investigated in southern right whales in South Africa. Using records of stranding neonates, length of fetuses, estimates of fetal growth rates, and mean size at birth, the gestation period was estimated at 357–396 days or roughly 12–13 months (Best 1994). A similar rarity of females seen in the prior year giving birth was attributed to short coastal residency or conceptions occurring outside coastal waters (Best 1994). Burnell and Bryden (1997) suggested a gestation duration of 355 days for right whales in the Head of the Bight, Australia, based on mating and calving activities. The latter two estimates suggest a 12-month gestation for southern right whales. The most likely of Payne's (1986) explanations is that mating can take place not only in coastal waters but also further offshore as there has been no support for a two-year gestation period (Best 1994) or delayed implantation, which is unknown for cetaceans (Boness et al. 2002).

Here we define the area where calves are born as the calving ground; the nursery ground is where mothers provide neonatal care (i.e., suckling, protection from predators), and the breeding ground is where courtship and copulation occur. More than one of these activities can take place in the same ground. For instance, southern right whales use the Atlantic coast of South America for different purposes, with most pregnant females concentrating in calving grounds such as Península Valdés in Argentina (Payne 1986; Payne et al. 1990) and southern Brazil (Groch et al. 2005), where mating also occurs. In other areas, such as the Uruguayan coast (Costa et al. 2007; Jorge et al. 2010) and Golfo San Matías in Argentina (Arias et al. 2018), mostly reproductively active individuals gather to breed and socialize while the areas are also used by some mothers with calves. In recent years, as population size and density increase in the Península Valdés calving ground in Argentina, mother-calf pairs use the optimum areas along the coast of the gulfs and displace solitary individuals and breeding groups to suboptimal zones that are farther from shore and in deeper waters (Sueyro et al. 2018); in this case, the mothers with calves are still well within the known breeding ground.

In southern right whales, behavioral observations are primarily confined to wintering calving areas. In these areas, the most common social unit is the mothercalf pair, with a strong bond between the two for the first year of the young whale's life. Permanent separation from the mother occurs when calves are 12–15 months old (Taber and Thomas 1982; Burnell 2001). Female right whales typically calve once every three years, and stay in nursery grounds such as Península Valdés and South Africa with their calves for the first 2–3-month postpartum (Payne 1986; Payne et al. 1990; Best and Rüther 1992; Cooke et al. 2003). During this time, the playful calves, which measure up to 5 m at birth, grow 2–3 m in length (Whitehead and Payne 1981; Best and Rüther 1992; Christiansen et al. 2022) and develop locomotor and social skills (Taber and Thomas 1982; Thomas and Taber 1984).

Cow-calf pairs then migrate to their feeding grounds (Best et al. 1993; Zerbini et al. 2016, 2018), and some return when the calves are almost one year old (Thomas and Taber 1984; Rowntree et al. 2001). The yearlings are weaned and begin their lives as independent whales (Sironi 2004). Mature females in their calving years show significantly higher fidelity to the nursery grounds than males, and they return repeatedly to calve and to wean calves at particular locations (Burnell 2001; Rowntree et al. 2001). Adult females that neither forage abundantly nor mate in the nursery grounds migrate to calving grounds with their one-year-old calves

Fig. 23.2 In this large SAG of North Atlantic right whales in the Bay of Fundy, the focal female is in the center of the image. There is one male attempting to copulate with her while she is belly-up.  Moira Brown, Canadian Whale Institute

probably to wean them there (Thomas and Taber 1984; Rowntree et al. 2001). This suggests that there may be important advantages for yearlings to be weaned in areas where they can socialize with conspecifics (Sironi 2004).

In the North Atlantic, right whales are studied year-round in various habitat areas from the calving ground in the southeast coast of Florida through the mid-Atlantic to well-known spring, summer, and autumn feeding grounds in the Gulf of Maine and more recently in the Gulf of Saint Lawrence. One of the mysteries of the North Atlantic right whale is that they appear to engage in SAGs that are sexual in nature in all the habitat areas year-round (Winn et al. 1986; Parks et al. 2007). Thus, SAGs are the most common social behavior observed for North Atlantic right whales and are thought to be related to reproduction (Fig. 23.2). The assemblage of right whales in a SAG was intentionally described simply as a temporary association of two or more animals (30+ individuals) in close proximity (<1 body length) engaged in frequent physical contact (Kraus and Hatch 2001). This basic definition, derived from hours of observations over decades, was chosen to avoid assigning functional attributes to social groups and avoid potentially masking discrete behavioral functions (Kraus and Hatch 2001). Although similar social groups and behaviors have been described for southern right whales off Argentina (Payne 1986), South Africa (Donnelly 1967; Best et al. 2003), Chile (Galletti Vernazzani et al. 2014), Australia (Burnell et al. 1990), and New Zealand (Patenaude 2000; Carroll et al. 2022), observations are confined to the nearshore southern hemisphere calving/breeding grounds. It is unknown if southern right whales participate in SAGs year-round. Satellite telemetry of southern right whales tagged in their calving grounds could help to discover the location of potential mating grounds further offshore (e.g., Argentina, Zerbini et al. (2016, 2018); Siguiendo Ballenas (2022); South Africa, Mammal Research Institute (2022); New Zealand, Tohora Voyages (2021)).

The discovery of an annual mating ground for North Atlantic right whales has remained elusive. It has long been speculated that the species' gestation period is similar to the 12–13 months estimated for southern right whales (Best 1994). Calves are born off the southeastern USA, sightings of neonates peak from December to February, and conception is speculated to occur between November and February (Kraus et al. 1993; Hamilton and Cooper 2010). There is one documented exception to the seasonal timing of a calf born in the late spring in northeastern US waters (Patrician et al. 2009) and a second geographical exception of a newborn observed in January 2013 in Cape Cod Bay (Hamilton PK pers. comm.).

There was some indication of a potential mating ground based on surveys over a seven-year period in the Gulf of Maine. Cole et al. (2013) compared proportions of females calving the following year (conceptive females) and the proportion of genetically identified fathers within each geographic region that the whales inhabit throughout the year. Based on documentation of about one-half of the cataloged population from November–January 2002–2008, Cole et al. (2013) found significantly higher proportions of known fathers and conceptive females present in the central Gulf of Maine during the estimated conception period when compared to most other areas seasonally inhabited by right whales. The discovery of reproductively successful males and females in the central Gulf of Maine during the boreal winter led the authors to suggest this area as the species' mating ground for some conceptions (Cole et al. 2013). However, the annual use of this region by right whales has not persisted (Cole TVN pers. comm.) and the concept of a single mating ground for North Atlantic right whales remains to be addressed. Some individuals stay in northern feeding areas in the Gulf of Maine and along the Scotian Shelf during the winter (Cole et al. 2013; Durette-Morin et al. 2022). North Atlantic right whale females migrate to a calving ground in the southeast USA to give birth but not to mate (Kraus and Rolland 2007; Cole et al. 2013). There are, however, some right whales including juveniles, adult males, and non-calving females that have been documented in the southeast US calving area during winter (Hamilton et al. 2007; Hamilton and Cooper 2010). Gowan et al. (2019) modeled decades of sighting data from the calving ground and found differences in migratory probabilities depending on an animal's reproductive state and age class, indicating that right whales have the potential to migrate to the southeast USA each winter but that this migration is condition-dependent. The model indicated that males were more likely to use the southeast US habitat area than non-calving females and that females in the year before and following calving may overwinter in feeding areas to increase blubber reserves for future reproduction (Gowan et al. 2019). This migratory behavior of females not migrating in a nonreproductive year is called skipped breeding partial migration (Gowan et al. 2019). For comparison in migratory differences, a southern right whale female was tagged with satellite monitored transmitters in Península Valdés, Argentina, in 2015 when she had no calf and in 2021 when she was accompanied by a calf (Siguiendo Ballenas 2022). The tracks showed that she used different areas of the southwest Atlantic in two years, possibly preferring different feeding destinations based on her reproductive status.

# 23.3 The Sexual Behavior of Right Whales: A Group Strategy

Sex and hunger are the two primary animal instincts: hunger propels animals to migrate in search of food and sex compels them to come together and mate. There are a bewildering number of mammalian mating systems for sexual reproduction, but it is all governed by one underlying instinct or drive to maximize individual reproductive success, as every animal tries to put as many copies of its genes into future generations. The distribution of males is largely governed by the distribution of females (Eichenberger et al. 2023, this book; Würsig et al. 2023, this book).

Arguments about which sex benefits the most from dispersal to avoid potential inbreeding in polygynous mammals were summarized by Greenwood (1980).  Greater benefits accrue to males gaining access to a large number of females than vice versa (Greenwood 1980). However, since intra-sexual competition is more intense among males than females, a large proportion of males may be denied access to females (Greenwood 1980; Payne and Dorsey 1983).

Right whales have a polygynandrous mating system, where a female may mate with multiple males within a breeding season and a male with multiple females (Brownell and Ralls 1986; Kraus and Hatch 2001; Kraus et al. 2007). In the North Atlantic, some SAGs involve a single focal female that emits calls to attract males, presumably inciting competition among males who compete for access to the focal female at the surface in a belly-up posture (Kraus and Hatch 2001; Kraus et al. 2007; Eichenberger et al. 2023, this book). Right whales produce their entire acoustic repertoire of known calls while in SAGs, that is, a stereotypical contact call, the upcall, and a loud broadband impulsive sound, the gunshot, which is described for all right whale species (Parks et al. 2007; Parks 2022; Eichenberger et al. 2023, this book). These sounds are considered to serve a social communication function (Parks et al. 2007). The focal female in a SAG, located roughly in the center of a group, typically spends most of the time on her back with her genital slit out of the water (Donnelly 1967; Kraus and Hatch 2001). The belly-up posture has been interpreted as an attempt by the female to avoid unwanted copulation, but Kraus and Hatch (2001) suggested it might be more of an assessment of the nearby male and if he is considered the most suitable partner. Males move actively to position themselves next to the female; they appear to follow her orientation (belly-up in avoidance or head-up for a breath) with their flipper(s) and wait until she turns over to breathe (Fig. 23.3), and then copulation can occur (Figs. 23.4. a and b) (Payne 1986; Kraus and Hatch 2001).

SAGs in the North Atlantic and southern hemisphere are undoubtedly sexual in nature as confirmed by frequent observations of erect penises and intromission that are indicative of mating (Donnelly 1967, 1969; Patenaude 2000; Kraus and Hatch 2001; Best et al. 2003; Sironi 2004; Mate et al. 2005; Parks et al. 2007). Males compete for access to the scarce females not through aggression but rather with

Fig. 23.3 An aerial image of at least four southern right whales in a SAG in Península Valdés. The female is belly-up and the closest whale to her left is keeping track of her movements with his left flipper placed on her belly. Mariano Sironi, Instituto de Conservación de Ballenas, Argentina

Fig. 23.4 Drone images of two southern right whales copulating in Península Valdés: (a) female is head-up and male on his side and slightly underneath the female; and (b) the female is inverted in the belly-up position and the male is on his right side. Nicolás Lewin, Instituto de Conservación de Ballenas, Argentina

physical stamina and ability to position themselves close to the focal females in a group and wait for a mating opportunity (Fig. 23.4).

 Competition among males can take two forms. First, males compete behaviorally during courtship when they swim, push, turn, and move within a SAG to increase their chances to copulate with a receptive female. This would likely be a learned skill with success related to body size and maturity (Frasier et al. 2007). Mating side-to-side or belly-to-belly, their fusiform body shape allows for few alternatives for copulatory positions. Second, the most decisive male competition likely occurs inside the female's body, through the production of huge volumes of sperm to increase each male's chances of fertilizing the female's only available ovum. The male that produces the most sperm outcompetes, possibly "diluting" or "washing out" that of other males who recently copulated with the female. Sperm competition likely explains the large testis-to-body-size ratio in this genus, the largest testes in the animal kingdom weighing 500 kg each, a ton in total (Brownell and Ralls 1986).

An additional behavioral indication for sperm competition and female choice in right whales has been collected from observations of multiple males achieving intromission simultaneously. Two males were observed copulating at the same time with the same female in a SAG in the North Atlantic (Mate et al. 2005), while similar observations were made of southern right whales off Argentina (Würsig 2000; D'Agostino et al. 2017) and among the critically endangered Chile-Peru southern right whale population where sightings are scarce (Galletti Vernazzani et al. 2014). Reproductive behavior has been observed off the northwestern coast of Isla de Chiloé, Chile, showing the extended penises of two males entering the genital slit of a female, highlighting the importance of these coastal waters as a mating ground for this population (Galletti Vernazzani et al. 2014). The observation of intromission during the peak of the breeding season suggests that this group was exhibiting reproductive behavior (Galletti Vernazzani et al. 2014).

SAGs in the North Atlantic are seen year-round including on the feeding habitats in the summer and early autumn. SAGs do not always occur at the right time for fertilization to happen; most conceptions should occur from October through December, a season with few observations (Kraus and Hatch 2001). Kraus et al. (2007) asked why North Atlantic right whales spend time and energy in SAGs during the high-priority feeding season if that activity does not result in conceptions (Supplementary Video 23.1). Kraus and Hatch (2001) and Kraus et al. (2007) suggested two possibilities: (1) Females may keep track of the performance of different males, make a choice, and mate with the selected male at a later time. (2) Females may require repeated practice to learn how to assess and select males in SAGs, and it may be lower risk to assess them during the feeding season before the stakes become high during ovulation. SAGs observed outside the breeding season in the North Atlantic contained an average of 4.6 animals, but the range was much greater in the North Atlantic than the southern hemisphere during the breeding season: 2–35 whales per group (Kraus and Hatch 2001) versus 2–10 in South Africa (Best et al. 2003). Group size of SAGs in other mating areas has not been published. During a SAG, female whales can mate sequentially with different males.

Frasier et al. (2007) found that fatherhood in North Atlantic right whales was significantly biased to older males, with successful paternity occurring only from age 15 onward, almost twice the age of females. Both the physical competition between mates and the internal competition between sperm may prevent younger males from securing conceptions, thus resulting in a lower effective population size (Frasier et al. 2007). A second factor that has been suggested to favor the reproductive success of older males is testicular development. Although it is unknown when male testes reach adult size, much higher levels of androgen hormones were found in adults than in juvenile males (Rolland et al. 2005). There may be two factors favoring reproductive success among older males – experience and sperm quantity. If only older males are successful at fertilizing females, then there are even fewer males contributing genes into the next generation. Other male adaptations such as seminal fluid proteins, copulatory plugs, prolonged copulations, and postejaculatory guarding behavior that reduce female remating probability have yet to be investigated for right whales (Parker 2020).

# 23.4 Behavioral Aspects and Differences in Behavior Patterns on Calving Versus Other Grounds

The normal reproductive cycle of northern and southern right whale females lasts for three years. Females give birth to a single calf every three years and lactate for approximately one year, with calves usually leaving their mothers at the end of their natal year (Thomas and Taber 1984; Hamilton et al. 1995; Burnell 2001; Sironi 2004), although genetic profiling of North Atlantic right whale calves revealed unexpected variations in some mother–calf associations and weaning times of 7.5 to 8.0 months (Hamilton et al. 2022). The female then rests for a year to rebuild blubber reserves for the following pregnancy (Marón et al. 2015b). The mean age at first parturition is nine in Argentina (Payne 1986; Cooke et al. 2003, 2015) and Australia (Charlton et al. 2022) and eight in South Africa (Best et al. 2001). The youngest recorded age of females at first calving is five for two individuals in South Africa (Vermeulen E pers. comm.) and six in Argentina, with five cases reported for Península Valdés. The mean age of sexual maturity for North Atlantic females and males is eight years old (Hamilton et al. 1998). There is one case of a minimum age of first parturition of age five (Knowlton et al. 1994). The gestation period is estimated to be the same for northern and southern right whales, 12–- 13 months (Best 1994).

With equal sex ratios, the above implies that for every potentially receptive female, there is an excess of mature males. With females investing much energy in gestating and lactating a calf (Christiansen et al. 2022), this scenario should promote strong competition among males, with females exercising mate choice in SAGs (Reeb et al. 2003). However, in recent years, changes in calving intervals have been detected for the Argentine and South African southern right whale populations, with intervals of four and five years becoming more frequent (Marón et al. 2015b; Thavar et al. 2021). Consequently, the recovery of the populations may be affected by a reduction in the rate of increase. While the potential reproductive cycle for North Atlantic females is similar, the observed cycle is not. There is a longer average calving interval that increased from 4.0 in 2009 to 9.2 in 2021 (Pettis et al. 2022), a male biased sex ratio (Pace et al. 2017), and an increase in the frequency of high calving intervals (6+ years, Bishop et al. 2022) that suggest there is an excess of mature males and that few nonbreeding females transition into the breeding pool (Reed et al. 2022). To investigate low birth rates of North Atlantic right whales, Stewart et al. (2022) compared age-corrected body lengths with age at first reproduction, average inter-birth interval, and the number of calves produced per potential reproductive year. Body lengths have been declining over the past 40 years, and although body length was significantly related to birth interval and calves produced per reproductive year, age at first reproduction was not (Stewart et al. 2021). Stewart et al. (2021) found that larger whales had shorter inter-birth intervals, produced more calves per potential reproductive year, and had higher lifetime calf production, although this was a result of longer potential reproductive spans. Declining body sizes are a potential contributor to low birth rates over the past decade for North Atlantic right whales (Stewart et al. 2021). In southern right whales, by combining historical whaling records and drone photogrammetry data, Christiansen et al. (2022) calculated fetal growth rates and birth and found that larger females produce calves that are larger at birth and that have higher fetal growth rates than those born to smaller females.

Southern right whales show site fidelity (Valenzuela et al. 2009) but also flexibility in habitat use on their wintering grounds (Rowntree et al. 2001). For instance, males and females of all ages move frequently between the major regions of concentration on the Península Valdés nursery ground in Argentina and can change their distribution, abandon some areas, and colonize others along the coastline with time (Rowntree et al. 2001). Females also use different calving grounds in different years, as 124 females were recorded calving in Santa Catarina, Brazil, in some years and in Península Valdés, Argentina, in others (Rowntree et al. 2020). The two areas are separated by nearly 2100 km.

Most southern right whale populations are growing (e.g., Argentina, Crespo et al. (2019); Australia, Bannister (2017); New Zealand, Carroll et al. (2022); South Africa, Brandão et al. (2018)). It has been suggested that with growth, populations in some nursing and breeding areas may be experiencing densitydependent processes: when a threshold in density is reached, this elicits a response in habitat use, with mother-calf pairs remaining in the area, while other groups are displaced to new areas (Sueyro et al. 2018). This would be expected to affect habitat use and therefore mating strategies, particularly among males. This is possibly the case in Península Valdés; mothers with calves may displace solitary animals and breeding groups that move to (and likely are recolonizing) peripheral areas with lower density, such as Golfo San Matías to the north (Arias et al. 2018). As a consequence, these areas are used mostly by solitary juveniles and adults for socializing, courtship, and mating and are becoming more important for the reproductive cycle of the species.

Similar spatial and temporal changes and preferences in habitat use, driven by a number of factors, have been described in other well-known wintering grounds such as Southern Brazil (Danilewicz et al. 2016), where mother-calf pairs remained closer to the coast compared to unaccompanied whales (Renault-Braga et al. 2018, 2021). Mating activity was observed in most of the social groups recorded around the Auckland Islands as evidenced by abundant white water, erect penises, and females exposing their bellies to the surface (Patenaude 2000, see also photos in Eichenberger et al. 2023). Two-thirds of the animals present in groups engaged in social/sexual activity were males (n = 86), although the sex ratio of animals biopsied was 1:1 (Patenaude 2000). In the 1990s, mother-calf pairs were about one-quarter of the whales present, with clear evidence that whales gave birth in the area (Patenaude 2000). However, groups containing cow-calf represented 50% of the animals surveyed in 2020/2021 in the Auckland Islands, a clear signal that the New Zealand population is growing and is not limited by food resources (Carroll et al. 2022). Although the high latitude of the Auckland Islands is more consistent with known summer feeding grounds worldwide, they are clearly both an important calving and breeding ground for southern right whales. Also, southern right whales off New Zealand are recolonizing the mainland presumably from a remnant population from the Auckland and Campbell Islands that survived whaling (Carroll et al. 2014). Recent surveys to the remote Campbell Island found an increase in abundance of mostly sub-adult animals; there have been no sightings of calves, but nine photoidentification matches were made with animals previously seen elsewhere in New Zealand (Torres et al. 2017).

Carroll et al. (2012) examined the reproductive autonomy of southern right whales on their New Zealand calving grounds by using paternity assignment and "gametic recapture." Results suggest that individuals returning to the calving ground are reproductively autonomous on a generational timescale and isolated by maternal fidelity on an evolutionary timescale from others in the Indo-Pacific region, indicating that whales using the same calving ground are mating together (Carroll et al. 2012). This is consistent with other southern hemisphere calving grounds such as Península Valdés in Argentina, where adult right whales are frequently seen copulating amidst mothers and calves (Figs. 23.3 and 23.4). In the western south Atlantic, the genetic differentiation between southern right whales sampled in Brazil and Argentina is subtle and likely reflects differences in the demographic aggregation of whales using each region (Carroll et al. 2020). This, coupled with likely immigration from Argentina into Brazil (Groch et al. 2005) and the observation of known individuals in both calving grounds (Rowntree et al. 2020), indicates that whales show plasticity in philopatric behavior and may mate in different years in different calving grounds within the same population.

#### 23.5 Parturition and Parental Care

Right whales give birth during the winter when they gather in their calving grounds. These are located in coastal waters, and in many sites in the southern hemisphere the whales are the focus of intense whale watching activity. In many cases, big, fat females are observed pregnant, and days later, they are resighted with a calf (Christiansen et al. 2022). Despite the many human eyes watching, observations of right whale births are exceedingly rare. In the North Atlantic, the first account of the birth of a right whale calf occurred in the calving ground in the coastal waters of southeast USA (Zani et al. 2008). Researchers on a survey aircraft described seeing a

Fig. 23.5 A southern right whale named Tehuelche photographed while in the midst of birthing a calf at Península Valdés, Argentina. The tail of the white calf is visible emerging from the genital slit of the female. Luis Pettite

known adult female thrashing at the surface and that the waters around her were red, and a few minutes later, a small calf emerged from subsurface (Zani et al. 2008). In South Africa, a southern right whale female was seen giving birth to a gray morph calf (Best 1981). Coincidentally, the only reported right whale birth at the Península Valdés, Argentina calving ground was also of a gray morph calf (Sironi et al. 2019). The mother was observed from a whale watch boat right before sunset, when the crew noticed unusual behavior and approached her, photographing the moment of birth (Fig. 23.5). Observations were ended before actual delivery occurred because the local whale watch regulations prohibit navigation after sunset (Sironi et al. 2019).

The rarity of the observations of right whale births suggests that they may occur at night, and the case of Tehuelche (Sironi et al. 2019) suggests that this could be the case, although how right whales would benefit from bringing their young to life during the night is a matter of speculation. Frasier et al. (2010) reported on a rare case of two North Atlantic right whale calves that switched mothers and remained with their adoptive mother until weaned. They speculated that the calves must have been in close associations before the biological mother-calf offspring recognition developed and noted that the births may have taken place during an intense storm but did not speculate on a nighttime birth (Frasier et al. 2010).

Fetal growth rate in baleen whales is among the fastest in the animal kingdom. During the last month of gestation, southern right whale fetuses grow between 3 and 4 cm per day (Christiansen et al. 2022). Calves can measure between 4.5 and 5 m in length at birth. The biggest calves are born to the biggest mothers, being nearly 35% of the mother's length (Christiansen et al. 2022). Producing such large offspring is energetically very costly to the females. The main energetic cost for a pregnant female is to produce the heat necessary for gestation (74%), followed by fetal growth (21%), and the energetic cost of the placenta (5%). The energetic cost increases during the 12 months of gestation and is highest during the last 4 months (Christiansen et al. 2022). With such high investment, it is not surprising that lactating females maintain proximity and display maternal behavior patterns to prevent their calves from spending too much precious energy and to protect them from potential predators including killer whales (Orcinus orca) that are present on nursing grounds such as Península Valdés, where at least 12 attacks have been reported (Sironi et al. 2008).

# 23.6 Non-conceptive Sexual Behavior in Calves and Juveniles

Non-conceptive sexual behavior refers to those animals that participate in SAGs without any possibility of conception taking place (Ham et al. 2023, this book). Conception is not possible if (1) the sexual activity takes place outside of the conceptive season (in the North Atlantic, SAGs have been seen during all months, whereas calving occurs primarily from December through February (Kraus and Hatch 2001)), (2) the focal female is already pregnant (Kraus and Hatch 2001), (3) the sexual interactions are among individuals that are sexually immature, or (4) the individuals in the SAG are of the same sex.

What functions could non-conceptive SAGs have? In North Atlantic right whales, almost all known aged right whales were first sighted in SAGs as juveniles and more than half of the SAGs examined had at least one juvenile (Parks et al. 2007). SAGs with a juvenile focal female were on average smaller than SAGs with mature focal females (Kraus and Hatch 2001). The behavior and social interactions of juvenile male and female southern right whales were studied at their nursery ground in Península Valdés, Argentina, including sexual behaviors (Sironi 2004). Sexual behavior was considered to occur in groups where the penis of one or more males was visible (erections), or body postures involving potential physical contact between the genital slits of two or more whales were repeated during the interactions. The posture belly-to-belly was considered separately from other surface activities to assess the time females and males were in a position where potential genital stimulation (and potential mating) could have occurred, although actual copulations in this posture are not usually possible to see from shore. Females could practice this posture that appears to be relevant to avoid unwanted copulations when they engage in surface active groups as adults. There is only one record from 1974 of a shorebased observation of copulation where a classic belly-up female with two attendant males appeared to choose one male: the pair spent a couple of minutes in close contact with the male's penis partially inserted (Würsig 2000).

Juvenility begins when a young individual can survive the death of its mother and ends when sexual maturity is reached (Janson and van Schaik 1993). Environmental feedback, including social learning and practice, is thought to play an important role in juvenile development (Pereira 1993). Sironi (2004) described sex differences in juvenile southern right whale behavior at Península Valdés. Juvenile females actively maintain interactions with mother-calf pairs while males spend more time with other juveniles. During social interactions, females spend significantly more time belly-up than males, probably to avoid unwanted copulations, and end encounters more frequently by turning away from other whales (Sironi 2004). Juvenile right whales may use the nursery grounds as places to practice locomotory behavior and to socialize with conspecifics. Males may establish relationships with age peers that could be important during their adult lives, especially in SAGs. Females actively seek to interact with mothers and calves, possibly to learn maternal behavior by observing them. Sex differences in social interactions that are part of adult whale behavior begin to be established during the juvenile stage in southern right whales (Sironi 2004).

Juvenile right whale females spend substantial time in the vicinity of and interacting with mothers and their calves as well as more time than males in body postures that are typical of adult females. Juvenile males engage in locomotory behavior patterns that resemble adult mating behavior with partners of similar developmental state (Sironi 2004). Testing the social learning hypotheses in right whales can be difficult without experimentation. However, behavioral data show that the opportunities juveniles have at Península Valdés to learn and to practice skills when they engage in social activities are frequent and might be relevant for their future. Juveniles may also spend time at Valdés to become familiar with the environment where a significant amount of sexual and maternal behavior, and therefore essential behavior for their reproductive success, will take place during their adult lives (Sironi 2004).

 In one instance, a calf was separated from its mother by an adult male, which positioned itself in a belly-up posture underneath the calf, holding it between its flippers (D'Agostino et al. 2017).  Similarly, there are two cases of a North Atlantic adult male seen belly-up that held the calf belly-to-belly with its flippers on either side of the calf.  Non-conceptive sexual behavior between a calf and an adult male could be adaptive as it could be important for immature animals to learn successful mating behaviors (Kraus and Hatch 2001; Sironi 2004). Play behaviors of southern right whale calves (e.g., rolling, turning, and touching) with their mothers are thought to help calves develop motor skills and coordination for future socializing, mating, and feeding (Thomas and Taber 1984). Participation in SAGs, a common behavior for juveniles, may function in play, social bonding, dominance sorting, or simply practicing mating behavior (Ham et al. 2023, this book). Juvenile

Fig. 23.6 An adult North Atlantic right whale male on his back, belly-up, holding a calf between his flippers during copulation in the Gulf of St. Lawrence, July 2021. Gina Lonati, University of New Brunswick

males were observed displaying erections in SAGs, but contrary to adults, they were never seen copulating with a female, possibly because they do not yet have the skills nor strength to displace adult males from the best positions to mate (Kraus and Hatch 2001).

Most homosexual behavior in right whales, as in other baleen whales, was observed (or was more evident) among males than among females at Península Valdés (Sironi 2004). No evidence of kin selection or reciprocal altruism in mating strategies exists yet for male right whales. The main function of male-only SAGs involving sexual behavior may be to develop and assess their ability in courtship activity by practicing upon one another, and it could simply be a form of juvenile play behavior (Kraus and Hatch 2001; da Silva and Spinelli 2023, this book; Ham et al. 2023, this book).

#### 23.7 Conclusions and Future Directions

Detailed modern right whale identification catalogues and the use of new technology allow researchers to track life history data – calving events, growth rates, age, sexual maturity, longevity, deaths, sex ratio, and trends in scar acquisition over time. Location and demographic data contribute information on seasonal movements, geographic range, and distribution, as well as reproductive success, associations, abundance, and body condition. Genetic profiling adds to the reproductive story with parentage assignments when possible. These data are critical to undertake population-wide assessments and to develop and monitor recovery strategies. Perhaps more importantly, these data help track the effects of a changing ocean climate that are resulting in habitat shifts and affecting whale population dynamics (Mesnick et al. 2023, this book).

The critically endangered North Atlantic right whale faces substantial hurdles. Population-wide decline in reproductive output, as characterized by low number of calves born and increase in calving intervals, documented in the late 1990s, were attributed to limited prey availability (Caswell et al. 1999; Fujiwara and Caswell 2002; Meyer-Gutbrod et al. 2015) and a combination of fewer actively reproducing females and lower reproductive rates of some females (Brown et al. 1994).

Although the population decline in the 1990s was followed by a decade of reproductive resurgence until 2010, population decline since has been attributed to a shift in feeding habitat from the Gulf of Maine to the Gulf of St. Lawrence, longer calving intervals for some females recovering from nonfatal entanglements, a greater number of longer calving intervals, and fewer pre-breeding females transitioning to the breeding pool (Meyer-Gutbrod et al. 2021; Stewart et al. 2021; Pettis et al. 2022; Reed et al. 2022). Pregnancy and lactation have high energetic demands (Christiansen et al. 2022) and have been linked to variations in reproduction in North Atlantic right whales (Fortune et al. 2013). Miller et al. (2011) concluded that many females were unable to build a sufficient blubber layer to sustain successful reproduction, thus delaying reproduction until enough food could be consumed. Reed et al. (2022) speculated that sublethal effects of entanglement leading to stunting of North Atlantic right whales (Stewart et al. 2021) affect the transition from pre-breeding to breeding females as small individuals have less energy stores to invest in reproduction.

There have yet to be analyses to assess if shifts in prey availability are affecting the frequency and intensity of SAGs. Knowledge of the location of a mating ground for right whales in the North Atlantic eludes us. Bishop et al. (2022) reported that sexually mature females who have used the feeding habitat of the Gulf of St. Lawrence, Canada, since 2015 were significantly more likely to give birth over this time compared to individuals who were not seen there; juvenile males and females were significantly more likely to use the Gulf of St. Lawrence if their mothers did, although this declined as the youngsters aged. An earlier example of site fidelity from mother to offspring was found for animals using the Bay of Fundy from the 1980s to the late 1990s (Malik et al. 1999), but that was before the climateinduced changes in prey availability affected whale movements and distribution which have become much less predictable than in the late twentieth century.

In the North Atlantic, fewer than one-half of cataloged whales have been recorded in the Gulf of St. Lawrence, Canada (Crowe et al. 2021). A portion of the population is using a yet undiscovered summer feeding area(s), and about one-half of the calves born over the past few years were attributed to mothers who do not use the Gulf of St. Lawrence and are older, on average, than Gulf of St. Lawrence mothers (Hamilton PK pers. comm.). High mortality and injury rates associated with right whales using the Gulf of St. Lawrence pose a significant threat to the species because calf fecundity is associated with the mother's and the pattern of habitat use is learned from the mother. Mother-offspring fecundity and calf-learned distribution patterns seen previously in the Bay of Fundy emphasize the need to locate other feeding areas (Malik et al. 1999). Future population growth may hinge on our ability to provide adequate protection from anthropogenic stressors on all their feeding, calving, nursing, and breeding grounds. The lethal and sublethal effects and reproductive failure from entanglements in fishing gear can be ameliorated through targeted fishery management, and mitigation is critical for the recruitment of breeding females (Reed et al. 2022).

Combining genetic and isotopic data, researchers have shown that southern right whale calves learn the locations of the feeding grounds from their mothers and that this culturally inherited site fidelity to feeding grounds has a timescale of at least several generations (Valenzuela et al. 2009, Carroll et al. 2015, 2016). This cultural transmission can benefit the young animals in their first migrations, but in turn it could limit the exploration of new feeding areas and opportunities. This could be the reason why adult females at Península Valdés show increased rates of reproductive failure in years following elevated sea surface temperature anomalies in their feeding grounds in the South Atlantic (Leaper et al. 2006, Valenzuela et al. 2009).

A rapidly changing ocean environment is also affecting the southern species. For instance, five decades of photo-identification data on 1380 southern right whale females of Península Valdés, Argentina, have shown that the mortality of adult females increases after strong El Niño events, which could impede population recovery and could cause the population to decline (Agrelo et al. 2021). The South African southern right whales have changed their foraging strategy, with a significant northward shift from South Georgia/Islas Georgias del Sur in the 1990s to the waters of the Subtropical Convergence, Polar Front, and Marion Island, South Africa, in the 2010s, and have a more diverse diet too (van den Berg et al. 2021). These shifts are an indication that right whales are flexible in their prey and habitat preferences, but the recorded decline in reproductive success is a warning sign that in fact the shifts could be a suboptimal strategy (van den Berg et al. 2021).

Since the late 1990s, there have been extensive efforts throughout the range of the North Atlantic right whale to reduce the impacts of human activities, vessel strikes, and entanglement in commercial fishing gear (Kraus and Rolland 2007). Ocean conditions can change quickly, and the human adaptations to protect right whales in a new habitat area need to respond. Since 2009, an unprecedented climate-associated change in prey availability in the Gulf of Maine affected the distribution and reproductive dynamics of right whales (Meyer-Gutbrod et al. 2015, 2022). Right whales adapted temporally and spatially to the decline in prey in their traditional foraging habitat in the Gulf of Maine by finding food in the Gulf of St. Lawrence (Meyer-Gutbrod et al. 2022). Although the whales redefined their distribution to find food in the decade after 2010, the absence of protective measures from humaninduced serious injury and mortality in the new habitat had catastrophic effects (Davies and Brillant 2019). The mortalities from vessel strikes and fatal entanglements and serious injury from live entanglements galvanized the Canadian government, in consultation with right whale researchers and industry, to proactively adapt human activities in the Gulf of St. Lawrence. Mandatory measures were implemented to reduce vessel speed and close fisheries where there was a high

Fig. 23.7 Researchers observe two right whales mating next to a boat in Península Valdés, Argentina, 11 September 2022. Claudio Nicolini

risk of overlap (Davies and Brillant 2019). Where there was a disaster for a highly endangered whale, humans found a way to develop, implement, monitor, and enforce protection measures.

It is unknown how the anthropogenic stressors that cause poor body condition and stunting in North Atlantic right whales (Christiansen et al. 2020; Stewart et al. 2021) affect offspring survival and a female's capacity to reproduce nor how they will affect the frequency and timing of social behavior and sexual strategies. In general terms, the distribution of females is determined by resources. If resources are widely scattered, females and males will also be. Different habitat conditions and situations produce different mating strategies for both sexes. Of concern is how prey availability and habitat shifts in response to changes in foraging success will affect male access to adult females. Southern right whales have a circumpolar distribution, and rates of recovery for various populations have ranged from near maximum growth rates (Southwest Australia, South Africa, Eastern South America, and sub-Antarctic New Zealand) to poor or not measurable in others (Harcourt et al. 2019). The Auckland Islands population is an example of a population that is in excellent condition and has high and increasing reproductive rates indicative of being able to find sufficient prey (Carroll et al. 2022) (Fig. 23.7).

Will right whales adapt their lives, including sexual strategies and behavior, to the new ocean conditions? Or will humans change the conditions to make the ocean again a home instead of a threat to right whales? Peaceful coexistence and mutual enrichment could be the basis for human-cetacean relations (Barstow 2008). It is possible (Supplementary Video 23.2).

Acknowledgments We thank the Canadian Whale Institute, New England Aquarium, Center for Coastal Studies, and Instituto de Conservación de Ballenas (Argentina) and Ocean Alliance (USA) and their funders for the support during all stages of our research with right whales. The over halfcentury of right whale studies by many hundreds of researchers around the world and their insights and conservation work are greatly appreciated. We thank the editors and external reviewer Rochelle Constantine for detailed and valuable comments on the drafts of this chapter.

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# Chapter 24 Cetacean Sociality, Reproduction, and Conservation

Sarah L. Mesnick, Randall R. Reeves, Paul R. Wade, Philippa Brakes, and Taylor A. Hersh

Abstract The world's cetaceans (like most of biodiversity) are in crisis, and the need for well-informed conservation action has never been greater. Scientific advancements over the last few decades have provided much insight on the reproductive anatomy, physiology, and behavior of whales, dolphins, and porpoises. Our goal in this chapter is to link scientific findings to practical actions that will improve resilience and conservation prospects of cetaceans. We provide an overview of human activities and their impacts on cetacean reproduction and review the progress (or lack thereof) toward conserving species, with a particular focus on those for which sociality and culture may be important to population recovery. For all cetaceans, it is important to preserve or, where necessary and feasible, reestablish the ecological, demographic, and social conditions that allow the animals to reproduce successfully in their natural environment. The better we understand and integrate knowledge concerning cetacean reproductive health into conservation strategies, the better the chances of achieving species recovery, protecting biodiversity, and preventing future extinctions.

R. R. Reeves

IUCN SSC Cetacean Specialist Group, Okapi Wildlife Associates, Hudson, QC, Canada

Committee of Scientific Advisers, Marine Mammal Commission, Bethesda, MD, USA

P. R. Wade

Marine Mammal Laboratory, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA, USA

P. Brakes

Centre for Ecology and Conservation, University of Exeter, Cornwall, UK

Whale and Dolphin Conservation (WDC), Chippenham, Wiltshire, UK

T. A. Hersh

S. L. Mesnick (✉)

Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, USA e-mail<EMAIL_ADDRESS>
Comparative Bioacoustics Group, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands

Keywords Anthropogenic noise · Bycatch · Cetacean · Climate change · Conservation · Fecundity · Human impacts · Insemination · Mating · Recovery · Reproduction · Resilience

#### 24.1 Introduction

Like most of biodiversity, the world's cetaceans are in crisis and the need for wellinformed conservation action has never been greater. Scientific advancements over the last few decades have improved our knowledge of reproductive anatomy and physiology, mating behavior, and parental care of many species of whales, dolphins, and porpoises. Our goal in this chapter is to link these scientific findings to practical actions that will improve conservation prospects for cetaceans.

Human impacts on, attitudes toward, and relationships with cetaceans have changed over time (Notarbartolo di Sciara and Würsig 2022). Commercial whaling, essentially ended since the mid-1980s, killed millions of baleen whales (mysticetes) and sperm whales (Physeter macrocephalus, an odontocete) (Rocha et al. 2014) and sparked global conservation efforts (Fig. 24.1). Drive hunts of small- and mediumsized cetaceans continue in a few regions (e.g., Japan, Faroe Islands, Solomon Islands), but the most serious known obstacle to conserving small cetaceans is incidental mortality in fishing gear (i.e., bycatch) (Read et al. 2006; Brownell et al. 2019). Non-deliberate killing and injuring have also hindered or prevented the recovery of some species and populations of large whales (Johnson 2005; Knowlton et al. 2016). In addition to mortality in fishing gear, the energetic cost of nonfatal entanglement—due to drag from towing gear—can influence a pregnant or lactating whale's energy budget, increase the time needed for her to replenish her energy stores, and ultimately lengthen the birth interval by months or years (van der Hoop et al. 2017; Stewart et al. 2022). There are numerous other sublethal threats, that cetaceans face including habitat loss and degradation, depletion of prey, anthropogenic noise and disturbance, biotoxins, and pathogens. Climate change heightens the threats facing cetaceans through direct, indirect, and cascading effects on habitat, prey, predators, and human activityies in our oceans, rivers, and lakes (Gulland et al. 2022).

The reproductive health of some populations of mysticetes is apparently quite good as they are recovering from the impacts of commercial whaling (Thomas et al. 2016; Fig. 24.2). However, some species of toothed cetaceans (odontocetes) appear less capable than mysticetes of recovering from the severe depletion caused primarily by direct removals through whaling, hunting, and fishery bycatch (Wade et al. 2012; Whitehead and Shin 2022). Wade et al. (2012) suggested that this apparent difference in resilience is at least partly due to the effects of exploitation on highly social odontocetes, including, for example, social disruption, fragmentation of social units, and loss of key individuals. In this chapter, we revisit, update, and expand on these ideas. We do not assume that humans can improve upon what the cetaceans have evolved to do themselves with regard to reproduction. Rather, we consider an important role of conservation biologists is to find ways to preserve, or reestablish,

Fig. 24.1 A large male sperm whale socializing with a group of females and young in waters off the island of Dominica in the Caribbean Sea. Sperm whales are the most sexually dimorphic cetacean in body size. The male's gigantic nose, which is the largest sexually selected organ on the planet (Cranford 1999), contains the spermaceti organ complex, the world's most powerful natural sonar system. The valuable spermaceti oil was part of the impetus for two massive waves of commercial whaling that targeted sperm whales (along with large baleen whales). Post-whaling, population trajectories are varied. Sperm whale populations facing minimal human impact are recovering slowly, but the lingering impacts of whaling may be impeding recovery in some areas by affecting the sex ratio and/or the social cohesion of females. In populations currently experiencing anthropogenic impacts, calving rates are declining (Whitehead and Shin 2022). Photo: ©Flip Nicklin/Minden Pictures; 1994. All rights reserved

the environmental, demographic, and social conditions that would enable cetaceans to reproduce successfully.

As noted by van der Hoop et al. (2017, p 103), "Historically, whale conservation measures have focused on reducing mortality; a shift is required to also address morbidity and the sublethal impacts on individuals and their reproductive rates."

Fig. 24.2 A singing male humpback whale, Maui, Hawaii. Many humpback whale populations have recovered from commercial whaling and some populations are increasing at maximal rates of about 7% per year (Calambokidis et al. 2008; Calambokidis and Barlow 2020). Humpback whale songs are once again reverberating through the ocean soundscape on traditional mating grounds and migratory routes where males sing complex, evolving songs (Darling et al. 2019). While their function and relationship to other aspects of male reproductive behavior remain largely unknown, songs indicate some degree of association between individuals and are generally thought to play a role in breeding (Darling et al. 2019). As human activities in the oceans increase, ambient noise levels are rising too, with potential impacts on communication space for humpback whale song. Photo: ©Flip Nicklin/Minden Pictures (NOAA Fisheries permit #19225); 2020. All rights reserved

Many approaches to the management of human-caused mortality involve calculation of reference points, which are considered "best practice" for managing bycatch and other human-induced mortality (Wade et al. 2021). The "potential biological removal" (PBR) level is one specific reference point used in the United States to meet the objectives of the Marine Mammal Protection Act (Wade 1998). PBR input values are designed to account for population differences in reproduction (see Box 24.1), which theoretically allows for the PBR approach to accommodate cases where a population's reproductive rate has been decreased by sublethal human-caused factors.

Our specific objectives are to (1) define resilience in the context of cetacean reproductive health and conservation, (2) review progress on understanding the social conditions necessary for maximizing cetacean reproductive success, (3) summarize the accumulating evidence showing that aspects of cetacean "reproductive health" (fecundity, mating, survival of young) can be impacted by human activities, and (4) suggest ways of using knowledge about cetacean reproductive health to improve management models and strengthen conservation actions and outcomes.

#### 24.2 Resilience

Wade et al. (2012) defined resilience as the ability of a cetacean population to recover from extreme depletion (very low numbers), the condition that some of the large baleen whales had reached by the time commercial whaling was either brought under strict control or otherwise banned. Such use of the term comports with that of psychologists, who regard resilience as a construct with two distinct dimensions, namely, significant adversity (e.g., whaling) and positive adaptation (e.g., ability to recover) (Fleming and Ledogar 2008; see also Hodgson et al. 2015).

Wade et al. (2012) evaluated species or population differences in resilience to extreme depletion. Moore and Reeves (2018) applied the concept of resilience to the ability of cetaceans to adapt to the effects of climate change. Here, we extend this thinking to examine the resilience of cetaceans to disruption of, or damage to, their reproductive health and how behavioral and physiological plasticity, and sociality, may play a role in aspects of reproductive success. Reproductive health can be impaired by some of the same factors that determine an organism's survival (e.g., bycatch, ship strike, acute disease, toxicity), but there are several additional forms of "significant adversity" that affect reproduction itself (e.g., decreased fertility due to high pollutant burden, sublethal injury, or chronic disease, inadequate nutrition, social disruption). Although survival has generally been viewed as the most pertinent parameter for long-lived animals, it is likely that reproduction is just as (or even more) important and relevant in some cases (Manlik 2019).

#### 24.3 The Social Context of Reproduction

Social living can enhance resilience in an increasingly human-dominated ocean (Brakes and Rendell 2022). Here we briefly review our understanding of sociality and its importance to cetacean reproductive health but also how it can increase vulnerability to disruption by human activities. Perrin et al. (1984) and numerous chapters in this book provide examples of how cetaceans may adapt their reproductive strategies depending on body condition, age, and dominance status (Chivers and Danil 2023, this book; Manitzas Hill et al. 2023, this book). Much has also been written about density-dependent changes in female reproduction following commercial exploitation or high levels of incidental mortality in fisheries (reviewed in Hohn et al. 2007). Density-compensatory changes in reproductive parameters, such as decreased age at sexual maturation and increased rates of ovulation and calving following intense harvest or fisheries bycatch, are generally attributed to changes in prey resources (Fowler 1981, 1984; Hohn et al. 2007). Less focus has been given to the impacts of sublethal anthropogenic impacts on reproductive rates, which may result in delayed age of first reproduction, longer interbirth intervals, and/or extended lactation (e.g., Cramer et al. 2008; Ward et al. 2009; McGuire et al. 2020; Stewart et al. 2022).

Despite the attention that social behavior garnered in the early years of conservation biology (Allee 1931; Ehrenfeld 1970) and recently renewed attention (Brakes et al. 2021; Brakes and Rendell 2022), consideration of animal sociality is complex and not easily integrated into conservation actions. Reduction of a local population to a very small size can exacerbate Allee effects ("undercrowding" or densitydecompensation; reviewed in Stephens and Sutherland 1999) and even lead to population collapse (Gilpin and Soulé 1986). When population size is greatly reduced, individuals can have difficulty finding one another for mating (Gascoigne et al. 2009). Antoniou et al. (2018) suggested that a high observed incidence of introgressive hybridization in the Gulf of Corinth, Greece, between an extremely depleted, geographically isolated population of common dolphins (Delphinus delphis) and a less depleted and comparatively large local population of striped dolphins (Stenella coeruleoalba) was due to the scarcity of conspecific mates, a situation referred to as the Hubbs principle, also known as the "desperation hypothesis" (Hubbs 1955). For some species, returning regularly to a specific location could be a mechanism for ensuring that mates can be found. This may be the case for humpback whales (Megaptera novaeangliae), which congregate around tropical and sub-tropical islands in winter, although humpbacks may in fact mate during migration as well (Darling et al. 2019). Reductions to extremely low population sizes can also lead to inbreeding, which has been identified as a factor potentially impeding the recovery of one population of eastern North Pacific salmon-eating killer whales (Orcinus orca) (Lacy et al. 2017; Ford et al. 2018; Kardos et al. 2023).

Group living has numerous benefits (Gowans 2019). For mating and reproduction, these include the ease of finding and assessing a suitable mate, such as in dusky dolphins (Lagenorhynchus obscurus) that engage in scramble competition (Orbach et al. 2014) and in Amazon river dolphins (Inia geoffrensis) that gather in lek-like aggregations (Martin et al. 2008; da Silva and Spinelli 2023, this book). The formation of dominance hierarchies among males presumably confers preferential access to mates and enables females to mate with fit and dominant males (e.g., beaked whales, Alves et al. 2023, this book; narwhals (Monodon monoceros), Graham et al. 2020; Fig. 24.3). Alliance formation, such as in male Indo-Pacific bottlenose dolphins (Tursiops aduncus), provides advantages over rivals and facilitates control of females (Connor 2007), and male "squads" of offshore pantropical spotted dolphins (Stenella attenuata attenuata) may play a role in social ordering and reproduction (Pryor and Shallenberger 1991; Mesnick et al. 2019; Fig. 24.4). Communal calf care and defense against predators are some of the many benefits females may derive from group living; these groups may be temporary or long-lasting associations (Wells 2003; Whitehead 2003; Konrad 2019; Mesnick et al. 2019).

When sociality is disrupted, mating, fecundity, and the ability to raise young can be compromised. Populations of highly social species may take longer than expected to recover from depletion if individuals that enhance reproductive success, such as dominant males and female matriarchs, have been lost. Some populations of sperm whales, for example, have not recovered since the end of commercial whaling, perhaps due to the lingering demographic effects of the removal of large males on

Fig. 24.3 "Tusking" male narwhals, Baffin Island, Nunavut, Canada (1985). The tusk of the narwhal, which is actually a greatly enlarged left-spiraling upper left tooth, usually erupts only in males and can exceed 3 m in length. The tusk likely functions as a signal and a weapon during aggressive disputes between rivals (Graham et al. 2020).  Some populations are still overexploited even though quotas are now established for nearly all areas where narwhals are hunted. A host of other threats are increasing. Noise from vessel traffic, seismic surveys, ice-breaking, fishing, and other sound sources may disturb and stress the whales and decrease their fecundity (NAMMCO 2021). Photo: ©Flip Nicklin/Minden Pictures. All rights reserved

reproduction, while other populations face present-day threats to female social cohesion and pregnancy rates (Whitehead et al. 1997; Gero and Whitehead 2016; Whitehead and Shin 2022). In the eastern tropical Pacific, repeated chase, encirclement, and release of dolphins in the tuna purse seine fishery can cause separation of mothers and calves and decrease weaning and pregnancy rates (Archer et al. 2004) and have negative effects on female reproductive rates (Cramer et al. 2008, Kellar et al. 2013). In one of the populations impacted by the fishery, eastern spinner dolphins (Stenella longirostris orientalis), only a tiny fraction of males examined reached fully active testes weights and were thus likely capable of successful mating, a situation that suggests a polygynous mating system that could be susceptible to perturbation by the fishery (Perrin and Mesnick 2003).

Although the degree to which mating and rearing strategies in cetaceans are socially learned is unknown, there are hints that some aspects are socially transmitted, such as the socio-sexual "dances" within the lek-like aggregations of Amazon river dolphins, where males wave objects in the air, possibly to attract or impress females (Martin et al. 2008; Fig. 24.5). Baleen whales are dispersed over vast areas, which could make locating a suitable mate challenging. Social learning of the timing

Fig. 24.4 Adult male subgroup of offshore pantropical spotted dolphins in the eastern tropical Pacific Ocean. An individual from another adult male subgroup rising from below gapes his jaws in an apparent threat gesture at the group passing over him. Dominant adult male "squads," all with prominent post-anal keels, heavily spotted bodies, and striking facial coloration, swim in precision while other individuals move aside. We know little about the function of these squads, but observations suggest they have a role in social ordering and reproduction (Pryor and Shallenberger 1991). Chase, encirclement, and release from tuna purse seines likely disrupts these and other subgroups in the (Wade et al. 2012; Mesnick et al. 2019). Photo: Karen Pryor; 1979

and routes of migration between feeding and breeding habitat (Carroll et al. 2015), as well as horizontally transmitted song patterns (Garland and Carroll 2022), may have evolved in part to ameliorate the problems associated with long-distance dispersal, although the role of song in male-male interactions, mate selection, and assortative grouping remains enigmatic (Darling et al. 2019; Garland and McGregor 2020; Fig. 24.2). Remarkably, male humpbacks in a population sing fundamentally the same song at any one time, and the song progressively evolves over the course of a season, and over years (Darling et al. 2019). How this is accomplished is not clear, but apparently it involves mutual melding or adoption, which are forms of cultural transmission (Noad 2011; Darling et al. 2019). Similar mechanisms of vocal learning may occur in blue whales (Balaenoptera musculus) and fin whales (Balaenoptera physalus) (McDonald et al. 2006; Archer et al. 2020), in which males typically sing the same song within a region, and in other baleen whale species that sing (Cerchio 2022; Risch 2022), although there is variation in the degree of social conformity and individual innovation among species (Stafford 2022). The importance of social learning is also evident in the evolution of post-reproductive lifespans in killer