Right Whale Sexual Strategies and Behavior

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 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.

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).

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

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.

North Atlantic and southern right whales are tracked over time using photo and video images of natural markings called callosities, unique patterns of keratin-structured 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 mother-calf 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 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)).

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. His light gray penis is moving across the female’s genital area. Moira Brown, Canadian Whale Institute

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). Females, who invest heavily in offspring, are the limiting sex while males invest relatively little and compete for access to females. 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).

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

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

Males have a fibroelastic penis that is a flexible and mobile organ and the actual act of intromission is quite passive. 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 post-ejaculatory 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 density-dependent 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 photo-identification 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 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).

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

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 shore-based 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). The penile contractions observed were interpreted to be a male orgasm and deposition of sperm with the penis softening and contracting into the genital slit followed by about 20 s of close contact before leisurely swimming away together until out of sight (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).

There are a few records of non-conceptive sexual behavior between a calf and an adult male. 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). An underwater video camera captured footage of the male inserting its penis into the calf genital slit (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. One event was filmed using a drone and the male appeared to probe the calf’s genital region with his extended penis underwater while the calf rolled, thrashed, and arched (Fig. 23.6) (Lonati et al. 2022). 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 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).

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

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 climate-induced 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 human-induced 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 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).

Fig. 23.7

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

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).