Keywords

7.1 Introduction

Non-conceptive sexual behavior (NCSB), or socio-sexual behavior, is sexual in form but does not facilitate direct reproduction and has been reported in more than 300 animal species from insects to primates (Bagemihl 1999; Bailey and Zuk 2009). NCSB often involves mounting interactions during which the participants employ stereotyped copulatory movements (including pelvic thrusting) in non-reproductive contexts. NCSB can occur between two sexually immature individuals (Gunst et al. 2013), sexually immature and sexually mature (Ogawa 2006), two same-sex sexually mature animals (Hohmann and Fruth 2000), two opposite-sex sexually mature animals (Gunst et al. 2020), or even between different species (Gunst et al. 2018). Socio-sexual behavior is a subset of NCSB that appears sexual in terms of its outward form but is thought to primarily be used to mediate adaptive goals that are not directly related to reproductive coitus (Wickler 1967). These adaptive goals are often employed to solve social problems the participants encounter.

Multiple functions have been proposed for NCSB, including practice for reproduction, attracting opposite-sex mates, reducing the reproductive opportunities of same-sex conspecifics, reinforcing dominance relationships, alliance formation, reconciliation, and social tension reduction (reviewed in Vasey 1995; Bagemihl 1999; Bailey and Zuk 2009). For example, female mountain gorillas (Gorilla g. beringei) may use NCSB to re-affirm dominance hierarchy (Grueter and Stoinski 2016). In Japanese macaques (Macaca fuscata), sexually mature females mount sexually mature males (often with pelvic thrusting), which prompts the male to mount the female (Gunst et al. 2020). Mutual genital contact, where one animal touches the genitals of the other and vice versa, between male yellow baboons (Papio cynocephalus anubis) appears to facilitate alliance formation (Smuts and Watanabe 1990), and ventro-dorsal mounting among female vervet monkeys (Cercopithecus aethiops) appears to achieve the same function (Fairbanks 2002).

The topic of NCSB has been most studied in primates; however, non-primate exemplars do exist. For example, courtship behavior, mounting, and pair-bonding appear to facilitate alliance formation between male graylag geese (Anser anser; Kotrschal et al. 2006). Research on NCSB has also focused on smaller animals with little attention to large mammalian species, although, once again, exceptions exist (Hill et al. 2014). For example, evidence suggests that mounting between domestic cattle helps reinforce dominance relationships during periods of social uncertainty and stress (Klemm et al. 1983). For the most part, however, NCSB appears to be characterized by some mixture of both sexual and socio-sexual motivations (Vasey 1995; Bagemihl 1999). In bonobos (Pan paniscus), genito-genital rubbing is accompanied by vocalizations and facial expressions that are indicative of sexual reward, but it also appears to reduce social tension associated with food sharing (Hohmann and Fruth 2000).

Steadily increasing interest in cetaceans over the past 70 years has led to an explosion in the literature on various behavioral topics for these aquatic mammals. This growth in focus and the ability to study smaller cetacean species housed in managed care facilities have enabled a substantial increase in knowledge (e.g., behavior, physiology; see Chap. 10). This chapter reviews the literature on NCSB in cetaceans by outlining the distribution among species, general behavioral repertoire, and potential functions (Table 7.1).

Table 7.1 Hypotheses and predictions on the function of non-conceptive sexual behaviors
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7.2 Distribution of NCSB Across Mysticeti and Odontoceti

To illustrate the widespread distribution of NCSB across Cetacea, we created a cladogram using cladistic data from ten K tree project data (Arnold et al. 2010) and FigTree (Rambaut 2018). To date, 35 of the 87 extant species of Cetacea have been observed engaging in NCSB, in both managed care facilities and wild settings, with some species engaging in inter-species NCSB (Fig. 7.1). However, we suspect this is an underestimation as many cetaceans are under-studied (e.g., Ziphiidae, beaked whales). Evidence for this underestimation was found when comparing the research effort (i.e., the number of articles published on each species of Cetacea) as reported by Fox et al. (2017), compared to the presence or absence of NCSB. Employing a logistic regression (R Core Team 2020), we found that the number of articles previously published on a given species, as reported by Fox et al. 2017, predicted the presence or absence of NCSB in a given species that we report in this chapter (χ288 = 95.89, p < 0.001). This finding suggests that as species are studied more, evidence for NCSB in additional species will be found; though, this is a crude measurement and should only be used to encourage the study of behavior in species that are rarely reported on. This might be true of the highly cryptic Ziphiidae, which are rarely observed despite the number of species (i.e., more than 19) within this family. However, this prediction may be inaccurate as gregarious species, and thus the ones most likely to engage in NCSB, are more frequently studied. With increased behavioral observation through the use of drones (reviewed by Whitt et al. 2020; Ramos et al. 2023, this book), we suspect more species will be observed engaging in NCSB and that this behavior will be understood in greater detail (e.g., Orbach et al. 2020); though other factors, such as social structure, are far more important in predicting if a species engages in NCSB.

Fig. 7.1
A cladogram depicts the known species of cetacean. The squares indicate the gender of the species, the triangles indicate the environment, and the circles indicate non-conceptive sexual behavior.

A cladogram of all known species of cetacean. The cladogram represents species that we know engage in non-conceptive sexual behavior (NCSB), the environment NCSB have been observed in, the sex of the animals that have been described engaging in NCSB, and if they engage in NCSB with species other than their own. Star symbols indicate the presence of interspecies sexual behavior. White squares indicate that NCSB has been observed in males, gray indicate NCSB has been observed in females, and black squares indicate both sexes have been observed engaging in NCSB. White triangles indicate NCSB has been observed in the wild, gray indicate NCSB has been observed in managed care, and black triangles indicate NCSB has been observed in both environments. Finally, white circles indicate that NCSB is absent or has not been reported, while black circles indicate NCSB has observed in that species

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7.3 Behavioral Repertoire and Physical Form of NCSB

While most prominent in toothed whales, many species of baleen whales have also been observed engaging in NCSB with the behavioral repertoire of NCSB described across species showing similarities. Typically, NCSB consists of a few behaviors (e.g., thrusting, intromission, genital presentation, genital contact or manipulation, penile erections, and contact of another’s body with an individual’s ventral area); however, bouts of NCSB can also consist of just one of the behaviors listed in Table 7.2. Many of these behaviors (e.g., penile erections and ventral contact) also occur during courtship (e.g., Hill et al. 2015; Lilley et al. 2022), so describing the partners involved is important when deciphering if the behavior being observed is non-conceptive or copulatory. Species-specific descriptions of behavior, as well as corresponding references, are available as Supplementary Material.

Table 7.2 An ethogram of non-conceptive sexual behaviors
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NCSB can be contactless (Fig. 7.2) or involve physical contact (Fig. 7.3). For example, beluga whales (white whales, Delphinapterus leucas) engage in s-posture sexual presentations and lateral sexual presentations frequently without contact (Lilley et al. 2022), with sexually mature males often doing so toward sexually immature individuals (Hill et al. 2015; Lilley et al. 2020) (Fig. 7.4). Bubbles also seem to be a part of the beluga NCSB repertoire and may be used to communicate, either as a visual signal or as a result of vocalization (Hill et al. 2015). However, insertion, intromission, genital rubbing, mouthing, thrusting, and petting involve contact, whether it be with a conspecific, heterospecific, or inanimate object. Both contactless and contact NCSB occur between same-sex partners (male-male and female-female pairings) and mixed-sex partners, age-matched and non-age-matched partners, and between different species.

Fig. 7.2
An illustration of two whales. A sexually mature male with a penile erection is depicted on the top and an immature male with a penile erection is depicted at the bottom.

A form of non-tactile sexual behavior exhibited by humpback whales. Known as penis extrusions, an immature and sexually mature male swims with penile erections (Illustration by Nichole Ham and inspired by Pack et al. (2002))

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NCSB is most easily recognized when the partners are incapable of reproduction (i.e., two males or two females engaging in NSCB, two sexually immature animals engaging in NSCB, one sexually mature and one sexually immature animal engaging in NCSB, between two species that cannot produce hybrids) or with a dead conspecific (i.e., necrocoitus; Dudzinski et al. 2003; Kincaid et al. 2022). In addition, sexual behavior with an object or the environment (e.g., masturbation) is also a form of NCSB. When sexual behavior occurs between mixed-sex pairs and both animals are sexually mature, it is very difficult to determine if the behavior observed was NCSB in context or conceptive behavior, unless life history or hormonal information is available (e.g., age, sex, pregnancy status). For that reason, we describe behavior between same-sex partners, sexually mature-immature partners, or behavior between two species, with the caveat that NCSB likely also occurs between sexually mature mixed-sex partners. As well, in some species, NCSB may occur between multiple partners simultaneously (e.g., surface-active groups; Parks et al. 2007) (Fig. 7.5).

Fig. 7.3
An illustration of the sexual intercourse between two spinner dolphins. The dolphin on the right inserts its beak into the genital slit of the dolphin on the left.

Beak-to-genital contact made by spinner dolphins. In this case, a female inserts her beak into the genital slit of a male dolphin (Illustration by Nichole Ham and inspired by Norris and Dohl (1980) and Wells (1984))

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Fig. 7.4
An illustration of a mature beluga whale and an immature whale. A sexually mature male beluga with a penile erection is depicted on the left and a sexually immature whale is depicted on the right.

A sexually mature male beluga exhibits an s-posture display, with a penile erection, toward a sexually immature whale. This, a non-tactile form of non-conceptive sexual behavior, is a sexual display used during courtship and in bouts socio-sexual behavior and sexual play (Hill et al. 2015; Lilley et al. 2020; Ham et al. 2022) (Illustration by Nichole Ham and inspired by Hill et al. (2015))

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Fig. 7.5
An illustration of three whales. The two whales on the left are involved in sexual intercourse. One of the whales scrapes its ventral region on a sexually immature whale.

Right whales engaging in tactile sexual activity. A male rubs his ventral region on a sexually immature while a third whale is present. Often characterized as a surface active group, this illustration is inspired by Donnelly (1967), Kraus and Hatch (2001), Parks et al. (2007), and Lonati et al. (2022) (Illustration by Nichole Ham)

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7.4 Possible Functions of NCSB

For some species, NCSB emerges within the first months of life, while for others it takes much longer. For example, thrusts and erections in sexually immature bottlenose dolphins (Tursiops spp.) and Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) emerge in the early months of life (Mann 2006; Xian et al. 2010), whereas thrusts are only observed after the first few months and erections after the first year of life in beluga whales (Ham et al. 2022). This variation could be due to differences in developmental timelines, juvenile periods, or social structures, but understanding the emergence of a behavior ultimately provides clues to the function of the behavior (e.g., practice, social bonding). Detailed studies of the development of NCSB can provide clues to the function, benefit, and adaptive value these behaviors might have on mating ecology, social relationship management, and the development of sexual behavior (Table 7.1).

7.4.1 Managing Social Relationships: Dominance, Greeting Behavior, and Bonding

While tooth raking is frequently associated with agonism and dominance relationships (Scott et al. 2005; Lee et al. 2019; Ham et al. 2021a; Grimes et al. 2022), NCSB has also been suggested to play a role in the formation of dominance relationships (Östman 1991; Mann 2006; Wu et al. 2010; Furuichi et al. 2014; Harvey et al. 2017; Serres et al. 2021) and may even occur at the same time. Dominance relationships among individuals may influence the success of copulatory behavior. One interesting question should be explored: are those that are more dominant more successful in copulatory behavior? Further, are these animals more successful because they are more dominant or because they engage in NCSB more frequently to maintain their dominance position or both? Studying the dominance position and number of offspring, in addition to the frequency of NCSB, for a given individual would begin to answer some of these questions.

In addition to dominance, same-sex NCSB can help manage social relationships or reduce social tension, especially for those species where social groups include unrelated individuals, as in some primates (reviewed by Vasey 1995; Furuichi et al. 2014). There is also evidence that dolphins employ NCSB in managing social relations (Tursiops spp.; Würsig and Würsig 1979; Connor and Mann 2006; Mann 2006; Harvey et al. 2017; Stenella longirostris, Norris and Dohl 1980; Sousa spp. Saayman and Tayler 1979; Lagenorhynchus obscurus, Würsig and Pearson 2014). This function may be especially true for those species that live in large pods and/or fission-fusion groups such as bottlenose dolphins, in which social relationships must be continuously negotiated, re-established, and re-affirmed. Long-term studies of Indian Ocean bottlenose dolphins (T. aduncus) have found that male dolphins develop long-lasting bonds or alliances with other males (Connor et al. 1992, 2001, 2006, 2022) characterized by recurrent NCSB and symmetrical relationships (Mann 2006).

For some species, including bottlenose dolphins in managed care facilities, sexual play occurs nearly every day (Brown and Norris 1956). Studies of wild cetaceans have reported frequent NCSB (Johnson and Norris 1994; Connor et al. 2000; Mann 2006). For example, male bottlenose dolphin calves engage in NCSB at a rate of 2.38 interactions per hour (Mann 2006), which is quite frequent considering the generally poor visibility conditions which obstruct the human observers. Additionally, despite displaying typical copulatory behavior with sexually mature females on a seasonal basis, sexually mature male beluga whales in managed care facilities display a high frequency of NCSB throughout the year, except the month of peak conceptive behavior when male-male NCSB almost completely stops (Glabicky et al. 2010). With increasing age, the NCSB of beluga whales becomes seasonal, suggesting that maturity and fluctuation in hormone levels might be drivers (Ham et al. 2021b). The decrease in male-male pelvic thrusting during the months when beluga whales are mating suggests that pelvic thrusting serves both as a copulatory function (when directed toward females) and as a form of NCSB (when directed toward males). During the non-breeding months, the NCSB of same-sex thrusting seems to serve an adaptive social function such as social bonding or dominance hierarchy maintenance (Glabicky et al. 2010). Thus, for beluga whales, NCSB does not take the place of reproductive conceptive behavior but does seem to occupy a larger portion of a male beluga’s social interactions. Furthermore, s-posturing in beluga whales occurs in both agonistic/aggressive displays and courting displays (e.g., Hill et al. 2015), but the s-postures have different topographies in each context. The overlap of behaviors in sexual and aggressive contexts could be a result of dominance relationships being displayed and reinforced through both sexual means and aggressive displays or could be the result of specific behaviors taking on different meanings in different contexts. NCSB in beluga whales is highly reciprocal (Lilley et al. 2020; Manitzas Hill et al. 2022), at least between sexually mature males and sexually immature males, so more information on the reciprocity of such behavior is needed to determine if dominance is a possible function for this species.

Not only does NCSB occur before sexual maturity in some cetacean species, NCSB also occurs among individuals who are post-reproductive. For example, female short-finned pilot whales (Globicephala macrorhynchus), which have a post-reproductive phase of their life (Acevedo-Gutiérrez 2018) and live in mixed sex and age, mid-sized pods (Fox et al. 2017), were found to have spermatozoa in their reproductive tract, postmortem (Kasuya et al. 1993). This suggests that although the females were no longer reproducing, they were still involved in sexual activity (Kasuya et al. 1993). The complex social groupings of short-finned pilot whales might explain the use of NCSB in non-reproductive females if they are employing NCSB to manage social relations.

In some killer whale (Orcinus orca) populations, differing matrilines/pods congregate seasonally when males of differing ages from different pods join, forming a temporary all-male group (Bagemihl 1999; Baird 2000). Once formed, the males engage in energetic NCSB. Around 90% of the observed male-male NCSB is reciprocal and includes turn-taking of genital rubbing (Bisther and Vongraven 1995; Bagemihl 1999). Despite the formation of all male pods of dissimilar ages, “adolescent” killer whales (12–25 years old) engage in these behaviors the most (Bagemihl 1999; Baird 2000). Individuals have partner preferences, interacting with the same conspecific year after year (Bagemihl 1999). More recently, an anecdotal report describes a mature and immature male engaging in genital-genital rubbing, with penile erections, in reciprocal manner (Sanvito and Galimberti 2022). In managed care facilities, reciprocation in killer whales is also observed, and it is seemingly used in managing social relations (Sánchez-Hernández et al. 2019). For killer whales, it seems that NCSB is being used as “social glue” (see Bailey and Zuk 2009) not only between members of the same pod but also among pods that coinhabit the same area.

It seems that NCSB is used by many cetacean species as a greeting behavior in brief meetings with other pods and even between different species (Saayman and Tayler 1979; Würsig and Würsig 1979, 1980; Heimlich-Boran 1988; Bisther and Vongraven 1995; Rendell and Whitehead 2001; Dudzinski 2010; Dudzinski et al. 2010; Nakamura and Sakai 2014; Würsig and Pearson 2014). NCSB-driven greeting rituals may be used as a way to evaluate the physical ability of the novel pod members as occurs in some primates and rodents (Pellis and Iwaniuk 1999; Smith et al. 1999). More observations of social group meetings and reunions are necessary to further investigate the role of NCSB as ritual greetings. Similarly, when animals living in managed care facilities are moved from one facility to another, researchers/veterinarians/animal care staff should assess if NCSB is employed when animals are first introduced to one another, although this could also be a display of dominance.

To further understand the function of NCSB with respect to dominance, bonding, and other social functions of NCSB, more detailed analyses are needed, where observers note the partners involved and the results of behaviors. Given the high frequency of occurrence and prevalence across cetacean species (Fig. 7.1), NCSB is likely a very important aspect of cetacean social behavior.

7.4.2 Learning

NCSB might be used to practice general motor skills (D’Agostino et al. 2017), especially during sensitive periods of development (Byers 1998), and has also been suggested to be of potential importance for successful conceptive behavior later in life (Fairbanks 2002; Mann 2006), which may be more challenging in the three-dimensional aquatic environment. While empirical evidence of sexually immature animals engaging in NCSB to practice copulatory behavior is limited, this has been suggested for many species (beluga whales; Glabicky et al. 2010; Hill and Ramirez 2014; Hill et al. 2015; Lilley et al. 2020; Manitzas Hill et al. 2022; right whales (Eubalaena spp.); Thomas and Taber 1984; Kraus and Hatch 2001; Parks et al. 2007; D’Agostino et al. 2017; killer whales; Baird 2000; harbor porpoises (Phocoena phocoena); Keener et al. 2018; spinner dolphins; Estrade and Dulau 2017; bottlenose dolphins; Scott et al. 2005; Connor and Mann 2006; Kuczaj et al. 2006; Mann 2006; Kuczaj and Eskelinen 2014; Delfour et al. 2017; Harvey et al. 2017). The often-playful expression of NCSB may help fine-tune and enhance an individual’s ability to copulate. It may be the case that engaging in NCSB play is essential to learning how to copulate. In flies (Drosophila spp.), the individuals that engaged in same-sex NCSB had a higher copulatory success rate (McRobert and Tompkins 1988) demonstrating the importance of NCSB. Turtles (Chrysemys, Graptemys, Pseudemys, and Trachemys) also engage in precocious NCSB, which supports that this form of “play” occurs across many taxa (reviewed by Burghardt 2005). Mann (2006) suggests that this “practice may be more important in dolphins than terrestrial mammals because cetaceans are constantly in motion and females can easily turn belly-up or away from males during mating attempts” (p. 126).

To understand how important engaging in NCSB from a young age to learn and practice copulatory behavior requires further observational evidence. For example, comparing the frequency and form of NCSB as a sexually immature individual to how many offspring an individual has may provide some evidence on how important early NCSB experiences are. Immature male beluga whales with access to sexually mature males develop their sexual repertoire faster than those who did not have access to mature males (Ham et al. 2022). This variation in development does not confirm whether those beluga whales will be more successful in future copulatory behavior, but it suggests there is an element of learning involved. For populations where the life history of individuals is known (e.g., managed care facility beluga populations, bottlenose dolphins in Shark Bay), we suggest that the frequency of NCSB and the copulatory success rate be explored in tandem to determine if NCSB is learned and if the individuals who engage in more NCSB are more successful in copulatory behavior.

7.4.3 Pleasure

Another potential reason cetaceans engage in NCSB is that such behavior is pleasurable (Dudzinski et al. 2012). Whether it be masturbation on an inanimate surface or by rubbing on a conspecific, cetaceans likely experience a pleasurable sensation (Brennan et al. 2022). This does not exclude the possibility of adaptive functions. For example, the behavior might function to regulate dominance or manage social relations while also pleasurable and rewarding. However, the most obvious indication that this behavior may be pleasurable comes from observing cetaceans engaging in masturbation by themselves even though social partners are available.

Masturbation or genital rubbing has been described in toothed whales (McBride and Hebb 1948; McBride and Kritzler 1951; Spotte 1967; Caldwell and Caldwell 1977; Shane et al. 1986; Caldwell et al. 1989; Boede et al. 2018) and in baleen whales (Herman et al. 1980; Glockner-Ferrari and Ferrari 1985) and can even lead to ejaculation (Terry 1984). While most typically described in males—likely due to the obvious nature of the behavior, especially when the animal has a penile erection—females have also been observed masturbating (McBride and Kritzler 1951). A number of anecdotal reports describe female bottlenose dolphins engaging in a myriad of genital stimulation activities, including walls, objects, water, and each other (M. Sakai, personal communication, The Dolphin Company, Dolphin Quest). Bottlenose dolphin females possess a highly innervated and highly sensitive clitoris, suggesting that female masturbation and other NCSB are pleasurable (Brennan et al. 2022).

7.4.4 Play

If NCSB is performed in a playful context, it may be pleasurable and “fun” because it is cognitively stimulating (Kuczaj and Eskelinen 2014; Serres and Delfour 2017) and may even serve as a good indicator of positive welfare in both wild and managed care settings (Held and Špinka 2011; Ahloy-Dallaire et al. 2018). Many cetaceans engage in sexual play with others, also called “socio-sexual behavior” within the literature, although it should be classified as a type of play behavior (e.g., McBride and Hebb 1948; Brown and Norris 1956; Sauer 1963; Xian et al. 2010; Würsig 2018; Soriano Jimenez et al. 2021). These sexual play behaviors, most frequently reported in young animals (Thomas and Taber 1984; Mann 2006; Parks et al. 2007; Lilley et al. 2020; Manitzas Hill et al. 2022, this book), seem to be mostly exhibited in a social context where two or more animals incorporate aspects of their sexual repertoire (Table 7.2) into their rough-and-tumble play. It seems that cetaceans also incorporate sexual play in social or cooperative object play (Entiauspe-Neto et al. 2022). However, animals also engage in sexual play with objects in non-social contexts (Martin et al. 2008; Araújo and Wang 2012; Hill et al. 2015, da Silva and Spinelli 2023, this book).

Detailed studies of socio-sexual play in beluga whales (e.g., Hill et al. 2015; Lilley et al. 2020; Ham et al. 2022) and bottlenose dolphins (e.g., Mann 2006; Mackey et al. 2014) have revealed that the play of sexually immature animals influences social bonding and that there are sex differences in both the behaviors observed and the frequency in which males and females engage in sexual play. For beluga whales, sexual behaviors developed in a piece-meal fashion (Ham et al. 2022), with simpler behaviors (e.g., genital rubs) emerging before more complex behavior patterns (e.g., thrusting). Further, female and male immature beluga whales prefer to play with older males when engaging in NCSB, but prefer to play with same-age and -sex partners when engaging in non-sexual rough-and-tumble play (Ham et al. 2023). While sexually immature NCSB may be “fun,” it the form of this sexual play suggests it might also be used in learning or practicing copulatory behaviors.

7.5 Why Sexualize a Social Behavior?

NCSB does not appear to serve just one function for any one cetacean species. The use of NCSB is widespread and can be used as communication (Gaskin 1982; Tyack 2000), self-pleasure (Dudzinski et al. 2012), dominance (Östman 1991; Mann 2006; Wu et al. 2010; Furuichi et al. 2014), or as a type of play (Dudzinski 1998; Mann 2006; Hill and Campbell 2014; D’Agostino et al. 2017). The combination of functions NCSB might serve for any given cetacean species depends on sociality and conceptive behavior strategy, among other factors such as age, sex, and species. Although the overall behavioral repertoire might look similar, the underlying mechanisms and functionality appear variable. This variability is likely greatly influenced by the overall sociality of the cetacean species itself (Fox et al. 2017). For species that live in large pods, there is a greater opportunity for NCSB to occur, and NCSB may be less costly as there are multiple opportunities for reproduction. However, both conditions likely facilitate the increasingly diverse functions of the behavior. In contrast, relatively solitary whales, such as gray whales, may only engage in NCSB/NCSB during specific times of the year when they aggregate in social groups, such as during the mating season (Gilmore 1960; Swartz 1986). Species differences must be considered when trying to make sense of the functions of NCSB, if any.

One of the biggest questions that results from studying NCSB is, what value is added by sexualizing a social interaction? Why add a sexual component to social behaviors that could be otherwise devoid of sex? Despite there not being a concrete answer for cetaceans at this time, the following hypotheses can be formed: (1) NCSB allows for specific social bonding that other forms of contact do not, specifically in fission/fusion societies, where bonds have to be re-established quickly, it may be more effective than other social interactions that are devoid of sex; (2) NCSB is necessary for both learning and practicing in order to reproduce later; and (3) NCSB is associated with immediate sexual reward (i.e., pleasure). Bailey and Zuk (2009) provide a number of explanations for why same-sex NCSB has been adaptive for many diverse species; for example, flies engage in NSCB to practice sexual behavior, and American bison (Bison bison) use NCSB to manage intrasexual conflict. More recently, Monk et al. (2019) posited that same-sex NCSB is not the evolutionary paradox it was once thought to be. For cetaceans, NCSB, and specifically same-sex NCSB, is quite prevalent and could be due to a number of explanations. To Monk et al.’s (2019) point, this behavior seems characteristic of many species and a normal occurrence, even though it was not scientifically documented until relatively recently.

NCSB is an important part of many cetacean species’ behavioral repertoire, comprising a substantial portion of their daily lives (e.g., Lilley et al. 2020). NCSB is important to study for exactly this reason. Although not directly used for reproduction, these behaviors can still be used to satisfy social demands. By understanding NCSB, we further our understanding of reproductive behavior and social relationships in non-human species (Vasey 1995; Bailey and Zuk 2009; Xian et al. 2010).

7.6 Conservation, Welfare, and Future Research

Beyond the basic science to better understand animal behavior, understanding NCSB can affect conservation and welfare in several ways. For example, there is evidence that for some species, individuals had better reproductive success if they participated in NCSB prior to sexual maturity (e.g., Drosophila spp., McRobert and Tompkins 1988). If practice is necessary for successful offspring production or practice makes an individual more reproductively successful, individuals with access to the appropriate setting for NCSB (e.g., social group composition) would have a fitness advantage. Although paternity success as the result of NCSB prevalence has yet to be examined in many cetacean species, evidence in beluga whales points to the gradual development of the socio-sexual repertoire (Lilley et al. 2020; Ham et al. 2022). Specifically, behaviors non-essential for reproduction, such as genital rubs, were present early in life, but pelvic thrusts were not commonly part of the NCSB repertoire until beluga whales were sexually immature.

The exact social composition conducive to NCSB needs to be examined in further research and might vary by species. For example, young beluga whales were most likely to participate in NCSB when other young, and mostly male, conspecifics were present (Lilley et al. 2020), and sexually mature male beluga whales are most likely to engage in NCSB with other sexually mature males (Glabicky et al. 2010). If sexually mature males serve as role models for NCSB, even only occasionally, then social group composition might be very important for the continuation of endangered cetacean populations or species. Anecdotal observations have reported that sexually immature male bottlenose dolphins (T. truncatus) watch sexually mature males engage in a variety of attention-getting behavior in the presence of interested sexually mature females, supporting the hypothesis of mentoring in some species of odontocetes (personal communication, K. Dudzinski). For example, small populations of killer whales with seasonal breeding congregations may particularly benefit from NCSB if it indirectly enhances survival or reproductive potential.

Aside from conservation issues, the social welfare of some species may be enhanced by opportunities to engage in NCSB. In cetacean species that form long-term bonds with certain individuals (e.g., alliance formation in bottlenose dolphins), engaging in NCSB may facilitate those bonds, increase group cohesion, and provide social welfare benefits. NCSB may also help alliances form and therefore also increases reproductive fitness by contributing to the reproductive success of the male dolphins in alliances. At least for bottlenose dolphins, welfare appears to vary by access to and engagement with conspecifics (Clegg and Delfour 2018). This relationship could be tested in other species to determine the extent to which NCSB might impact social well-being.

7.7 Conclusions

Overall, there is much work to be done on the topic of NCSB in cetaceans. For many cetacean species, it is unknown if NCSB is exhibited at all, and for many of the species in which NCSB has been documented, there has yet to be a systematic study of ontogeny, repertoire, welfare benefits, or fitness benefits. The work thus far has provided evidence that NCSB is common and is also more important than simply an exaptation of reproductive behavior. Further, with the knowledge that many species engage in NCSB, researchers should aim to move beyond post hoc attribution of socio-sexual functions and work toward rigorous hypothesis testing to determine if NCSB is truly NCSB and has adaptive functions (Vasey 1995).

While we have attempted to provide discrete categories as to the function of NCSB to explain why cetaceans engage this behavior, our suggestions are likely over-simplified (Table 7.1). It is most plausible that for many species, NCSB is often playful—especially when sexually immature—but aids in social bond formation (with peers, their mother, and others) and social relation management. It is reinforced by the pleasurable nature of NCSB and, ultimately, improves reproductive outcomes, especially when the NCSB mirrors copulatory behavior patterns. With new observation techniques, such as drone recording and autonomous surface vehicles (reviewed by Whitt et al. 2020) and animals in managed care facilities, these studies are possible and should be explored, especially in those species that have been reported previously to engage in NCSB.