Beaked Whale Sexual Dimorphism, Mating Strategies, and Diversification

Abstract

Beaked whales (Ziphiidae), with 24 currently recognized species, are arguably the least known large animals on the planet, despite being widespread and at times abundant. Mesoplodon, with 16 currently recognized species, is by far the most speciose cetacean genus. Recent technological and taxonomic advances, long-term photographic-identification studies, and historical whaling data have allowed new insights into their social and mating strategies and how these may have driven diversification within the family. In most beaked whales, only adult males have exposed teeth—a single “tusk” erupts from each lower jaw and is used in contests to determine access to breeding females. How forcefully males of different species engage conspecifics varies widely based mainly on differences in tooth size/placement and jaw structure. We compiled data on key dimorphic traits including beak modification, tooth size and location, and prevalence of scarring in adults, for all beaked whales. More detailed information is given for the four best-studied species—northern bottlenose whale and Baird’s, Cuvier’s, and Blainville’s beaked whales. We then compared these traits with what is known about their social organization and reproductive anatomy to make inferences about mating strategies. More aggressive species tend to occur in small groups with only one dominant adult male present and have small testes relative to body size, suggesting that male reproductive success is largely determined by precopulatory contest competition and female defense polygyny. Less aggressive species tend to occur (at least at times) in larger, mixed-sex groups with multiple adult males present, and females may mate with multiple males, which favors postcopulatory sperm competition and polygynandry. We further discuss how conflicting pressures arising from males using their beaks for both feeding and fighting could have sparked an adaptive radiation in tooth development and beak morphology among beaked whales, especially within Mesoplodon, which would have had implications for male-male competition, social structure, sexual strategies, and, perhaps ultimately, evolutionary divergence and speciation within this group.

17.1 Introduction

Sexual selection is responsible for the evolution of some of nature’s most extravagant animal features, endowing males with showy ornaments to attract receptive females and equipping others with an arsenal of weapons to fight for them (Darwin 1871; Emlen 2008). As part of a strategy for acquiring mates in the deep oceans of the world, male beaked whales (Ziphiidae) famously use the combat option, brandishing enlarged tusks or a weaponized melon for their armament and a reinforced beak for armor (Heyning 1984; Gowans and Rendell 1999; MacLeod 2002; Lambert et al. 2010). These whales comprise the second most diverse cetacean family (after Delphinidae), and although the evolutionary drivers behind this diversification are unknown, sexual selection, in which males battle over reproductive access to females, likely plays an important role (Dalebout et al. 2008; Steeman et al. 2009; Lambert et al. 2011). In this chapter, we review morphological diversity among extant beaked whales and discuss possible socio-ecological drivers of this diversification.

17.2 Background

Beaked whales first appeared in the early Miocene, and by the middle Miocene, a major diversification had occurred, related to sexually selected modifications to the beak and teeth for mandibular tusk development in adult males (Lambert et al. 2010; Bianucci et al. 2016; Ramassamy 2016). Today, there are 24 known species in 6 genera: Berardius, Hyperoodon, Indopacetus, Tasmacetus, and Ziphius include 8 species, while Mesoplodon is by far the most speciose cetacean genus, with 16 currently recognized species. All extant beaked whales are deep divers that prey mainly on meso- and benthopelagic fish and squids (MacLeod and D’Amico 2006). They show a remarkable range of sexual dimorphism, most of which pertains to modification to male feeding and fighting apparatus—teeth and beaks.

Beaked whales are thought to feed primarily by suction feeding, which has resulted in a significant reduction in the number of functional teeth (Heyning and Mead 1996; Werth 2006). The females and young in most species do not have erupted teeth, while adult males retain one or two pairs of enlarged mandibular teeth as tusks for fighting with other males, most likely used to establish dominance and determine access to breeding females (Heyning 1989; MacLeod 2002). Interestingly, despite the prevalence and severity of scarring among males of various species, there are no reported observations of males using their tusks in actual battles. There is a wide and diagnostic array of variations in the number, shape, size, and location of teeth in beaked whales (Table 17.1; Mead 1989; Dalebout et al. 2008). In adult males of most species, a single, enlarged tooth erupts from each lower jaw. The exceptions are from the two most basal genera (Bianucci et al. 2016; McGowen et al. 2020); in Berardius spp., both sexes have a pair of teeth in the tip of each lower jaw, and in Shepherd’s beaked whale Tasmacetus shepherdi, both sexes have a full set of functional teeth, with an enlarged tooth at the tip of each mandible that erupts only in adult males. In the four remaining genera (Hyperoodon, Ziphius, Indopacetus, Mesoplodon), males retain a single pair of functional teeth. Given the prevalence of contest competition among living ziphiids, they show surprisingly little sexual size dimorphism (Box 17.1): except for the northern bottlenose whale H. ampullatus in which males are considerably larger than females (Gowans et al. 2000). Overall, for species in which there are data, there is little dimorphism in body size, although females may be slightly larger in some species (Table 17.1; MacLeod 2006, 2018).

Table 17.1 Aggression in male beaked whales

Box 17.1 Size Relationships Between Sexes

When males engage in direct combat for females, males are usually larger than females (Clutton-Brock 1989; e.g., sperm whales Physeter macrocephalus, Amazon river dolphins Inia geoffrensis; Dines et al. 2015). When males are much larger than females, they are not the optimal size for foraging and traveling with groups of females and young (Weiss et al. 2021) and may spatially or socially segregate (Whitehead 2003; Martin and da Silva 2004; Foster et al. 2012). Most beaked whales are monomorphic with respect to body size (MacLeod 2006)—is it because males generally occupy the same range and habitats year-round as females? Agility could aid in contests between males, or males might form alliances to increase their “size” (Tolley et al. 1995).

Based on an analysis of group sizes, MacLeod and D’Amico (2006) suggested that there may be two different social structures among beaked whale species. Longman’s I. pacificus and Baird’s beaked whales B. bairdii occur in large groups (up to 100 individuals, mean group size of 19 and 8 individuals, respectively). In contrast, Cuvier’s beaked whale Z. cavirostris, bottlenose whales Hyperoodon spp., and mesoplodonts Mesoplodon spp. occur in small groups (averages ranging from 2 to 4 individuals, maximum group size ~20). Among these, large groups usually comprise multiple adult males with females and immatures, while small groups typically include one or two adult males together with females and immatures (MacLeod and D’Amico 2006; MacLeod 2018).

17.3 Four Species of Beaked Whales

Detailed information about the biology and social organization for the four best-known beaked whale species is summarized below, highlighting what is known about their mating strategies.

17.3.1 Northern Bottlenose Whale

The northern bottlenose whale is endemic to the North Atlantic, where it inhabits temperate to arctic waters, with an apparent preference for deep continental slope areas (> 500 m; Moors-Murphy 2018). Large-scale migratory movements are unresolved, as some suggest that the whales undertake seasonal north/south migrations (Gray and Flower 1882; Benjaminsen and Christensen 1979; MacLeod et al. 2004) while others suggest inshore/offshore movements because sightings are observed in part of their range year-round (Whitehead and Hooker 2012).

Life history information comes largely from whaling and stranding data (Benjaminsen 1972; Christensen 1973; Benjaminsen and Christensen 1979; Mead 1989). After a gestation of about 12 months, calves are born at a length of ~3.5 m. Lactation was estimated to last 1 year with a calving interval of 2–3 years, but recent work using stable isotopes from dentine suggests that calves do not wean until 3–4 years of age (Feyrer et al. 2020). Females reach sexual maturity at a shorter mean length than males (6.9 vs. 7.5 m, respectively) but at an older mean age (11 vs. 7–11 years, respectively, based on dental layers). At physical maturity, males are approximately 1 m longer than females and live approximately ten years longer (maximum length and longevity based on dental layers: males, 9.8 m, 37 years, and females, 8.7 m, 27 years). The mean testes weight for mature males was 1.2 kg/pair with a maximum of 2.6 kg.

Northern bottlenose whales appear to be unique among beaked whales in that they apparently use their prominent maxillary crests and enlarged melons (Box 17.2, Fig. 17.1) in head-butting contests (Gowans and Rendell 1999). Southern bottlenose whales H. planifrons have only moderately developed maxillary crests; flattened melons have not been reported, and head-butting has not been documented. The high degree of synchronicity in diving and circling behavior observed during at least four instances of head-butting suggests some degree of ritualization, perhaps similar to the “parallel” walks of red deer stags Cervus elaphus (Gowans and Rendell 1999). Groups are generally small (mean 3.6, range 1–22), and there is some evidence of sexual segregation at sea (MacLeod and D’Amico 2006). Females show fission/fusion associations, while males sometimes form longer term (1–2 years) alliances—a situation more like the common bottlenose dolphin Tursiops truncatus (Brightwell and Gibson 2023, this book) than the ecologically similar sperm whale (Gowans et al. 2001). Geographical segregation of the sexes was noted by early whalers (Gray and Flower 1882); old males sometimes form groups of 4–5 animals, and females with calves sometimes form separate groups, especially in June (Ohlin 1893). The small testes (relative to body size) are consistent with a large investment in precopulatory contest competition, and it is possible that large males or male alliances prevent other males from accessing estrous females.

Fig. 17.1

Top: An adult male southern bottlenose whale in the Southern Ocean; the tooth rake marks on the body appear to be random squiggles. Photo: Stephen E. Gast. Bottom: The head and beak of an adult male northern bottlenose whale in the Gully, Nova Scotia. As is often the case, there are no visibly erupted teeth. Photo: Whitehead Lab, Dalhousie University

Box 17.2 Bottlenose Whales: Butting Heads

Compared to northern bottlenose whales, adult male southern bottlenose whales have a moderately developed melon and a single pair of teeth that erupts from the tip of the lower jaw; like most beaked whales, they are often heavily scarred with rake marks from other males. By contrast, adult male northern bottlenose whales have apical teeth which are rarely visible and their rake marks are inconspicuous. Instead, older males have a massively developed melon that sometimes bulges out over the tip of the relatively short beak; it is so imposing that it appears to restrict the male’s ability to make contact with their teeth during aggressive encounters. They have been observed to headbutt (Gowans and Rendell 1999), possibly to resolve their disputes, and this probably explains their conspicuously flattened foreheads (Fig. 17.1). The skull of the adult male northern bottlenose whales has a pair of massive boney (maxillary) crests that rise up from the rostrum; these are not found in females (or any other beaked whales) and are presumably used to buttress its weaponized melon.

17.3.2 Baird’s Beaked Whale

Largely because it has been targeted by (mostly Japanese) whalers, Baird’s beaked whale is one of the best-known ziphiids. It is distributed mostly over deep (1000–3000 m), continental slope waters around the temperate North Pacific, including the Sea of Japan, Sea of Okhotsk, and Bering Sea (Jefferson et al. 2015; Kasuya 2017). Off the Pacific coast of Japan, it occurs along continental shelf margins during the summer (May–November) and then moves to unknown wintering grounds (Kasuya and Miyashita 1997; Kasuya 2017). School size is generally large for a beaked whale, usually ranging from 3 to 20 individuals (mean 7.9, range 1–100; MacLeod and D’Amico 2006; Kasuya 2017); groups at the surface are typically tightly bunched, often seemingly in contact with each other (Fig. 17.2; Balcomb 1989).

Fig. 17.2

Baird’s beaked whale is the largest beaked whale (to 11 m); it occurs in some of the largest groups (to 100 animals), but at the surface, it forms tight groups, perhaps as a defense against killer whales Orcinus orca. Older individuals, of both sexes, are heavily raked from the teeth of conspecifics as shown in this group off Southern California. Photo: Delaney Trowbridge

Life history information for Baird’s beaked whale was recently summarized by Kasuya (2017). After a gestation of approximately 17 months, a single calf is born at a length of about 4.5 m; fully mature individuals reach 11 m with females slightly longer than males (40 cm). Compared to males, females attain sexual maturity at an older age (10–15 vs. 6–11 years), at a longer body length (9.8–11.1 vs. 9.1–10.7 m). Based on tooth layer counts, males live longer than females by ~30 years (maximum 84 and 54 years., respectively). The mean testis weight (i.e., mean of both testes) of mature males ranged from 1.4 to 8.7 kg with an asymptote of 5.3 kg at age 40 years. While histological data can detect the onset of sexual maturity, the testes continue to grow until the whale is 30–40 years old, and it is possible that only these old males participate in reproduction.

Berardius spp. are unique among extant beaked whales as both sexes have erupted teeth and extensive tooth rake marks. Adult males are often more heavily scarred than females but probably only because they live longer than females (Kasuya 2017). This suggests that within this genus, teeth are not used to establish breeding hierarchies among mature males but instead have been retained for mediating social interactions among individuals of both sexes. There is also evidence of sexual segregation at sea, including a stranding of ten mature males in Mexico (Urbán et al. 2007); schooling is probably adaptive for evading predators such as killer whales, but pregnant or lactating females may also want to avoid the attentions of aggressive males, which could lead to segregation (Weiss et al. 2021). Fedutin et al. (2015) presented evidence of a fission/fusion society but with some stable alliances among older animals, possibly males. Berardius is the least sexually dimorphic beaked whale, and testes are larger relative to body size than in most other beaked whales (MacLeod 2010; Dines et al. 2015), indicating that males are less likely to be able to monopolize access to females through contest competition, that females may mate with multiple males, and that postcopulatory sperm competition likely occurs. Kasuya (2017) noted the unusual life history characteristics of Baird’s beaked whale (lower male mortality resulting in an excess of mature males) and speculated that older males, perhaps relatives, may help in rearing young.

17.3.3 Cuvier’s Beaked Whale

Cuvier’s beaked whale has the most extensive range of any beaked whale species (Heyning 2002), being widely distributed in offshore waters of all oceans, in both hemispheres, excluding only polar waters (Heyning and Mead 2009). Populations often occur in restricted ranges (Cioffi et al. 2021); photographic identification and telemetry data have found a high degree of individual residency (Baird et al. 2008; Foley et al. 2021; Tenan et al. 2023), which can lead to genetic structuring, especially in the presence of biogeographical barriers (Onoufriou et al. 2022). One effect of genetic structuring is the morphological variation with regional differences in osteological cranial characters (Heyning 1989).

The average length at sexual maturity is 5.8 m for females (min 5.27 m) and 5.5 m for males (min 5.1 m; Heyning 1989; Santos et al. 2007). The largest reported length was 6.9 m (Heyning 1989), but there appears to be no difference in length between the sexes, and the ratio of female-to-male maximum length varies from 96% to 104% (Omura et al. 1955; Nishiwaki and Oguro 1972; MacLeod 2006; Box 17.1). The modal length (all age classes combined) reported from stranding data was 5.5–5.6 m (MacLeod 2006). Gestation period is unknown but probably around 12 months, and the mean length at birth is 2.7 m. Interbirth interval is around 3–4 years and weaning occurs when the calf is 2–3 years (Tenan et al. 2023). There are no detailed studies of longevity, though females have been estimated to live to 30 years and males 36 years based on tooth layer counts (Heyning 1989). The two longest spans for documented individuals were 24 years for a female identified as a probable adult at first identification (Hawai’i; Baird 2019) and 22 years for a female with a calf at first identification (Mediterranean Sea; Tenan et al. 2023).

Median group size ranges between 2 (Hawai’i, Canary Islands, Mediterranean Sea) and 3 individuals (Cape Hatteras; Baird 2019); the largest group recorded was 11 individuals (Moulins et al. 2007). Groups may separate while foraging at depth and then rejoin during ascent (Alcázar-Treviño et al. 2021). Mixed age/sex class groups with multiple adult males are common (Falcone et al. 2009). Preliminary data from Hawai’i suggest that females with small calves may associate with other adults (Baird 2019). In the Mediterranean Sea, females with calves are more likely to associate with one or two adult males, while juvenile individuals are more likely to associate with other juveniles (Rosso et al. 2007). Using satellite-linked depth-recording tags, Cioffi et al. (2021) found that adult male-male pairs showed extended periods (weeks) of synchrony in diving behavior while all pairs that included an adult male with an individual of another age/sex class dove synchronously for less than one day.

The few photographic identification studies of Cuvier’s beaked whales suggest a fission/fusion social structure without stable groups (Rosso et al. 2007; Falcone et al. 2009; Baird 2019), and although multi-male groups occur (McSweeney et al. 2007), heavy scarring on males (e.g., Rosso et al. (2011)) suggests that contest competition is the most likely mating strategy. However, in situations where males cannot monopolize access to females, theory predicts that selection will favor males that locate and inseminate females using both pre- and postcopulatory traits (Parker et al. 2013; Lüpold et al. 2014). Consistent with this theory, Cuvier’s beaked whale has relatively larger testes relative to their body size than other ziphiids (MacLeod 2010; Dines et al. 2015), and postcopulatory sperm competition could also occur (Cioffi et al. 2021).

17.3.4 Blainville’s Beaked Whale

The Blainville’s beaked whale M. densirostris is the most widely distributed mesoplodont, with a circumglobal distribution in tropical and warm temperate waters, preferentially over deep and slope waters (MacLeod et al. 2006; Abecassis et al. 2015; Fernandez et al. 2021). Studies near oceanic islands in the Atlantic and Pacific have identified resident populations (reviewed in Hooker et al. (2019)).

Analysis of longitudinal datasets on associated individuals of known age class, sex, kinship, residency status, and spatiotemporal patterns reveals a social structure driven by available access to females (McSweeney et al. 2007; Badenas et al. 2022). Female defense polygyny by males has been suggested for populations in Hawai’i (McSweeney et al. 2007), the Bahamas (Claridge 2006), and Canary Islands (Suárez 2018); this hypothesis was also supported, along with high residency levels among adult females, at Madeira Island (Badenas et al. 2022). Associations are stronger between adult females and immatures than between either class and males. In Madeira, adult females associated with immatures for at least 3.5 years (Badenas et al. 2022), while in Hawai’i the maximum period has been about 2.5 years. This suggests that calves disperse between two and three years of age (Baird 2019), as supported by the lactation period that may last 2–3 years (MacLeod and D’Amico 2006). Blainville’s beaked whales exhibit a general pattern of one adult male traveling with a small group of females for hours to months, and females have higher site fidelity and longer-term associations than males (Badenas et al. 2022), indicating a social structure driven by female philopatry and defense polygyny. Throughout their range, their social structure is stratified by age/sex class, with group sizes relatively small (mean 3–4 individuals, range 1–11; MacLeod and D’Amico 2006; Alves et al. 2018; Baird 2019).

Gestation period is unknown for Blainville’s beaked whales but is probably about 12 months, and females give birth to a single calf, as inferred for most beaked whales (MacLeod 2018; Baird 2019). Based on a tooth layer count, a female that had recently become sexually mature was estimated to be nine years old, so it likely takes a decade to reach sexual maturity and give birth to the first calf (Claridge 2013; MacLeod 2018). Due to the males’ large tusks, raised like horns above the top of the head, and extensive mandible reinforcement, Blainville’s beaked whales incur the heaviest tooth rake damage among beaked whales (Box 17.3, Fig. 17.3). This along with small testes (relative to body size) is further evidence of contest competition as the dominant male mating strategy. Most groups are small, with only one male present (Badenas et al. 2022), so it is likely that roving males search and fight for receptive females and spend little time with them other than to mate, although some males may mate guard long enough to increase assurance of paternity.

Fig. 17.3

Top: A battle-scarred adult male Blainville’s beaked whale with a broken right tooth in the Bahamas; beginning just behind the blowhole and running along the back are numerous longitudinal tooth rake furrows from other males. Photo: A. Friedlaender. Bottom: Adult males often show a conspicuous hump on the back, as in this animal photographed in the Canary Islands, which may be to blunt the impact of the gouging tusks. Photo: Crístel Reyes, University of La Laguna, with permit from Spanish Government

Box 17.3 Jousting Beaked Whales?

The tooth rake marks on adult male Blainville’s beaked whales tend to be concentrated on the top of the head and run down along the back (Fig. 17.3), which may only occur if two males pass by each other dorsum to dorsum (MacLeod 2002). For this maneuver to work, opponents would have to face each other, both turn 90° either left or right in the same direction, and charge at each other, similar to the jousting of knights on horseback. In addition to the deep furrows that they give each other, the occasional broken tooth (presumably from hitting the tooth of another whale) is testament to the violence inflicted. Male Blainville’s also show a hump on their back just behind the blowhole—perhaps some extra padding to absorb impact, like the chest shield on male elephant seals Mirounga spp. Other mesoplodonts (e.g., pygmy and Hubbs’ beaked whales) show tooth rake scarring more prevalent on the ventrum (Heyning 1984; Pitman and Lynn 2001), and it is possible that males of some species deliberately target the genital area.

17.4 Sexual Competition in Beaked Whales

Beaked whales appear to show marked variation in level of aggression during male-male contests (Heyning 1984; Dalebout et al. 2008), with the results of this ranging from the disfiguring furrows of Blainville’s beaked whales (Fig. 17.3), to the often barely perceptible scratches of ginkgo-toothed beaked whales M. ginkgodens (Table 17.1). In this section, we review the sexually dimorphic characters of beaked whales, including scarring patterns, and how they might relate to overall mating strategies.

17.4.1 Teeth and Beak Morphology

How forcefully males of different species can strike conspecifics depends on the relative size and location of the teeth and on the amount of buttressing teeth received from additional bone and gum tissue around them (Heyning 1984; MacLeod and Herman 2004; Table 17.1). Tooth location in beaked whales varies from the tip of the lower mandible (Cuvier’s, Shepherd’s, Longman’s, Ramari’s M. eueu, and True’s M. mirus beaked whales, bottlenose whales) to various locations caudally (Mead 1989; Jefferson et al. 2015). Apical teeth are oval in cross section, while post-apical teeth are laterally flattened along the long axis of the lower jaw (Heyning 1984). Tooth size of adult males ranges from 5 cm in True’s beaked whale to approximately 33 cm in strap-toothed beaked whale M. layardii (Box 17.4, Fig. 17.4). The two species with the largest amount of exposed tooth—Stejneger’s M. stejnegeri and strap-toothed beaked whales—show conspicuous wear on the front and inner surfaces of the teeth (Yamada 1998; Pitman et al. 2019), which may be attributed to prey abrasion during suction feeding (Ramassamy 2016). In other species with large teeth (e.g., Blainville’s, Hubbs’ M. carlhubbsi, and Andrew’s M. bowdoini beaked whales), most of the teeth is sheathed in bone or gum tissue, perhaps to prevent abrasion. At the opposite end of the exposed tooth-size spectrum, adult male northern bottlenose whales have small teeth that do not always erupt and are barely visible when they do (Moors-Murphy 2018); perhaps because males apparently butt heads to settle contests (Gowans and Rendell 1999), they may not require teeth (Fig. 17.1). The male ginkgo-toothed beaked whale has a relatively large tooth (6.5 × 11.5 cm), but only the tiniest tip is exposed above the bone and gum tissue so that tooth rake scars are almost nonexistent (Nishiwaki et al. 1972); Heyning (1984) viewed this as evidence that this species had a different social structure than other mesoplodonts.

Fig. 17.4

Top: Overhead view of the lower jaw of an adult male strap-toothed beaked whale showing how teeth would have wrapped around the rostrum and overlapped each other. Photo: collected 2004, Te Kaha near Mouriuri stream, New Zealand. CC BY 4.0. Te Papa (MM002655). Bottom: Different skull close-up of top of teeth showing the tiny denticles that do raking during tussles with other males. Photo: T. Sim, https://en.wikipedia.org/wiki/Strap-toothed_whale, accessed 11 May 2023 (Creative Commons CC-BY-SA)

Box 17.4 Strap-Toothed Beaked Whale

The strap-toothed beaked whale has some of the most bizarre teeth in the animal kingdom. Among the 16 currently known species of Mesoplodon, tooth size, shape, and placement among adult males vary according to species (Sect. 17.4.1). Teeth positioned further back on the lower jaw can be used more forcefully, but they need to be elevated above the rostrum, which can be done by raising the tooth up on a boney arch or growing a longer tooth. Male strap-toothed beaked whales grow the longest teeth of any beaked whale: a single tooth, at least 33 cm long, erupts from the middle of each lower jaw; it is flat (strap-shaped) and armed with a small, sharp denticle on the tip (Fig. 17.4). Normally among beaked whales, the bigger the tooth, the more vigorous the combat; but it appears that the only reason for this massive tooth is to provide support for the tiny cutting edge. Overlong teeth, however, are vulnerable to breaking or loss during forceful contact between males; to guard against this, the teeth grow up and back, and wrap around the upper jaw, where they can be supported by the underlying flesh and bone. The teeth can grow long enough that they overlap each other on top of the beak, and they can wrap so tightly around the upper jaw that movement is severely restricted: a mature, 5.4 m male could open its jaws only 4.0 cm at the tip (Sekiguchi et al. 1996). Although this might appear to constrain feeding ability, adult males clearly feed normally, and a reduced mouth opening may allow for more powerful and directed suction.

The amount of reinforcement that males’ teeth receive in the mandible ranges from almost none (e.g., Gervais’ M. europaeus, Hector’s M. hectori, and True’s beaked whales; Heyning 1984) to the massive boney arch in Blainville’s beaked whale, which raises each tooth above the level of the head (MacLeod 2002; Fig. 17.3). In addition to strengthening the mandible, adult males (and some females) of extant and extinct species also show various degrees of mesorostral ossification (increased swelling and density of various rostral bones that fills in the mesorostral canal) forming, in some cases, the densest bone recorded in the animal kingdom (Heyning 1984; Lambert et al. 2011); this modification may allow combative males to make forceful contact with their teeth while reducing the possibility of damaging their own rostrum (Heyning 1984). Alternative explanations for mesorostral ossification (e.g., ballast for diving, acoustic reflector for sound production) fail to account for the sexually dimorphic aspect of this trait (MacLeod 2002; Lambert et al. 2011). Gol’din (2014) suggested that beaked whales might use “echoic imaging” of the species-specific bony structures in male skulls for individual or species recognition. Acoustic studies, however, have shown that beaked whales in the North Pacific have species-specific vocalizations (Baumann-Pickering et al. 2013) such that passive acoustics would be more effective and less costly. Furthermore, the dimorphic skull structure of beaked whales could generate an “acoustic signature” that identifies individuals as adult males (Cranford et al. 2008).

Beak length in extant ziphiids ranges from extremely long and narrow Gray’s M. grayi and Sowerby’s M. bidens beaked whales to the short stout in Cuvier’s (Table 17.1). Blunt heads and wide jaws have been identified as important adaptations for suction feeding in odontocetes (Werth 2006); furthermore, it has also been suggested for a beaked whale with a long set of jaws, “suction pressures are weakest anteriorly and decline precipitously as gape increases” (Ramassamy 2016). Neither of these arguments address that beaked whales are likely obligate suction feeders and that many extant and extinct taxa have extremely long rostra (Mead 1989; Bianucci et al. 2013, 2016). It is clear that “feeding through a straw” has some yet undetermined advantage for some deep divers.

17.4.2 Color Patterning

Most beaked whales have a subtle, often ontogenetically developed, color patterning, which along with an accumulation of persistent scarring means that the sex and maturity of individual whales become more evident with age and perhaps a useful social signal. Color pattern variation among different ziphiid species comes mainly from two different sources: (1) externally acquired markings and (2) genetically controlled, species-specific pigmentation patterning. Externally acquired markings are derived from several sources, but the most important are bite wounds from cookie-cutter sharks Isistius spp. and tooth rake marks from conspecific males. Cookie-cutter sharks are small (to 50 cm), mesopelagic, and feed by taking single bites of flesh out of large animals and retreating (Pitman et al. 2019). The wounds can form white scars that are visible for many years (Baird 2016), and although relatively small (5–7 cm), they are often numerous so that older beaked whales of both sexes are usually easily distinguished. How prominent tooth rake scars are from adult male conspecifics depends on the relative size and placement of the teeth and how aggressively males of different species wield them (Heyning 1984; Table 17.1). Although females and young animals are sometimes raked, adult males are often readily distinguishable by their conspicuous scarring—forming an acquired sexually dimorphic trait. Some species have long, longitudinal scars while others have random patterns; for some species, rake marks appear to be concentrated dorsally between the blowhole and the dorsal fin and on the sides and ventral area for others (Box 17.5, Fig. 17.5). Although it has been suggested that extensive rake marks might be a signal of male quality in aggressive interactions (MacLeod 1998), it is not clear how prominent scarring would distinguish winning combatants from losers. Much remains unknown about tooth rake patterns on beaked whales and what they can reveal about the fighting tactics of different species.

Fig. 17.5

Right flank photos of the same Cuvier’s beaked whale male in the Mediterranean. The two pictures on the left were taken when the animal was still a toothless subadult, while the two pictures on the right were taken 13 years later, when the animal was a toothed adult. During the juvenile age, this male acquired intraspecific scarring along the lumbar area only; during the adult age, the scarring accumulated also along the cape and the antero-dorsal body part. Photos: Marco Ballardini and Massimiliano Rosso

Box 17.5 Scarring in Beaked Whales

In beaked whales, adult males are generally more heavily scarred by tooth raking than are adult females—up to seven times more in Cuvier’s beaked whales. Also in Cuvier’s, the prevalence of scarring on different body parts also appears to be age/sex related where adult males have more scarring along the cape; the dorsal area behind the blowhole, and lumbar flanks, while scarring on adult females, juveniles, and subadult males occurs mainly around the lumbar flanks (Coomber et al. 2016, 2022). Generally, as males mature, they acquire more scarring along the cape and the antero-dorsal part of the body (Fig. 17.5), likely caused by ritualized charging (jousting, Box 17.3) and that might indicate experience/dominance that can be evaluated by rivals before escalating the fight (MacLeod, 1998). The reason for intraspecific scarring along the ventrum is unknown but may be the result of harassment or sexual coercion.

Beaked whale calves are generally counter-shaded (darker above and paler below; Jefferson et al. 2015; Carwardine 2020), perhaps associated with being left at or near the surface during the foraging dives of their mothers (Box 17.6, Fig. 17.6). The juveniles of most beaked whales have very similar, largely nondescript, color patterns (Mead 1989). Adults of most beaked whales also have largely nondescript color patterns, which often makes field identification of this group problematic. Most species appear black, slate gray, or sometimes brownish, tan, or white, with little or no obvious patterning. In most species, the adult color pattern of both sexes is monomorphic (e.g., Berardius spp., Gervais’, True’s, Shepherd’s, strap-toothed, and Blainville’s beaked whales; Jefferson et al. 2015; Carwardine 2020). In pygmy beaked whales M. peruvianus, the adult male develops a conspicuous broad white swathe over its back that passes down and back between the blowhole and the dorsal fin (Pitman and Lynn 2001), making it the most sexually dimorphic ziphiid with respect to color patterning. Strap-toothed beaked whales are unique among extant ziphiids in having a bold black, white, and gray color pattern; Shepherd’s beaked whale also has a distinctive pattern and is unique among ziphiids in that juveniles and adults have the same color pattern (Pitman et al. 2006; Donnelly et al. 2018). In several species, adults of both sexes have a prominent white beak (e.g., Gray’s, Hector’s, Hubbs’, strap-toothed, and Andrew’s beaked whales), which may be useful for social signaling in lowlight conditions (Pitman 2018).

Fig. 17.6

An adult female (presumably the mother) and calf Blainville’s beaked whale off Madeira Island. Photo: Annalisa Sambolino, MARE-Madeira/ARDITI

Box 17.6 Do Foraging Mothers Leave Their Calves Alone at the Surface?

Beaked whales dive deep (1000–3000 m) during long periods (1–3 hours) to forage. Their infants (Fig. 17.6) have not likely yet developed such extraordinary diving capabilities. There are no records of calves alone at the surface and little evidence of alloparental care (MacLeod and D’Amico 2006; Dunn et al. 2017; pers. obs.). This is especially relevant in species of beaked whales with small groups of 2–4 individuals (Sect. 17.2) and highly coordinated foraging dives (Aguilar de Soto et al. 2020; Alcázar-Treviño et al. 2021). In deep diving and matrilineal sperm whales and pilot whales Globicephala spp., calves stay with other members of the group or alone at the surface (Gero et al. 2009; Augusto et al. 2017; pers. obs.). While their mothers forage in synchrony with other members of the group, do beaked whale calves stay at the surface? Do they remain alone, a couple of hundred meters below the surface, perhaps to avoid predators like killer whales? Do they dive in synchrony with their mothers, even as neonates (Dunn et al. 2017)?

It seems unlikely that beaked whales use color pattern for species recognition—adults spend much of their time in total darkness, either at depth or at the surface at night, situations where acoustic signaling for species recognition is probably much more reliable. Instead, we suggest that beaked whale pigmentation patterning serves primarily to distinguish adults from juveniles and in many cases males from females. Furthermore, a lack of scarring and adult color patterning on juveniles may help prevent unwanted social interactions by identifying them as either females not yet ready to breed or males not yet ready for combat.

17.4.3 Reproductive Anatomy

Testes size (relative to body size) is positively correlated with the intensity of sperm competition across a diversity of taxa and can provide insights into beaked whale mating strategies and the relative strength of pre- vs. postcopulatory sexual selection (Kenagy and Trombulak 1986; Dines et al. 2015). For example, males in species that display conspicuous weaponry (several mesoplodonts, northern bottlenose whales) exhibit smaller testes relative to their body size, which suggests that their reproductive success is largely dependent on precopulatory competition (reviewed in Dines et al. (2015)). On the other hand, one species that does not appear to engage in combat or display dimorphic weaponry—Baird’s beaked whale—has larger testes relative to body size compared to the other beaked whales; individuals may mate with multiple partners and males apparently invest more heavily in postcopulatory traits that provide advantages in sperm competition (Dines et al. 2015). Currently, we lack testes data for most beaked whale species that would allow more rigorous testing of these predictions. Interestingly, some beaked whales with less conspicuous teeth and scarring (e.g., ginkgo-toothed and True’s beaked whales) also show very small relative testes size (Dines et al. 2015).

The unique vaginal foldings of female cetaceans can also provide insights into mating strategies, as they are thought to be under sexual selection and may provide some clues into postcopulatory cryptic female choice (Orbach et al. 2017, 2023, this book). Orbach et al. (2017) examined four species of Mesoplodon (Sowerby’s, Stejneger’s, Gervais’, and pygmy beaked whales). All four had only very thin, “leaflike” cranial vaginal folding, less than observed in any other cetacean species; an observation consistent with the relatively small testes sizes observed in male mesoplodonts and low levels of sperm competition (Dines et al. 2015).

17.5 Social Segregation

In cetaceans, differences between the sexes (e.g., energetic needs, predation risk, disease risk, male harassment) result in fundamentally different pressures, often leading to spatial or social sexual segregation (Wells et al. 1987; Martin and da Silva 2004; Galezo et al. 2018; Weiss et al. 2021). The best evidence for sexual segregation among beaked whales comes from mass strandings (e.g., ten adult male Baird’s beaked whales (Urbán et al. 2007) and eight adult female Stejneger’s beaked whales (Savage et al. 2021)). From a group of six Sowerby’s beaked whales swimming nearshore, three that stranded were all males, perhaps indicating a male social group (Lien et al. 1990). Additional evidence for sexual segregation among other species comes from at-sea sightings and whaling data, including Baird’s beaked whale (Omura et al. 1955; Nishiwaki and Oguro 1972), northern bottlenose whale (Benjaminsen and Christensen 1979), pygmy beaked whale (Pitman and Lynn 2001), and strap-toothed beaked whale (Pitman et al. 2019). Although sexual segregation at sea appears to be widespread among beaked whales, its adaptive significance is unknown, but it could be that females pregnant or with calves gain an advantage by foraging without males or need to avoid harassment or coercion by adult males (e.g., Würsig and Pearson 2015; Galezo et al. 2018; Markowitz et al. 2023, this book).

17.6 Discussion

Adult males of most beaked whale species likely have few breeding opportunities: females take about a decade to reach sexual maturity, they may come into estrus only once every 3–5 years, most occur in groups of only 2–3 individuals, and in at least some species, females do not live as long as males, resulting in a surfeit of males. A receptive female is a rare resource—one to be fought over.

Interspecific differences in the prevalence and severity of tooth rake scarring on male beaked whales highlight different levels of aggression during male-male interactions. These differences are associated with different social organizations and different mating strategies (Heyning 1984; Ralls and Mesnick 2019). Species with heavily armed, aggressive males (e.g., Cuvier’s, Stejneger’s, and Blainville’s beaked whales) apparently engage in male-male combat to monopolize access to females. These species typically have only a single dominant adult male, or occasionally two (Baird 2019; Cioffi et al. 2021; Badenas et al. 2022), associated with female calf groups. In contrast, species with long beaks and smaller, more apical teeth are known to occur (at least at times) in larger, multi-male groups (Longman’s, Sowerby’s, Gray’s, and strap-toothed beaked whales; Table 17.1).

It is likely difficult or impossible for individual males to control access to females in larger, mixed groups. In these cases, selection may favor male agility and speed (and perhaps smaller body size, Box 17.1), and females may mate with more than one male, which favors larger testes and increased spermatogenesis to win paternity (Mesnick and Ralls 2018). In addition, males of some species may find advantage in numbers by forming alliances as has been suggested for northern bottlenose whale and Cuvier’s and Baird’s beaked whales (Gowans et al. 2001; Fedutin et al. 2015; Baird 2019; Table 17.1).

Beaked whales have been cited as the only sexually selected mammalian radiation outside of terrestrial ungulates (Dalebout et al. 2008). In both groups, male-male battles over reproductive access to females has apparently led to diversification of weaponry and speciation (Heyning 1984; Emlen 2008). We suggest that diversification among beaked whales may have resulted from a conflict that arose when males began using a relatively fragile beak for both feeding and fighting. Cuvier’s beaked whale is a monotypic genus with a worldwide distribution, while Mesoplodon species cumulatively occupy essentially the same geographic range but comprise at least 16 different species. Cuvier’s beaked whale has a relatively short, stout beak, allowing males to retain their apical teeth and use them with considerable force. Mesoplodon spp., on the other hand, have longer, narrower, more vulnerable beaks (Fig. 17.7), and the evolutionary trend in this genus appears to have been toward moving the teeth further back in the jaw and modifying the rostrum, so they can be used more forcefully (Moore 1968; Heyning 1984; Mead 1989). This trend has occurred at different times, to different degrees, and in different geographic locations. It appears to represent a series of localized responses to the problem of maintaining a long, narrow beak for suction feeding at depth while also using it as a weapon in combat, and it could be key to the remarkable radiation within this group.

Fig. 17.7

Dorsal view of the skull of an adult male Gray’s beaked whale from New Zealand showing the long, narrow beak at risk during interspecific combat. Photo credit: CC BY 4.0. Te Papa (MM002134)