Life without Procreation: Nonbreeders, Celibacy, and Reproductive Suppression

It is apparent that in some cases the bulls withdraw entirely from active participation in sexual competition for the herd.

—S. K. SIKES, The Natural History

of the Elephant ⁸²

Virtually every animal population includes nonbreeding individuals. There is a tendency to regard the urge to procreate among animals as instinctual, all-pervasive, and unstoppable. While heterosexual interactions often do have this quality, there are just as many examples of animals who do not reproduce: individuals who actively remove themselves from the breeding cycle, whose nonparticipation in reproduction is guaranteed by the overall social organization of the species or by physiological constraints, who produce offspring rarely (if ever), or who lead complete lives after (or without) reproducing. Many nonbreeding animals are still sexually active; on the other hand, celibacy, abstinence, and other kinds of asexuality are also prevalent in the animal kingdom. The proportion of nonbreeding individuals varies widely between different species, and between different populations of the same species. In some cases, only a few lone individuals are not actively reproductive; at the other extreme are species where more than half (American Bison, Right Whales), three-quarters (Blackbuck, Giraffe), or even 80–95 percent (New Zealand Sea Lions, Northern Elephant Seals, naked mole-rats, some dragonfly species) of one or both sexes do not reproduce.⁸³ Between these extremes, nonbreeders may constitute a quarter (Long-tailed Hermit Hummingbirds) to a third (Common Murres, Kestrels) of the population.⁸⁴

Many types of nonbreeding are found in the animal world, involving individuals of different ages, social circumstances, and varying lifetime reproductive and sexual histories. In hoofed mammals and seals, for example, males often “delay” reproducing for several years after they reach sexual maturity, frequently living in large “bachelor” herds separated from the breeding animals. Although many such animals eventually go on to reproduce, at any given time nonbreeders constitute a large segment of the population, in part because of a preponderance of younger animals in the demographics. In these species as well as others that have polygamous or promiscuous mating systems (where males typically mate with a large number of females without forming pair-bonds with any of them), there are usually also further “mating skews.” Only a portion of the male population establishes breeding territories and courts females; of those who do, moreover, only a fraction ever get to actually mate with females and sire offspring. Among Guianan Cock-of-the-Rock, for example, a fifth of the males, on average, do not have courtship territories, while almost two-thirds of the males who do are unable to mate with females. In species that have a ranked form of social organization, it is typically only the higher-ranking males that participate in the most matings. In Squirrel Monkeys and Grizzly Bears (among others) the opposite sometimes happens: the highest-ranking males may fail to obtain any heterosexual copulations at all, due to their greater aggressiveness.⁸⁵ In many animals with communal breeding systems, only one or two individuals in each group reproduce while the others are nonbreeders; many of the latter help the breeding animals raise their young, but in a few species such as Red Foxes and Gray-capped Social Weavers, some nonbreeders do not even contribute to other group members’ reproductive efforts as helpers.

A period of temporary nonbreeding can sometimes involve an entire population. In one troop of gray-cheeked mangabeys, for instance, all the females stopped cycling for a period of four months, while no reproduction took place in a population of Musk-oxen for several years.⁸⁶ In other cases, such as Hanuman Langurs, Northern Fur Seals, Mountain Zebras, Red Deer, Ruffed Grouse, Pied Kingfishers, and red-winged blackbirds,⁸⁷ some individuals live their entire lives without ever reproducing, while in some species of mole-rats as well as in Northern Elephant Seals, 90 percent or more of the population never procreates.⁸⁸ Entire flocks of Flamingos often abandon or “give up” on breeding in the middle of a season, or forgo reproducing for three to four years at a time, while individual female Silver Gulls may go as long as sixteen years without reproducing. Although most animals have yearly breeding cycles (sometimes even reproducing more than once a year), others have nonyearly or “supra-annual” cycles. King Penguins and Australian Sea Lions, for instance, have 16-to-18-month cycles, while large mammals such as Elephants, Manatees, and Whales typically reproduce only once every several years. Among White-handed Gibbons, males and females are thought to interact sexually with each other only every two years or so, while Siamang females often space their pregnancies by a couple of years, turning over parental duties to males while they assume leadership roles.

One particularly interesting form of nonbreeding involves “postreproductive” animals: individuals who have bred previously during their lifetime but are now “retired” from reproducing. Menopause and/or a period of nonbreeding in old age were long thought to be uniquely human traits. It was assumed that all animals continued to reproduce until they died, or alternatively, died shortly after they were no longer able to reproduce. In chapter 2 we saw the pitfalls of asserting human uniqueness in any area of behavior, and indeed postreproductive animals are now known to occur in several primate, hoofed mammal, seal, and whale species, and even in some birds such as Antbirds.⁸⁹ In some cases (e.g., male African Elephants), such animals are loners or peripheral to the social organization of the species. In other instances (e.g., Rhesus Macaques, short-finned pilot whales), they are integrated into the social fabric and may even assume central roles.⁹⁰ Among Killer Whales, for example, pods are often led by older, postreproductive matriarchs. Because males remain with their matriarchal group in this species, some pods eventually “die out” (even though they contain breeding-age males) because all of their females are postreproductive. Many postreproductive individuals remain sexually active until their death. Menopausal or old-aged female short-finned pilot whales, Orcas, Japanese Macaques, and Hanuman Langurs, for example, frequently engage in heterosexual (and in some cases homosexual) activity, sometimes with younger partners.

Sexual activity also occurs in other nonbreeding animals. Among birds that typically form heterosexual pair-bonds, for instance, some individuals remain single yet still court or copulate with members of the opposite sex, often during periods when fertilization is not possible (e.g., Oystercatchers, Humboldt Penguins, Hoary-headed Grebes). In many other cases, birds form heterosexual pairs or trios but do not breed—even though they still continue to be sexually active. Researchers even found that some nonbreeding pairs of Canada Geese had higher copulation rates than breeders.⁹¹ On the other hand, many nonbreeding animals are asexual or “celibate,” not courting or interacting with members of the opposite sex at all. An interesting variation of this sort involves Japanese Macaques, who sometimes form “platonic” heterosexual consortships, in which either partner may nevertheless interact sexually with other individuals besides the consort. Similar platonic “friendships” are also found between male and female Savanna Baboons. Paradoxically, the opposite situation to sexually active nonbreeding animals also occurs in a number of animals. In several bird species, pairs that are ostensibly involved in breeding actually stop copulating before the female’s fertile period has ended, while males of some marine turtles leave the waters where females are located long before the breeding season is over. Although most such animals do reproduce, it appears that in some ways they are not exploiting their reproductive potential to its fullest.⁹²

Why do animals not reproduce? Biologists have coined the term reproductive suppression to refer to various forms of nonbreeding, implying that all animals would breed if they could, but are somehow “prevented” from doing so. However, the underlying mechanisms involved in nonbreeding are far more complex than this term implies. Numerous social, physiological, environmental, and individual factors are implicated, often interacting in ways that are still poorly understood.⁹³ In some animals, procreation is indeed actively “suppressed.” In Wolves, for example, dominant pack members often physically attack lower-ranking individuals who try to mate; female Savanna Baboons sometimes form coalitions to attack cycling or pregnant females and prevent or terminate their reproductive efforts; while in many hoofed mammals, higher-ranking males prevent other males from gaining access to females. However, in other species the term suppression is a misnomer, since no coercion is involved. Young American Bison bulls, for instance, are not “prevented” from mating by older males—they simply do not participate to the same extent (as discussed in chapter 4). In other species—particularly birds with communal breeding systems such as the Pied Kingfisher, as well as primates such as tamarins and marmosets—scientists describe individuals not as “unwillingly” suppressed in their reproductive efforts, but rather as “choosing” to forgo reproduction or exercising “self-restraint” in their reproductive participation.⁹⁴ Further evidence that animals are often “voluntary” nonbreeders involves species such as Ocher-bellied Flycatchers and Ruffed Grouse, where prime breeding territories often go unused even though many nonreproducing individuals are in the population. Sometimes physiological mechanisms are involved in nonbreeding, such as lowered hormonal levels, delay of sexual maturation (sometimes indefinitely), inhibition of ovulation, and even blocking of pregnancy following conception (seen in many rodents).⁹⁵

Finally, reproduction is often a physically demanding and exceedingly dangerous undertaking that some animals may simply “avoid.” Nonbreeders are often in better physical condition than breeders, since they do not have to experience the rigors of reproducing and parenting. In fact, breeding could even be considered “suicidal” in some cases, since it may lead to a reduced life expectancy. Male Bighorn Sheep and female Red Deer that breed, for example, have significantly higher mortality rates than nonbreeders. In several species of carnivorous marsupials, most males die after mating while nonbreeders generally survive longer. The life expectancy of nonbreeding male Ruffed Grouse often exceeds that of breeding males. And female Western Gulls that breed more often during their lives have a lower survival rate than individuals that are less reproductively “prolific.” Sometimes specific biological factors serve to discourage breeding, such as the astonishing phenomenon of clitoral, as opposed to vaginal, births in the Spotted Hyena. Many females of this species die during their first pregnancy or labor because their genital anatomy requires the baby to be born through the clitoris, which ruptures and often results in many other complications for both mother and fetus.⁹⁶ Finally, the risk of acquiring sexually transmitted diseases (which are found in a surprising number of animals) may also affect reproductive activity. For example, female Razorbills (a kind of bird) avoid reproductive copulations with males when the risk for infection from STDs is greatest (although they continue to have nonprocreative sex, i.e., mounting without direct genital contact). Heterosexual behavior in a number of other species may also be curtailed by the potential danger of STDs.⁹⁷

In the end, then, there is no single “reason” why animals don’t reproduce: nonbreeding, like sexuality, is simply a part of the fabric of animals’ lives, manifesting itself in many different ways. Heterosexuality constitutes a whole range of behaviors and life histories, not a single, inalterable template that every animal must follow. And nonbreeding is one of the many ways to be “heterosexual.” Regardless of the number of nonprocreating animals in a particular population or the “causes” of their nonbreeding, one thing is certain: nonreproducing (heterosexual) animals are a ubiquitous feature of animal life.