Paternity Suits Them
by Robin Meadows
In the summer of 1992, Thomas Kunz of Boston University and his colleagues netted ten mature male Dayak fruit bats (Dyacopterus spadiceus) in Malaysia's Krau Game Reserve. Much to the biologists' surprise, these males were lactating--their mammary glands yielded small amounts of milk when palpated. While male mammals are known to be physiologically capable of producing milk under unusual circumstances such as severe inbreeding or a hormone imbalance, this was the first time lactating males have been found in the wild.
Whether male Dayak fruit bats actually suckle their young remains to been seen. However, the discovery by Kunz and his colleagues raises at least the possibility of a male mammal caring for its young single-handedly, a scenario that had previously been considered impossible. Conventional wisdom has long been that female mammals must necessarily care for their young by virtue of their mammary glands.
But about five percent of mammal species exhibit at least some paternal care. Such behavior is most common among rodents, carnivores, and primates, and the lion's share of species with paternal care are monogamous, an arrangement that may give males a greater assurance of paternity.
Mammalian males can be very dedicated parents. For example, male gray meerkats (Suricata suricatta), in addition to feeding, grooming, and guarding their young, will babysit them while females go out to hunt. Among primates, New World monkeys exhibit the most extensive male care. Male golden lion tamarins (Leontopithecus rosalia) take over most of the parental duties by the fourth week after the birth of their offspring, including grooming, carrying, and feeding the young insects and other foods. And male prairie voles (Microtus ochrogaster), small rodents closely related to the prolific lemming, diligently care for their young, covering them for warmth, grooming them, and retrieving wandering offspring that leave the nest too soon. The extensive parental care given by male prairie voles presumably helps females have litters in rapid succession, which benefits males by increasing their reproductive success.
Unlike mammals, females in other classes of animals are not physiologically bound to care for their young. Even so, females usually provide what care there is in non-mammalian species. But there are exceptions to every rule: Males are responsible for all the care in a variety of species ranging from invertebrates and fish to amphibians and birds.
Most invertebrates simply lay huge numbers of eggs and trust that some of the young will survive long enough to reproduce. But among the invertebrates that do guard their eggs and young, there are a handful of species in which the male provides all the care. For example, males always guard the eggs in at least two species of polychaetes, marine worms that use their many-bristled appendages to swim.
In one species, Neanthes arenaceodentata, which lives in bays and river mouths in many parts of the world, a female will enter a male's burrow and lay up to 1,000 eggs, losing 85 percent of her body weight in the process. The male fertilizes the eggs, then may eat what is left of his mate to sustain himself during the three or more weeks he guards them. If uneaten, the female dies within a few days anyway. Females, at least under laboratory conditions, live four or five months before laying their eggs and dying, while males live on to breed more than once.
Exclusive male care predominates in another type of marine animal, sea spiders. Found in all seas, these arthropods typically have eight legs and superficially resemble spiders. A male sea spider reaches into a female's ovary and extracts her egg mass with his third pair of legs, which have hooks and adhesive-producing glands that hold the mass. The male then cradles the fertilized eggs against his belly until they hatch, which takes as long as ten weeks in the case of one of the best-known sea spiders, Pycnogonum littorale, a beige, penny-sized species that lives in England's nearshore waters.
Other species of sea spiders are polygynous and a given male can carry egg masses from more than one female: Nymphon gracile males carry up to four egg masses at a time, and Phloxichilidium femoratum males carry as many as 14. The theory is that by carrying so many young at once, the males' investment of care yields a profitable return.
Males of some freshwater invertebrates can also carry eggs from more than one female. In the giant water bug (Abedus herberti), a brown, inch-long creature that lives in shallow streams and ponds in Mexico and the southwest U.S., the male bears the fertilized eggs on his back. A female uses mucus to affix her eggs to his folded forewings, and he tends the eggs by periodically exposing them to the air and by rocking his body up and down, which pumps a cleansing stream of water over them. By the time the nymphs emerge at three weeks, the eggs have grown so large that they have effectively tripled the male's weight.
There are also a few examples of terrestrial invertebrates in which the male is the sole caregiver. The first arachnid known to exhibit male care is a daddy longlegs (Zygopachylus albomarginis) found on Barro Colorado Island, Panama. The males construct shallow, round nests out of mud and bark on a tree trunk, and after a female lays her eggs in a male's nest she leaves him to guard them until they hatch about 20 days later. During this time, he devotedly picks fungus off the eggs and fends off would-be predators, picking up ants and throwing them out of the nest, and chasing and biting other daddy longlegs. Interestingly, the females of this species actively court males and even fight other females to win them (atypical behavior similar to that found in some fish and birds).
While exclusive male care is rare in most groups of animals, it is common in teleosts (a group containing most bony fish). More than half of the species have some form of parental care, usually egg guarding, and male care is more common than female or shared care. Male fish that guard eggs typically fertilize them externally, and the theory is that this makes the males confident that they are caring for their own young.
Male fish generally guard their young either by defending territories or nests where females lay eggs or by carrying the eggs around with them. In the four-spined stickleback (Alpetus vulgaris), a drab two- or three-inch fish that lives in brooks, males use fine plant material to weave nests that can reach five levels high. Each level houses the eggs of a different female.
One of the most remarkable methods of egg care is practiced by the splash tetra (Copella arnoldi), a three-inch, greenish-gold fish found in the Amazon River basin. This species spawns on leaves that overhang the water: A male and female leap out of the water in unison and adhere to the underside of a leaf by spreading out their fins, which allows the surface tension of the water to hold them up for several seconds. A pair typically makes about ten jumps to lay and fertilize about 100 eggs. Then the female goes on her way while the male stays behind, flicking his tail to splash the eggs about once a minute until they hatch several days later. As in many other species with exclusive male care, a male splash tetra can simultaneously care for several spawns from several females.
Other male fish care for their eggs by carrying them in their mouths or other parts of their bodies. In Betta anabantoides, two- to three-inch Indonesian fish with showy iridescent red or blue fins, the female releases her eggs into a male's curled anal fin. After he fertilizes them, she sucks the eggs into her mouth and returns them to the male, who then holds them in his mouth for protection, a behavior called "mouthbrooding." In three species of the South American catfish Loricaria, the male carries the eggs attached to his lower lip. And in the Kurtidae, a little-known group of fish that live in streams and small rivers along the coast of western Australia, males carry the eggs on a hook that projects from the back of the neck and over the top of the head.
Perhaps the most famous egg-carrying male fish are the sea horses and pipefish that carry the eggs either attached to their bellies or in brood pouches. Like the Panamanian daddy longlegs, some seahorses and pipefish have reversed sex roles. In the pipefish Nerophis ophidon, which live in meadows of eelgrass along Atlantic and Mediterranean coasts of Europe, females are larger and brighter in color, and actively court males. Sea horses take the sex-role reversal even further: The female inserts her prehensile ovipositor into a male and lays her eggs directly into his pouch, and males of some species actually have "pseudoplacentas" with blood vessels that nourish the young.
As in fish, amphibians with exclusive male care tend to fertilize their eggs externally. The five species of salamanders with male care have external fertilization, while the 12 species with female care have internal fertilization. In addition, most amphibians that care for their young are tropical species that lay their eggs on land; without care, the eggs would dry out and die.
Of
the about ten percent of amphibian species with parental care,
most guard their eggs. Some species, however, carry their
eggs or tadpoles with them. In midwife toads (Alytes obstreticans),
a gray-green, two-inch European species, males twist strings
of 50 to 100 eggs around their hindlegs. A male can carry
egg strings from more than one female at a time, and the eggs
hatch as he passes along the edges of various ponds.
Males
in two types of frogs, Sooglossus species and Assa
darlingtoni, guard the eggs, which are laid on land, until
they hatch. The male then secretes mucus that allows the tadpoles
to wriggle up his legs so he can carry his young on his back
until they metamorphose into tiny froglets. The tadpoles of
these species are endowed with enormous yolk sacs that sustain
them during the process. Male Sooglossus carry their
tadpoles on their backs, an adaptation that probably evolved
due to the lack of free-standing water in their high mountain
forest habitat in the Seychelle Islands, which lie northeast
of Madagascar in the Indian Ocean. In A. darlingtoni,
gray-to-reddish inch-long frogs that live in tropical forests
of western Australia, a male carries about ten tadpoles in
brood pouches that open on either side of his groin. These
pouches, which are part of the frog's lymphatic system, extend
along the side and belly, and bulge as the tadpoles grow into
frogs.
In contrast to invertebrates, fish, and amphibians, nearly all bird species care for their young. (Exceptions are brood parasites such as the brown-headed cowbird and European cuckoo, which lay their eggs in other species' nests so their young can be raised by the host species, and some megapodes, turkey-like birds such as the Australian mallee fowl, which lays its eggs in large mounds of decaying vegetation that produce heat and incubate the eggs without further parental involvement.) Birds are the only group in which it is most common for both parents to pitch in to care for their young. While females usually are responsible for most of the care, there are some species in which the males single-handedly incubate the eggs and care for the hatchlings.
Exclusive male care is found in ratites (kiwis, rheas, and other flightless species) and some shorebirds that nest on the ground. These birds have young that are precocial, which means that, like ducklings, they are down-covered and able to move freely immediately after hatching. Because precocial young are ready to leave the nest soon after hatching, they require far less care than the young of songbirds and other birds that have young that are altricial--naked, blind, and helpless upon hatching.
Some ratites care for more than one clutch at a time. For example, a male greater rhea (Rhea americana), an ostrich-like bird that lives in the pampas of northern Argentina, can have a harem of up to 15 females that can lay a total of 50 eggs in his nest. After incubating the eggs for about five weeks, the male leads and defends his hatchlings for another few weeks.
The shorebirds with exclusive male care include jacanas, seven-inch birds of tropical wetlands that have long green legs and exceptionally long toes, and phalaropes, sandpiper-like
birds that breed near ponds in the northern U.S. and Canada. In the northern jacana (Jacana spinosa), a species that lives from Central America to southern Texas, a female defends a territory where as many as four males build nests on floating plants. She lays up to five eggs in each nest, and the males incubate them for four weeks and then defend the hatchlings until they can fly. To distract predators, males crouch and slap their wings and feet against the ground or floating plants. Female jacanas are quite a bit larger than the males and dominate them completely.
In Wilson's phalarope (Steganopus tricolor), males incubate several eggs for about three weeks in grass-lined scrapes and then rear their brood. Phalarope females are larger and more colorful than the males, and court them aggressively, often chasing them through the air or swimming near them while puffing out their neck feathers and making a repeated "chugging" call. This nearly complete sex-role reversal (the females still lay the eggs) confused early biologists and led John James Audubon to mislabel the males and females in all his phalarope plates.
This all goes to show us that we can't second-guess parenthood in the animal kingdom. From diligent polychaete fathers to lactating male Dayak fruit bats, we are beginning to understand more about the diverse ways the sexes divide their duties, and with that understanding comes the realization that sometimes fathers prove to be the best mothers.
Robin Meadows is a contributing editor to ZooGoer.
(ZooGoer 24(3) 1995. Copyright 1995 Robin Meadows. All rights reserved.)
