Reproduction

An essential attribute of any species or population is the ability to produce a succeeding generation. As the first vertebrates to set foot on land, amphibians were faced with new reproductive challenges. The primitive reproductive behavior involves terrestrial adults moving to water. There the eggs are deposited, fertilized externally, and develop into larvae that obtain necessary nutrients from the aquatic environment; the larvae grow and change into adults with a body form adapted for life on land—a process known as metamorphosis. Early European naturalists observed this kind of reproductive behavior in local frogs, toads, and newts, and for more than a century, amphibians were characterized as having a biphasic (two-stage) life cycle (as implied by the name Amphibia).

One of the most fascinating aspects of amphibians is that their successful exploitation of a great variety of habitats necessitated the evolution of diverse reproductive modes; these modes made use of existing environmental resources in mixed climatic conditions and enhanced the survival of their young. It generally is conceded that the ancestral reproductive mode is the deposition of eggs that are fertilized externally and that development takes place in water or in a moist terrestrial or arboreal (tree) environment; this mode is known as oviparous. During their nearly 300 million years of reproductive experimentation, different groups of amphibians independently evolved terrestrial eggs, many of which undergo direct development into miniatures of the adults and bypass the free-living aquatic larval stage. Various amphibians exhibited different degrees of parental care, not only attending eggs or larvae or both but in some cases also transporting them; others evolved ways to fertilize eggs internally. In the latter case, the result is that embryos derive nutrients from the yolk for development (ovoviparous) or obtain nutrients from maternal tissues (viviparous) in a manner reminiscent of placental mammals. Both ovoviviparity and viviparity result in the birth of living young that are miniatures of the adults; again, there are no intermediate aquatic larval stages.

Within these general evolutionary trends, there are many specializations restricted to a few species (e.g., stomach-brooding and carrying larvae in pouches) and some deviations that are counter to general trends (e.g., nonfeeding larvae in terrestrial nests in humid regions). However, the overall pattern clearly is toward increased terrestriality. Thus, the existence among amphibians of manifold ways to reproduce is an example of multiple evolutionary success stories—amphibians have adopted disparate life-history strategies to cope with a variety of environmental regimes. The diversity of these strategies within the group as a whole and their flexibility within species and even within populations reflect the evolutionary and ecological diversity of amphibians, the vertebrate pioneers of the terrestrial environment.

There are costs and benefits associated with different reproductive strategies in amphibians. The presumed primitive strategy is to produce many small eggs with a small amount of yolk and deposit them in water; these eggs hatch into small larvae that obtain nutrients from the environment (exogenous larvae). Parental investment (energetic expenditure) per offspring is minimal, but survivorship is low. The large numbers of potential offspring maintain populations; this is the strategy common to ambystomatid salamanders and many families of frogs, (e.g., bufonids, hylids, and ranids). Chances of survivorship improve when larger eggs with more nutrients are produced; the embryos hatch as more advanced larvae. These larvae can survive in more strenuous environments, such as mountain streams (e.g., salamanders, such as Dicamptodon and Rhyacotriton, and anurans, such as Atelopus, Ptychohyla, and Scutiger), or require less time to complete metamorphosis (e.g., some species of marsupial frogs). This strategy requires greater investment per offspring by the female. The next step is production of fewer eggs with sufficient nutrients for the completion of development as nonfeeding larvae or as miniatures of the adults. Maternal investment per offspring and survivorship are high. Survivorship is enhanced by many kinds of parental care, but in many of these species fecundity is low.

Direct development not only has evolved independently in different lineages of anurans, but it also has taken place in distinct ways. In most direct-developing anurans, the early larval stages are absent; thyroid hormones that are essential to triggering metamorphosis in tadpoles also influence later developmental stages in frogs, such as Eleutherodactylus coqui, and bring about the metamorphic climax shortly before hatching. In contrast, in hemiphractine hylids, the usual larval stages are present within the egg capsules of those species with direct development. Possibly, the production of tadpoles in some species of marsupial frogs (Gastrotheca) is an example of

arrested development or simply suggests that there are insufficient amounts of nutrients in the eggs to complete development.

Courtship and mating

With the possible exception of some poison frogs of the genus Dendrobates, in which pairs apparently are bonded throughout a breeding season, amphibians are polygamous. Most salamanders reach sexual maturity during their second year, with females usually maturing later than males. Females of the aquatic cryptobranchids and proteiids do not breed before six years; in contrast, both sexes of the aquatic plethodontid Eurycea multiplicata reach sexual maturity shortly after metamorphosis at an age of five to eight months. Most anurans reach sexual maturity in six months to one year, but species inhabiting cool climates require much longer, up to four years in Ascaphus and many Rana. The limited data on caecilians suggest that sexual maturity is reached in two to three years.

Reproductive cycles are controlled by hormones, the actions of which are correlated with environmental variables as well as constraints of habitat, size, reproductive mode, and parental care. Caecilians reproduce biennially, and salamanders reproduce annually or biennially. In the wet tropics, anurans commonly reproduce continually and may deposit several clutches of eggs per year, but in seasonally dry or cold regions, the number of clutches may be limited to one per year or one every other year. In temperate regions, breeding coincides with higher temperatures and spring rains, whereas in semiarid regions and deserts, breeding activity is initiated by rains that result in the formation of temporary ponds. Thus,

breeding activities may be limited to only a few days or weeks in any given year.

In many amphibians, especially those laying terrestrial eggs, courtship and mating take place within their normal home ranges, but most of those species that deposit their eggs in water migrate to breeding sites, and large numbers of individuals often congregate at these sites. Several species of anurans and salamanders are known to return to the same breeding sites in successive years; in some cases, this is the site where they developed as larvae. Olfaction seems to be the primary method used by salamanders and some frogs to locate breeding sites, but vocalization plays the dominant role among most frogs. Calling by aggregations of anurans attracts not only females but also other males to the breeding site. Little is known about courtship in the secretive, subterranean caecilians; it is thought that olfaction is important for the location of mates in burrows.

Release of hormones (principally gonadotropin) during early phases of the reproductive cycle results in the development of many secondary sexual characters that can persist throughout adult life or might be transitory during the reproductive season. Among the former features are body size and skin texture. Females usually are larger than males. Males of some salamanders, especially newts (Salamandridae), develop

more intense coloration, and in many kinds of male frogs, vocal sacs become more brightly colored during the breeding season. Courtship glands develop on the chins of males of many kinds of salamanders, especially plethodontids, and on the chins and bellies of various kinds of frogs. The most conspicuous secondary sexual characteristics are horny growths known as nuptial pads or excrescences in males. Males use these growths to better grip the female during breeding. Most male anurans clasp females from above (amplexus); the clasp is around the waist (inguinal amplexus) in some frogs, but more often it is just behind the arms (axillary amplexus). Nuptial excrescences are present at the base of the thumb and sometimes on the fingers and the chest; typically, the excrescence is a roughened pad, but in some species it takes the form of one to many spines. Nuptial excrescences also develop on the insides of the arms or legs of some salamanders that breed in water.

Fecundity and egg deposition

Generally, larger species deposit more eggs than smaller species, and eggs placed in water are smaller and more numerous than those laid on land or carried by a parent. For example, the oviparous caecilian Ichthyophis glutinosus may lay as many as 54 eggs in a clutch, but the viviparous Geotrypetes seraphini gives birth to only one to four young. Fecundity is higher in salamanders; again, clutches deposited in water are the largest. The tiger salamander (Ambystoma tigrinum) can lay as many as 500 eggs, and the hellbender (Cryptobranchus alleganiensis) and the greater siren (Siren lacertina) deposit clutches of about 450 and 500 eggs, respectively. In contrast, clutches of the Olympic torrent salamander (Rhyacotriton olympicus) contain as few as eight relatively large eggs laid in mountain streams. Many plethodontid salamanders lay their eggs on land; clutches may contain as few as nine and as many as 40 eggs. The live-bearing salamander (Salamandra atra) gives birth to only two young at a time.

Fecundity in anurans varies much more widely than in other groups of living amphibians. Many species, especially large species of Bufo and Rana, that deposit eggs in water have extremely large clutches containing thousands of eggs. Many small and medium-size species in the humid tropics lay clutches of only a few hundred eggs, but females return to

breeding ponds in a matter of a week or two to deposit another clutch. Species (e.g., phyllomedusine hylids and hyperoliids of the genera Afrixalus and Hyperolius) that deposit their eggs on vegetation above water have smaller clutches, commonly fewer than 400 eggs, and the small glass frogs (Centrolenidae) usually deposit fewer than 40 eggs. Many kinds of frogs deposit clutches of six to 67 eggs on land; in some cases the eggs are deposited in chambers excavated by the parents. A few kinds of frogs give birth to no more than eight living young at a time.

Anurans deposit eggs in places other than in water or on land. Several kinds of hylids and microhylids lay their eggs in water-holding leaf axils, tree holes, or bromeliads; such clutches usually contain fewer than 60 eggs. Amplectant pairs of some leptodactylids and limnodynastids kick the eggs with their feet into a mixture of water, air, and secretions that form a foamlike mass floating on the water; the outer part of the foam nest hardens and protects the moist interior in which the eggs develop. Rhacophorid frogs also build foam nests on leaves or branches over water, and some leptodactylids (Adenomera) deposit eggs in terrestrial foam nests, where the eggs and embryos obtain all their nutrients for development from the yolk. Fecundity decreases from as many as 1,000 eggs in aquatic foam nests to as few as 25 in terrestrial foam nests.

Fertilization

The eggs, which consist of an ovum within one or more gelatinous capsules, are fertilized externally in nearly all anurans and in salamanders of the families Cryptobranchidae, Hynobiidae, and, presumably, Sirenidae. Eggs are deposited in water (on land in the case of many anurans), and males exude sperm over them. However, in all caecilians and in most salamanders, success is enhanced by internal fertilization. In caecilians, males have a penis-like intromittent organ, the phallodeum, which is inserted into the female's cloaca. This unique structure in amphibians is a portion of the cloaca that is eversible (able to turn inside out). An analogous, but not

homologous, "tail" (a posterior extension of the cloaca) in frogs of the genus Ascaphus (Ascaphidae), which breed in fast-flowing streams, conducts sperm from the male into the female's cloaca. Internal fertilization in salamanders is accomplished by another unique feature, the spermatophore, which is a conical, gelatinous structure with a cap of sperm. During courtship, males deposit spermatophores on the substrate; females pick up spermatophores in their cloacas, and the sperm are stored in a small pouch, the spermatheca, off the cloaca. Subsequently, often many months later, the eggs are fertilized as they pass through the cloaca. Aside from Ascaphus, internal fertilization is known in a few other anurans, namely, African toads (Nectophrynoides) and some West Indian species of the leptodactylid genus Eleutherodactylus. Internal fertilization also is suspected in the African bufonid Mertensophryne micranotis and an East Indian ranid of the genus Limnonectes, because of modifications of the cloacal regions of males.

Development and hatching

Most aquatic eggs hatch as small larvae, whereas many terrestrial eggs undergo direct development and hatch as miniatures of the adults. In direct-developing eggs, the larval stages are completed within the egg capsules, or the larval stage is suppressed. There is a positive correlation between ovum size and stage of hatching. The ova of salamanders that have aquatic larvae usually are 0.06–0.12 in (1.5–3.0 mm) in diameter, and anuran ova deposited in water are even smaller, 0.04–0.08 in (1.0–2.0 mm) in diameter. Such eggs contain small amounts of yolk that provide sufficient nutrients for only partial development. The larvae obtain nutrients from the environment for the rest of their development.

In those salamanders and frogs that undergo direct development, the ova contain all the nutrients necessary for growth into a small salamander or frog. Consequently, the ova are much larger—0.12–0.5 in (3.0–5.0 mm) in salamanders and 0.08–0.40 in (2.0–10.0 mm) in anurans—than eggs that hatch as tadpoles. A negative correlation exists between temperature and developmental rate. Aquatic eggs of salamanders develop in relatively cold water, and the duration of development ranges from 20 days in some newts (Triturus) to about nine months for the eggs of Dicamptodon in cold mountain streams. Likewise, most salamanders laying terrestrial eggs live in cool or temperate conditions; their eggs require 56–165 days to complete their growth to miniatures of the adults. The small aquatic eggs of many anurans hatch within one day of deposition, but those laid in cold water may require more than

40 days to hatch. Direct-developing eggs of anurans need longer, usually about a month, but those of the small leptodactylid Eleutherodactylus planirostris complete their development in as few as 15 days. In a few salamanders (e.g., the plethodontid Desmognathus aeneus) and several frogs (e.g., the myobatrachid Crinia nimbus, limnodynastids of the genera Kyarranus and Philoria, leptodactylids of the genus Adenomera, bufonids of the genus Pelophryne, and some dendrobatids of the genus Colostethus), terrestrial eggs hatch as nonfeeding larvae that obtain the nutrients necessary to complete growth from yolk encased in their body cavities.

Parental care

Parental care in the form of protection and feeding typifies birds and mammals; although they are less universal, diverse kinds of parental care exist among amphibians as well. Parental care can be defined as any behavior exhibited by a parent toward its offspring that increases the offspring's chances of survival; this behavior, however, can reduce the parent's ability to invest in additional offspring. Among amphibians, parental care includes attendance of eggs, transportation of eggs or larvae, and feeding of larvae. Parental care occurs only in those species that deposit their eggs in single clusters, never among species that scatter their eggs in aquatic situations. Nest construction and retention of eggs in the oviducts are not considered to be parental care.

Egg attendance

Egg attendance is the most common and taxonomically widespread type of parental care. In most cases, the eggs simply are guarded against potential predators, but some species of salamanders have been observed to rotate and possibly aid in aeration of aquatic eggs by creating water currents with their gills or tails. Guarding seems to be the principal function of terrestrial salamanders that coil about their clutches, but by osmotic transfer of moisture they also may help prevent desiccation of the eggs; some species also have been seen to rotate the eggs, which aids in the elimination of pathogenic fungi. A few anurans attend clutches of aquatic eggs, but many attend terrestrial or arboreal clutches.

Stream-inhabiting salamanders of five families are known to attend egg clutches attached to objects in streams; attendance is by males in Andrias, Cryptobranchus (Cryptobranchidae), and several species of Hynobius (Hynobiidae) but by females in two species of Dicamptodon (Dicamptodontidae), several species of plethodontids (Desmognathus, Eurycea, Gyrinophilus, and Pseudotriton), and Necturus maculosus (Proteiidae). Attendance is by either parent in the subterranean proteiid Proteus anguinus. Generally, the adults remain with the eggs from the time of deposition until hatching; the duration of this attendance varies from about six weeks in Necturus maculosus to about 13 weeks in Desmognathus marmoratus.

Attendance by females at terrestrial nests is known among many salamanders—the ambystomatid Ambystoma opacum and several genera of plethodontids (e.g., Batrachoseps, Bolitoglossa, Ensatina, Desmognathus, Hemidactylium, and Plethodon). Because egg deposition may occur many months after insemination by spermatophores, males of these salamanders may no longer be in the vicinity and do not attend nests. The duration of female attendance varies from about six weeks in Ambystoma opacum to nearly six months in Bolitoglossa rostrata. Females of some caecilians (Ichthyophis and Idiocranium) and one salamander (Amphiuma) are known to coil around subterranean clutches of eggs, presumably to minimize desiccation, or loss of moisture.

With the exception of males of the hairy frogs (Arthroleptidae: Trichobatrachus robustus), which sit on eggs in streams, and males of the moustache toads (Megophryidae: Vibrissaphora), which guard eggs under boulders at the edges of streams, attendance of aquatic eggs among anurans is known only in species that lay eggs in foam nests (Limnodynastidae: Adelotus) or in basins constructed by males (Bufonidae: Nectophryne; Hylidae: Hyla rosenbergi). In these cases, the eggs are in territories defended by males, who secondarily guard eggs. Eggs are not attended very long in these species—two to three days in Hyla rosenbergi, six days in Adelotus brevis, and 35 days in Nectophryne afra. Females of some species of Leptodactylus guard aquatic foam nests and subsequently remain with the schools of tadpoles, defending them from potential predators.

Male attendance of egg clutches on vegetation over water is common among territorial centrolenids, but it is unknown in the arboreal-nesting phyllomedusine hylids. Centrolenids not only guard the eggs from potential parasitic insects but also keep the eggs moist by perching on top of them by day. Species in three genera of microhylids (Anodonthyla, Platypelis, and Plethodontohyla) in Madagascar deposit their eggs in water-filled leaf axils; males attend the eggs for 26–35 days, until hatching. Females of the African ranid Phrynodon attend arboreal eggs, as do females of at least two hyperoliids (Alexteroon obstetricans and Hyperolius spinigularis), who not only guard their arboreal egg clutches but also moisten them by eliminating water from their bladders on the eggs.

Attendance of eggs is common among species that deposit their eggs on the ground and in burrows. The eggs of African Hemisus (Hemisotidae) and Breviceps (Microhylidae) are deposited in subterranean burrows and attended by females, who presumably moisten the eggs. Females of the former genus burrow headfirst from the chamber to a nearby pond, thereby releasing tadpoles into the water.

Several species of frogs in different families and one salamander, the plethodontid Desmognathus aeneus, have terrestrial eggs that hatch as nonfeeding larvae and derive all their nutrients from the yolk encased in their bodies. Attendance is by females in the salamander and in the leptodactylid frog

Zachaenus parvulus, but the eggs are attended by males in the leptodactylid Thoropa petropolitana, the bufonid Nectophrynoides malcolmi, three species of the ranid genus Petropedetes, and at least two microhylids (Breviceps adspersus and Synapturanus salseri).

Clutches of terrestrial eggs undergo direct development into froglets in many different lineages of anurans. This mode of development is characteristic of all arthroleptines and brachycephalids, three species of Leiopelma, two genera of myobatrachids (Arenophryne and Myobatrachus), a few bufonids and ranids, and leptodactylids of the genus Eleutherodactylus (and relatives). The mode also characterizes about 50% of the Microhylidae (all asterophryines, brevicipines, and genyophrynines and at least one microhyline, Myersiella microps). In some cases females attend the clutches, but in others attendance is by males, especially territorial species, such as some Eleutherodactylus. The known duration of attendance is 17–100 days.

Transportation of eggs and larvae

Adults of diverse species of anurans that attend developing clutches of eggs subsequently transport eggs, larvae, or

both. The European midwife toads of the genus Alytes exhibit the simplest form of this type of parental care. As the strings of eggs are deposited and fertilized in shallow water, they adhere to the hind limbs of the male; he carries them with him and enters water when the eggs are ready to hatch, at which time the egg membranes disintegrate, and the tadpoles swim away.

Most instances of larval transport are associated with terrestrial eggs. In all dendrobatids except Aromobates, an adult sits in the disintegrating gelatinous material, and the hatchling tadpoles wriggle up the legs and onto the back of the adult. The larvae do not hold on to the adult with their mouths; instead, their bellies adhere to the skin on the dorsum of the parent by means of a gluelike substance (mucopolysaccharide) that dissolves in water once the parent transports them to a stream, small pond, or water-holding plant. In some Dendrobates, adults transport tadpoles from terrestrial nests to arboreal bromeliads that may be as high as 100 ft (30 m) above the ground. Similar transportation of larvae from terrestrial nests to aquatic sites for tadpole development is known in two genera (Aphantophryne and Liophryne) of genyophrynine microhylids and in some species of the ranid genus Limnonectes. Terrestrial eggs of the sooglossid Sooglossus sechellensis hatch as nonfeeding larvae that wriggle onto the back of the attending female, where they complete their growth. Transportation of hatchling froglets occurs in three of the four species of Leiopelma in New Zealand; the hatchlings climb on the back of attendant males.

Males of the small myobatrachid frog in Australia (Assa darlingtoni) have an inguinal pocket on each side of the body. The male sits in a clutch of 10 or 11 terrestrial eggs; upon hatching, the nonfeeding tadpoles wriggle onto the male and into the inguinal pockets, where they complete their development and emerge as froglets about two months later. Males of the southern South American mouth-brooding frogs of the family Rhinodermatidae attend terrestrial clutches of eggs. Male Rhinoderma rufum transport the tadpoles in the mouth to water, where they complete their development. Male Rhinoderma darwinii pick up hatchling tadpoles in the mouth; the tadpoles enter the vocal sac via the vocal slits in the floor of the mouth. The male carries the tadpoles in his vocal sac for 50–70 days, at which time fully developed young crawl through the vocal slits and emerge from the mouth. Some evidence suggests that nutrients are provided by the epithelial lining of the vocal sac.

Two groups of anurans exhibit highly specialized modes of transport of eggs and developing embryos under entirely different environmental conditions. During inguinal amplexus in aquatic frogs of the genus Pipa (Pipidae), females exude eggs into the water, and males sweep them with the feet onto the backs of the females, where the eggs become imbedded in the females' skin. In all species the eggs hatch as tadpoles. In some species (e.g., Pipa carvalhoi and P. myersi), the tadpoles leave the chambers and complete development as free-swimming tadpoles. In other species (e.g., Pipa aspera and P. pipa), the tadpoles complete their growth within the chambers and emerge as froglets. Females of the terrestrial and arboreal hemiphractine hylid frogs transport eggs or

tadpoles on the dorsum (back) or in a dorsal pouch; the eggs are enclosed at least partially in bell-shaped external gills. The eggs adhere to the dorsum in Cryptobatrachus, Stefania, and Hemiphractus and hatch as froglets.

In Flectonotus, the eggs reside in a basinlike structure (which may be open or closed by lateral folds of skin) on the female's back; the eggs develop into nonfeeding tadpoles that are deposited in water in bromeliads or tree holes, where they complete their development in a few days. During amplexus, male marsupial frogs of the genus Gastrotheca push eggs into the opening of a pouch on the back of the female. In most species (e.g., Gastrotheca ceratophrys, G. guentheri, and G. plumbea), the large eggs develop directly into froglets that emerge from the pouch. In several species inhabiting high elevations of the Andes, the eggs hatch as tadpoles, at which time the females sit in shallow ponds and spread out the pouch opening with their toes to allow the tadpoles to escape into the water, where they feed and complete their growth.

Perhaps the most unusual mode of transport was in two species of Australian gastric-brooding frogs (Myobatrachidae: Rheobatrachus) that lived in mountain streams in northeastern Australia and are now presumed to be extinct. The female swallowed the fertilized eggs; the eggs or embryos secreted a hormone, prostaglandin E₂, that inhibited the usual production of digestive enzymes and acids by the epithelial tissue of the stomach. Thus, for a period of six to seven weeks, the female did not feed, because her digestive system had been shut down and her stomach converted to a gestation chamber. The tadpoles obtained all nutrients for development from the large amount of yolk contained in the eggs. Young were expelled from the mouth by the mother's propulsive vomiting. Within a few days after giving birth, the female's stomach resumed its digestive function, and the female began to feed.

Feeding of tadpoles

Females of frogs in four families are known to provide eggs as nutrients for developing tadpoles; all examples of this kind

of maternal behavior occur in cases in which the tadpoles are in confined or constrained situations, such as water in bromeliads or tree holes or in foam nests. After deposition of eggs or transportation of tadpoles, the female returns to the site and deposits eggs on which the tadpoles feed. Insofar as is known, tadpoles of some species are obligatorily oophagous (egg eating), whereas those of other species also feed on detritus or insect larvae, which may be present in the water in bromeliads or tree holes.

The simplest expression of this type of parental behavior is seen in a species of Leptodactylus (L. fallax) in the Lesser Antilles and several species of hylid frogs in Jamaica and Central and South America. The eggs of L. fallax are deposited as a foam nest in a shallow basin; the hatchlings remain in a disintegrating foam nest and produce secretions that mix with moisture to create additional foam in which they develop. The female periodically inserts her cloaca into the foam and exudes eggs, on which the tadpoles feed.

Likewise, females of several hylids that deposit eggs in bromeliads or tree holes provide eggs for their larvae; these species include Anotheca spinosa, Hyla picadoi, and H. zeteki in Central America; Osteocephalus oophagus and some species of Phyllodytes in South America; and Osteopilus brunneus in Jamaica. Because presumably conspecific (i.e. of the same species) frog eggs have been found in the stomachs of some other tadpoles, the females of those species are thought to provide eggs as nutrients for their tadpoles. These species include the microhylid Hoplophryne rogersi in Africa, a species of Philautus (Rhacophoridae) in Asia, Phrynohyas resinifictrix in South America, and Calyptahyla crucialis, Hyla marianae, and H. wilderi in Jamaica. With additional studies in the field, we should expect to find many more examples of this kind of parental care.

In some species of Dendrobates, females transport tadpoles individually from the terrestrial nest to an aquatic microhabitat (bromeliad, tree hole, or the husk of a Brazil nut). Subsequently, the female returns to each of the sites of tadpole development and deposits unfertilized eggs for the tadpoles to eat. In some other species of Dendrobates (e.g., D. vanzolinii), however, the male transports the tadpoles and subsequently leads the female to each deposition site so that she can feed the tadpoles.

Live birth

Ovoviviparity (in which all nutrients during development are provided by yolk) occurs facultatively (i.e. in some conditions but not others) in two salamanders (Mertensiella caucasica and Salamandra salamandra) and two frogs (Nectophrynoides tornieri and N. viviparus). True viviparity (maternal provision of nutrients during development in the oviducts) is known in several caecilians of three different families and in two salamanders (some populations of Mertensiella luschani and Salamandra atra) and one anuran (Nectophrynoides occidentalis). During their development, fetuses of the caecilians quickly exhaust their yolk supply, escape from the embryonic membranes, and obtain nourishment from the female by ingesting secretions and epithelial tissue from the lining of the oviducts; fetal caecilians have deciduous teeth that are specialized for scraping the lining of the oviduct. Maternal nutrients also are supplied from the walls of the oviduct in Salamandra atra and by epithelial secretions in the oviducts of Nectophrynoides occidentalis.

Resources

Books

Crump, Martha L. "Parental Care." In Amphibian Biology, Vol. 2, Social Behaviour, edited by Harold Heatwole. Chipping Norton, Australia: Surrey Beatty and Sons, 1995.

Duellman, William E., and Linda Trueb. Biology of Amphibians. Baltimore: Johns Hopkins University Press, 1994.

Taylor, Douglas H., and Sheldon I. Guttman, eds. The Reproductive Biology of Amphibians. New York: Plenum Press, 1977.

Tyler, Michael J., ed. The Gastric Brooding Frog. London: Biddles, 1983.

Periodicals

Callery, Elizabeth M., Hung Fang, and Richard P. Elinson. "Frogs Without Polliwogs: Evolution of Anuran Direct Development." BioEssays 23 (2001) 233–241.

Crump, Martha L. "Reproductive Strategies in a Tropical Anuran Community." Miscellaneous Publications, Museum of Natural History, University of Kansas 61 (1974) 1–68.

Duellman, William E. "Reproductive Strategies of Frogs." Scientific American 267 (1992) 80–87.

Elinson, Richard P. "Direct Development: An Alternative Way to Make a Frog." Genesis 29 (2001) 91–95.

Wassersug, Richard J., and William E. Duellman. "Oral Structures and Their Development in Egg-Brooding Hylid Frog Embryos and Larvae: Evolutionary and Ecological Implications." Journal of Morphology 182 (1984) 1–37.

William E. Duellman, PhD

Reproduction

The widely accepted belief that genocide only entails killing members of a racial, religious, national, or ethnic group misconstrues the multiple ways that genocide is perpetuated. Article II of the 1948 United Nations (UN) Convention on the Prevention and Punishment of the Crime of Genocide (hereafter referred to as the Genocide Convention) underscores the reality that genocide can be accomplished by other acts, independent of or along with killings. The infliction of serious physical or mental harm to members of a group, or the transfer of children from one group to another, suffices, under certain conditions, as an act of genocide. Likewise, Article II(d) of the Genocide Convention seeks to prevent, suppress, and punish those who would "impose measures intended to prevent birth within the group." This provision verifies that by impeding a group's ability to reproduce and thus denying the physical existence of its members, even prior to their birth, a group can be destroyed in whole or part.

German Laws on Racial Purity

In the mid-1930s Germany enacted a series of laws, ostensibly to ensure the physical health of its citizens, but in reality, to oversee the purity of "the German race." The idea that the political state should be composed of a single race or unique people intertwined several political and pseudo-scientific theories. The Enlightenment philosophy of the 1700s exalted the natural rights of man. Eighteenth-century European revolts against the monarchy and American revolts against colonialism were heavily influenced by Enlightenment philosophers who advocated the restructuring of political states according to the true nature of the democratic individual.

In the mid-nineteenth century ethnologists, influenced by Charles Darwin's theories on the biological origin of the species, tried to determine the historical origins of the races. In the 1850s Arthur de Gobineau, horrified by the decline of French society, proposed a racial theory to explain the evolution of human societies. In his Essay on the Inequality of the Human Race, Gobineau maintained the existence of three unequal races: white, yellow, and black. The white race was superior to the others, while the black race was inferior to the white and yellow races. Each race also possessed inherent intellectual abilities. A race's physiological traits, such as prominent noses among the white race, supposedly revealed immutable values. Gobineau concluded that the major threat to human society and the harbinger of a civilization's degeneration was mixed-race procreation.

In the late nineteenth century Houston Stewart Chamberlain, an Englishman residing in Germany, disseminated the "scientific" idea that among the white races, only the Teutons stood at the pinnacle of racial evolution. Chamberlain touted the Teutons, also called Aryans, as an ancient, noble, pure-blooded race. He believed that Teutons had, over the centuries, developed a "race-soul" that biologically rendered them morally, spiritually, and creatively superior. Chamberlain's findings nourished a genre of romantic-political myth about the Aryan race and prompted some Germans to believe that they were pure descendants of the Teutons. Inspired by Chamberlain's race-based premises, ethnologists eagerly unearthed certain linguistic and semiotic proof of the longevity and original purity of the Aryan race.

By the 1930s, when the Nazi Party assumed power in Germany, eugenics, the science of selective biological breeding, became a political goal under the guise of health regulations, euphemistically termed racial hygiene. Consequently, the state regulated reproductive capacity with the aim of preserving national purity by suppressing racial impurity. Initially, German racial hygiene laws affected persons who were racially recognized as German, but who comprised part of the less desirable segments of German society.

In July 1933 the Law for the Prevention of Genetically Diseased Offspring provided for the sterilization of an individual if he or she suffered from genetically determined illnesses, including feeblemindedness, schizophrenia, manic depression, epilepsy, Huntington's chorea, genetic blindness or deafness, and severe alcoholism. Commonly known as the Sterilization Law, it signalled a direct reversal of German policy that, until the 1930s, had strictly forbidden sterilization procedures. Germany justified its reversal, in part, by citing the example of other civilized countries such as Denmark, Norway, Czechoslovakia, Hungary, and the United States that permitted sterilization of the criminally insane or feebleminded.

In the first year after the Sterilizations Law was promulgated, genetic health courts, staffed by physicians, secretly administered and authorized over 56,000 sterilization procedures. In November 1933 the German state passed the Law Against Dangerous Career Criminals that required the castration of sex offenders. On July 26, 1935, a supplemental ordinance, authorizing forced abortions for women who were genetically unfit but who had already conceived and thus fell outside of the scope of the original sterilization edict, became law.

By the mid-1930s Germany asserted that only a subsection of Germans could be recognized as racially pure or Aryan. As a result in 1937, the genetic health courts, together with the Gestapo and state police, began to enforce the restrictive birth policy against mix-raced individuals. Under the Rheinlandbastarde policy, they secretly authorized the sterilization of some five hundred persons of mixed German and African ancestry. Reference to non-Aryans increasingly meant all Jews, even those who were German citizens. In 1938 a law provided for Jewish women to abort their pregnancies solely based on their new racial status.

By 1939 these sterilization policies ensured that over 400,000 Germans, either mixed-raced, Jewish, non-Aryan, or mentally or physically infirm underwent forced sterilization. The sterilization procedures included tubal ligation, vasectomy, x-ray exposure, or hysterectomy. The policies were a precursor to the Nazi euthanasia laws, which became law at the start of World War II. The euthanasia laws decreed that the outright killing of potential parents of undesirable offspring was preferable to regulating their ability to reproduce. Euthanasia was regarded as the ultimate means of ensuring racial and national purity.

The Nazi sterilization policies complemented another set of reproductive edicts that were collectively referred to as the Nuremberg Laws. In September 1935 the Reich Citizenship Law mandated that only full-blooded Germans were entitled to citizenship, whereas Jews would only be considered residents of Germany. Also in September of that same year the Law for the Protection of German Blood and German Honor proscribed marriages and sexual relations between Jews and non-Jews illegal. In October 1935 the Law for the Protection of the Genetic Health of the German People required couples to submit to premarital medical examinations to check for any of the illnesses sanctioned in the 1933 Sterilization Law; when deemed necessary, these marriages were prevented.

Whereas the sterilization policies mandated surgical interventions to stop reproduction, the Nuremberg Laws racially "declassified" individuals in declaring that they were not of German blood. They outlawed sexual contact between racially superior Germans and those termed racially denigrated. It is thus easy to understand why these measures, namely sterilization or compulsory abortions, segregation of the sexes, or obstacles to marriage, concerned the drafters of Article II(d) of the Genocide Convention.

A third set of reproductive policies introduced in the mid-1930s compelled German women considered to be racially Aryan to procreate, by offering pro-birth incentives. The German state awarded mothers of four or more children bronze, silver, or gold medals. It also provided loans of up to one year's salary to persuade women to leave the workforce and return home. Aryan women were encouraged to bear children out of wedlock. Infertility became recognized as grounds for divorce. A system of disincentives discouraged Aryan types from remaining childless. A penalty tax was levied on Aryans who had married and not procreated within five years. Stiff fines and prison sentences were meted out to physicians or others who performed abortions on Aryan women.

These birth incentive policies purported to rectify "the disproportionate breeding of inferiors, decrease the rampant celibacy of the German upper classes and control the threat posed by working women, liberated from the household" that the state viewed as detrimental "to the reproductive performance of the family." Although Article II(d) of the Genocide Convention refers to measures that prevent births, these countermeasures, to stimulate births among the Aryan population, unambiguously illustrate the fact that the Nazi sterilization policies and Nuremberg Laws did function as measures imposed to regulate all births.

This complex system of reproduction policies, based on the state's concepts of race and nation, must be grasped to understand the potential scope of Article II(d). Incongruously, when Japan, India, and Iraq be came German allies in arms during World War II, the non-Aryan racial and political treatise was not directed against them.

Eric Weitz, in A Century of Genocide Utopias of Race and Nation, observed that "slippage from the nation as a political community to the nation as a racial community became more prevalent when culture, not political rights was made the defining element in the formation of a nation" (2003). In the early twenty-first century ethnic, national, or religious identity might fall prey to subjectivity, as did racial groupings under the Nazi government. One need only reflect on white Australian immigration policies between the 1940s and 1970s, the former apartheid regime of South Africa, or the expulsion of Asian-descended Ugandans from their homes in the 1970s to comprehend the twentieth-century's malleable concepts of race and nation.

Article II(d) and World War II Cases

The potential breadth of Article II(d)'s prohibition is also rooted in the egregious forced labor programs and concentration camp experiments of World War II. Germany invaded Eastern Europe in 1939 and established forced labor programs, using Polish and Russian workers of both sexes. The Allied military trials of minor Nazi officials made clear that the Third Reich built into its forced labor policies measures intended to prevent birth among non-Aryan workers. In the United States v. Greifelt et al., the defendants were leading officials in the SS Main Race and Settlement Office and the Repatriation Office for Ethnic Germans. The SS Main Race and Settlement Office devised the following measures for foreign workers:

Comprehensive sterilization of such men and women of alien blood in German agriculture who, on the basis of our race laws—to be applied even more strictly in these cases—have been declared inferior with regard to their physical, spiritual and character traits.

A ruthless but skillful propaganda among farm-workers of alien blood, to the effect that neither they nor their children, produced on the soil of German people, could expect much good; in other words, immediate separation of parents and children, eventually complete estrangement; sterilization of children afflicted with hereditary disease.

Charged with crimes against humanity and war crimes for "compelling abortions on Eastern workers" and "preventing marriages and hampering reproduction of enemy nationals" Griefelt and all but one of the defendants were pronounced guilty and sentenced to imprisonment of up to twenty-five years.

In Poland v. Höss, the defendant, commandant of the Auschwitz concentration camp, was charged with the persecution of Poles and Jews, a crime against humanity, as well as war crimes against Soviet prisoners of war. Under the command of Höss, camp personnel performed medical experiments on the male and female prisoners. Data were collected to quantify the most effective means to castrate men, sterilize women, or terminate pregnancies. The castration experiments employed high dosages of x-rays that caused infertility together with severe burns on prisoners' genitalia, physical debilitation, mental stress, and often the death of the victims. The pregnancy experiments involved the premature terminations of pregnancy, including injecting pregnant women with typhus-infected blood and then artificially provoking labor. The Polish tribunal found Höss guilty and sentenced him to death.

In 1961 Israel prosecuted former Nazi Adolf Eichmann for devising measures intended to prevent childbearing among Jews in the Theresienstadt (in Czech Terezín) ghetto. The court found, however, that Eichmann was not involved in the imposition of measures to prevent births as an act of genocide. It held that the primary intent of forbidding births and interrupting the pregnancies of Jewish women in the Theresienstadt ghetto was to exterminate Jews and not prevent births. The court drew a distinction between the intent of cruel medical procedures and that of measures intended to prevent births as proscribed in Article II(d).

The three cases are instructive. The Greifelt case demonstrated the actual measures executed by Nazi racist ideology to prevent births among foreign forced laborers. The Höss and Eichmann cases revealed the gruesome nature of medical procedures performed on camp inmates who were already condemned to death. The experiments conducted at Auschwitz were not performed to prevent births among the inmates, but rather, they served to perfect any future measures to restrict births. The medical procedures cited in the Eichmann case were a first step in the extermination of Jewish inmates. Even though the medical experiments and other acts did not represent the imposition or execution of measures to prevent births among inmates, a frighteningly direct ideological link exists between Nazi sterilization policies, the Nuremberg Laws, and the camp experiments. Auschwitz and Theresienstadt were precursors of what would have become even more draconian measures to prevent births among non-Aryans had the Third Reich triumphed.

Legal Background of Article II(d)

On December 11, 1946, the General Assembly passed Resolution 96(I). It defined genocide as a denial of the right of existence of entire human groups and "[a]ffirmed that genocide is a crime under international law which the civilized world condemns." Resolution 96(I) was a declaration of principles that guided the drafting of the Genocide Convention. Another historical forerunner to the Genocide Convention was the Draft Convention for Genocide prepared by the UN Secretariat. The Draft Convention divided genocidal acts into three subcategories: the physical, biological, and cultural. Article I(2) of the Draft Convention characterized biological genocide as "measures aimed at extinction of a group of human beings by systematic restrictions on births, without which the group cannot survive." Methods cited to accomplish this form of genocide were sterilization or compulsory abortions, segregation of the sexes, or obstacles to marriage.

An ad hoc committee revised the Draft Convention and proposed language for Article II(4) that proscribed "imposing measures intended to prevent births within the group." The eventual Genocide Convention adopted the ad hoc committee's language. The final wording abandoned the terms "biological genocide" and "restricting births" and made no direct references to measures such as sterilization, compulsory abortions, or obstacles to marriage, or to the systematic allocation of work to men and women in different locations. Still, the drafters' objective in crafting Article II(d) was to shield groups from these very acts. The essential aspect of Article II(d) is that it condemns, as an act of genocide, measures intended to prevent births within a racial, national, religious, or racial group.

Commentary on Article II(d)

In 1949 Nehemiah Robinson wrote an early noteworthy commentary on the Genocide Convention. He focused on two aspects of Article II(d): the number of births that must be prevented and the range of acknowledged measures to prevent births. He addressed the first aspect as follows:

Subparagraph (d) may in practice give rise to the problem whether the intention must be to prevent all births within the group or is it sufficient that it relates to some births only [emphases in original]. Although this subparagraph speaks not of restriction but prevention, it must be admitted that the intent of partial prevention suffices since the requirement of total prevention would conflict with the definition of Genocide as relating not only to the group as a whole, but also to a part of it.

[T]he factual extent of prevention should be of no import once it is established that it was imposed on members of the protected groups only (1949).

Robinson observed that the number of actual births prevented is relevant only in terms of whether the intention was to prevent, even partially, the births within a group.

In Robinson's second commentary on the Genocide Convention, written in 1960, he reiterated the view that the "the actual extent of prevention may not be decisive once it is established that it was imposed . . . with the intent of destruction." Among contemporary historians, William A. Schabas writes that "Article II(d) of the Convention does not make a result [emphasis in original] a material element of the offence. The actus reus consist of the imposition of measures; it need not be proven that they have actually succeeded" (2000). Hence, a common interpretation of Article II(d) is that quantity or actual numbers of unborn members of a group is not required to establish an act of genocide. Such statistics could, however, demonstrate that the measures imposed were intended to prevent births and that they were effective.

Robinson's other observation in the 1949 commentary expressed the view that the Genocide Convention purposely implied a nonexhaustive range of measures which could satisfy Article II(d), noting that "the measures imposed need not be the classic actions of sterilization; separation of the sexes, prohibition of marriages and the like may achieve the same results" (p. ?). In his second commentary, written in 1960, Robinson added that other measures could be "equally restrictive." Schabas and Otto Triffterer agree with Robinson's remarks that Article II(d) does not limit the types of measures which can be imposed to prevent births within a group.

The language of the treaty leaves open for debate the scope of what could be considered "measures imposed with the intent to prevent births." During the prolonged period before the United States ratified the Genocide Convention, the phrase "intent of measures imposed" provoked controversy and remains polemical. The modern debate is linked to the historical circumstances that prodded the writing of Article II(d).

U.S. Ratification and Article II(d)

The United States was one of the original signatories of the Genocide Convention in 1948, but the U.S. Senate only gave advice and consent to ratification in 1987, after bouts of indifference, defiance, and finally adherence. The acceptance of Article II(d) was contentious. Some senators questioned whether governmentsponsored birth control programs used overwhelmingly by African Americans, Hispanic Americans, or Native Americans might be construed as an act of genocide within the context of Article II(d). They pointed to a thesis of African American genocide that questioned the motives behind proposed legislative bills to authorize involuntary or punitive sterilizations, or the real objectives of legalized family-planning programs and abortion laws as acts of genocide. Black Brazilians voiced similar concerns in the 1970s about state policies that favored a reduction in the number of Black Brazilian births. U.S. proponents of ratification countered such arguments by emphasizing that government-sponsored birth control and family planning programs are voluntary, not compulsory, and they do not aim to destroy any group within the United States.

Another issue of concern for lawmakers considering the ratification of Article II(d) was the history of medical experiments in the United States, notably the Tuskegee syphilis experiment. Between 1930 and 1950 U.S. government officials intentionally withheld the diagnosis of syphilis from a sampling of African American men, all the while diligently but silently recorded the progression of their disease, including the inevitable side-effect of sterility. The officials did not medically treat the men to alleviate or stop the disease. Some senators raised concerns that such acts would constitute violations under Article II(d). Proponents of the Genocide Convention insisted that such medical experiment policies had come to a halt by the 1960s.

Qualms about the United States' racist past and its vulnerability to charges under the Genocide Convention had been voiced from the outset of the Convention's existence. Raphael Lemkin, in the 1950s, had attempted to quell these American fears by observing that "in the Negro problem the intent is to preserve the group on a different level of existence, . . . but not to destroy it."

In 1986 the United States officially ratified Article II(d) as well as other provisions of the Genocide Convention. The Senate, however, expressed general reservation about the terms of the Convention, indicating that the United States could refuse the compulsory jurisdiction of the International Court of Justice (ICJ) if another state accused it of violating the Genocide Convention.

Article II(d) and International Criminal Tribunals

Several international tribunals have included Article II(d) of the Genocide Convention verbatim in their statutes. The ad hoc International Criminal Tribunals for the Former Yugoslavia (ICTY) and Rwanda (ICTR), as well as the Special Panels of East Timor, have jurisdiction over alleged acts of genocide that involve the imposition of certain measures to prevent births. As of 2003 cases tried before these international tribunals have not included prosecutions fort measures intended to prevent births. The Akayesu judgment, issued by the ICTR in 1998, however, held that measures under Article II(d) "should be construed as sexual mutilation, the practice of sterilization, forced birth control, separation of the sexes and prohibition of marriages."

On another matter, the Akayesu judgment abruptly departed from Robinson's list of measures, which argued that forced births could not be viewed as a measure to prevent births. The ICTR stated that in patriarchal societies, the rape of women during times of war could be construed as the enemy's attempt to impose their ethnic identity on any newborn children. The Trial Chamber opined that:

[A] measure intended to prevent births within a group is a case where during a rape, a woman of the said group is deliberately impregnated by a man of another group, with the intent to have her give birth to a child who will not consequently belong to the mother's group.

Similarly, in 1996, the ICTY had held, in a preliminary proceeding against former Bosnian Serb president Radovan Karadzic, that the "systematic rape of women in some cases is intended to transmit a new ethnic identity." The Akayesu judgment also observed that a psychological component to the prevention of birth could operate to violate Article II(d) safeguards:

[T]he Chamber notes that measures intended to prevent births within a group may be physical, but can also be mental. For instance, rape can be a measure intended to prevent births when the person raped refuses subsequently to procreate, in the same way that members of a group can be led, through threats or trauma, not to procreate.

The ICTR Akayesu judgment is considered obiter dicta, meaning that its interpretation lay outside of the relevant factual and legal issues in the actual case before the judges. In Kayhishema and Rutaganda, the second judgment issued by the ICTR, the Trial Chamber concurred, again in obiter dicta, with the interpretation of Article II(d) that had been voiced in the Akayesu case. Schabas acknowledged the potential absurdity of the judicial views that classify rape as a measure to prevent births; however, he also recognized that a sober reading of Article II(d) lends itself to the contemplation of any measures as long as the intent to prevent births is present. Infliction of rapes, sexual mutilations, and any other actions that transfer the ethnic identity of the child to a group other than the mother's, or that intentionally discourage or restrict future procreation feasibly, lies within Article II(d). Triffterer noted the potential judicial relevance of these ICTR findings and the influence they might exert on the interpretation of the Rome Statute of the International Criminal Court (ICC).

Biological Weapons and Article II(d)

Speculation about other potential "measures imposed to prevent births within a group" remains lively. Several propositions, related to wartime scenarios, are repeatedly raised, such as biological or chemical warfare or rape-induced AIDS as acts that could contravene Article II(d).

The Genocide Convention does not explicitly cite military weapons as a type of measure intended to prevent births within a group. Even though the Draft Genocide Convention employed the term "biological genocide," its use was unrelated to biological or chemical warfare, as those terms were utilized in World War I to denote the deployment of mustard gas against enemy soldiers. Modern armed conflicts have employed biological or chemical agents against enemy soldiers, civilian populations, or the environment to defoliate jungle terrain. Scientific research acknowledges the existence of the short- and long-term affects of these chemical or biological agents on male and female reproductive abilities. Exposed female populations exhibit higher rates of spontaneous abortions or miscarriages and the birth of terminally ill or severely disabled children. Exposure to chemical and biological weapons has prompted some men and women to forego childbearing, due to their fear of conceiving mentally or physically disabled offspring. Could the use of biological or chemical weapons be a means to prevent births within a group, or similar to the medical experiments performed in concentration camps during World War II, if the primary intent is to kill the population and not to prevent their reproductive capacity?

Analogous observations have been raised in regard to women raped by AIDS-infected soldiers during wartime. Sexually transmitted diseases that eventually kill the offspring of women who were raped could be seen as measures intended to prevent births. Women may make an anguished decision not to reproduce in order to refrain from bearing terminally ill children. The mental trauma that the ICTR cases refer to, which could cause victims of rape to forsake procreation, might apply to individuals exposed to chemical or biological agents, or sexually transmitted diseases. Either act could lead to the decision not to give birth. If the intent behind deploying biological weapons or ensuring the transmission of fatal sexually transmitted diseases, such as AIDS, includes destroying a religious, racial, ethnic, or national group, in whole or part, by preventing births, such measures clearly run afoul of Article II(d).

Conclusion

Genocide, the denial of the right of existence of entire groups of human beings, often erupts during vast political or military upheavals. Certain acts of genocide, however, can exist and flourish when—ostensibly nonwartime—policies are aimed at eliminating racial, religious, national, or ethnic groups. Policies supporting racial purity or nationhood, as when transformed into measures to determine who should live and procreate, are acts of genocide. Whether prompted by legislation, or overseen by politicians, doctors, lawyers, or cruel camp commanders, these are acts of genocide. Like massive extermination or killings, the intent to suppress a group prior to its birth and reduce or decimate the membership to a designated purpose is a fundamental crime, one that the Genocide Convention, as recognized in Article II(d), seeks to prevent or punish.

SEE ALSO Nuremberg Laws; Rape

BIBLIOGRAPHY

Abdias do Nascimento (1978). O Genocidio Do Negro Brasileiro-Processo de um Racismo Mascarada. Rio de Janiero, Brazil: Paz e Terra.

Ad Hoc Advisory Panel (1973). Tuskeegee Syphilis Study. Washington, D.C.

Annas, George, and Michael Grodin (1992). The Nazi Doctors and the Nuremberg Code. New York: Oxford University Press.

Poland v. Hoess. Case No. 7 LRTWC II, Supreme National Tribunal of Poland (1948).

Power, Samantha (2002). A Problem from Hell–America and the Age of Genocide. Hammersmith, U.K.: Flamingo/HarperCollins.

Proctor, Robert N. (1988). Racial Hygiene Medicine under the Nazis. Cambridge, Mass.: Harvard University Press.

Schabas, William A. (2000). Genocide in International Law: The Crime of Crimes. Cambridge: Cambridge University Press.

United States of America v. Geifelt et al. Case No. 13 LRTWC, United States Military Tribunal (1948).

Weitz, Eric D. (2003). A Century of Genocide Utopias of Race and Nation. Princeton, N.J.: Princeton University Press.

Patricia Viseur Sellers

I am setting forth the above in my personal capacity.
This article represents neither the policies of the Office of the Prosecutor of the International Criminal Tribunal for the Former Yugoslavia nor the United Nations.

REPRODUCTION

A woman's right to determine whether she will give birth was not legally recognized until the 1960s and 1970s, when U.S. Supreme Court decisions established that right. Until that time, women in the United States were denied access to birth control and to legal abortions by state criminal laws. Since the 1970s, there has been ongoing controversy over legalized abortion, with the Supreme Court allowing states to impose restrictions on obtaining the procedure. In addition, medical science has developed techniques of artificial insemination and in vitro fertilization that enable pregnancy. These advances, in turn, have created opportunities for surrogate motherhood, opening up even more legal issues dealing with reproductive rights. Because of the cultural importance placed on motherhood and the intersection of religious beliefs and public policy, the debate over reproductive rights has been contentious.

Historical Background

In the nineteenth century, the average size of the U.S. family declined dramatically. A white woman in 1800 gave birth to an average of seven children. By the end of the century, the average was three-and-a-half children. In part, the decline was caused by the dissemination of scientific information on birth control. Many of the nineteenth-century proponents of family planning were radical social reformers who offended church and community leaders with their graphic descriptions of human reproduction.

Conservatives sought to curtail this information on birth control and abortion. The most prominent conservative watchdog was Anthony Comstock, a New York businessman who led a national reform effort against obscene materials. His work resulted in the federal comstock law of 1873, which criminalized the transmission and receipt of "obscene," "lewd," or "lascivious" publications through the U.S. mail. The law specified that materials designed, adapted, or intended "for preventing conception or producing abortion" were included in the list of banned items. Some states passed "little Comstock laws" that prohibited the use of contraceptives.

Until the second half of the nineteenth century, few states had criminal laws against abortion. Women in colonial times had used abortion to dispose of the offspring of rape or seduction. Abortion was not illegal under the common law as long as it was performed before "quickening," the period at about four months when the fetus begins to move in the womb.

State legislatures passed laws in the first half of the nineteenth century that adopted the quickening rule, and a few states allowed abortion after quickening to save the life of the mother. Abortions increased markedly in the 1850s and 1860s, especially among middle-class white women.

Religious leaders began to denounce abortion, but the american medical association (AMA) proved to be the most successful in ending legalized abortion. The AMA was formed in 1847, and the all-male professional group (women were not allowed to become doctors) made abortion law reform one of its top priorities. The AMA saw abortion reform as a way to increase its influence and to drive out unlicensed practitioners of abortion. By the 1880s, medical and religious leaders had convinced all-male state legislatures (women were not allowed to vote) to impose criminal penalties on persons performing abortions and, in some states, on the women who had abortions. The laws were based on the states' police power to regulate public health and safety. This had some justification because abortion procedures of the time were dangerous, subjecting women to sterility and, in many cases, death. In response, women turned to birth control and to illegal abortions. The legal restrictions on birth control and abortion that were created in the late nineteenth century were not be removed until the 1960s and 1970s.

Restricting Antiabortion Protests

The legalization of abortion resulted in the creation of many groups opposed to the medical procedure. Some groups have sought to take away this reproductive right by lobbying Congress and state legislatures, and others have picketed outside clinics that offer abortion services. In the 1990s, groups such as Operation Rescue sought to prevent abortions by organizing mass demonstrations outside clinics and blockading their entrances, as well as confronting and impeding women seeking to enter the clinics.

Clinics responded by obtaining court injunctions that restricted how close abortion protestors could get to clinic property. Abortion protestors claimed that these court orders violated their first amendment rights of assembly and free speech.

The U.S. Supreme Court, in Schenck v. Pro-Choice Network of Western New York, 519 U.S. 357, 117 S. Ct. 855, 137 L. Ed. 2d 1 (1997), clarified what types of restrictions a judge could impose on abortion clinic protests. The Court upheld an injunction provision that imposed a fixed buffer zone around the abortion clinic. In this case the buffer zone affected protests within 15 feet from either side or edge of, or in front of, doorways or doorway entrances, parking lot entrances, and driveways and driveway entrances. Chief Justice william h. rehnquist ruled that the government had an interest in ensuring public safety and order, promoting free flow of traffic, protecting property rights, and protecting a woman's freedom to seek pregnancy-related services.

The Court did strike down a provision concerning floating buffer zones. These zones, which prohibited demonstrations within 15 feet of any person or vehicle seeking access to or leaving abortion facilities, "burdened more speech than was necessary" to serve the government interests cited in support of fixed zones. Thus, protestors were free to approach persons outside the 15-foot fixed buffer zone.

In 2000, though, the Court again considered the issue of a buffer zone in Hill v. Colorado, 530 U.S. 703, 120 S. Ct. 2480, 147 L. Ed. 2d 597 (2000). The Court upheld Colorado's 1993 statute, which prevented anyone from counseling, distributing leaflets, or displaying signs within eight feet of others without their consent whenever they are within 100 feet of a health-clinic entrance. The Colorado law was enacted, according to attorneys for the state, after abortion patients complained of being spat on, kicked, and harassed outside clinics. Those who challenged the law claimed it was a violation of their freedom of speech under the First Amendment. The court found sufficient public and state interest to uphold the restriction.

further readings

Briant, Keith. 1962. Marie Stopes: A Biography. London: Hogarth.

Korn, Peter. 1996. A Year in the Life of an Abortion Clinic. New York: Grove/Atlantic.

cross-references

Abortion; Roe v. Wade.

Birth Control

In the early twentieth century, a group of reformers sought to legally provide birth control information. The most prominent of these reformers was margaret sanger, who coined the term birth control. Sanger challenged state laws restricting birth control information, seeking to draw public support. Though the courts generally rebuffed her efforts, Sanger helped build a national movement. In 1921, she founded the American Birth Control League, which, in 1942, became the Planned Parenthood Federation of America.

Renewed legal challenges to restrictive state laws began in the 1950s. By 1960, almost every state had legalized birth control. Nevertheless, laws remained on the books that prevented the distribution of birth control information and contraceptives. A specific target was the 1879 Connecticut little Comstock law that made the sale and possession of birth control devices a misdemeanor. The law also prohibited anyone from assisting, abetting, or counseling another in the use of birth control devices.

The Supreme Court reviewed the Connecticut law in griswold v. state of connecticut, 381 U.S. 479, 85 S. Ct. 1678, 14 L. Ed. 2d 510 (1965). Estelle Griswold was the director of Planned Parenthood in Connecticut. Just three days after Planned Parenthood opened a clinic in New Haven, Griswold was arrested. She was convicted and fined $100. The Connecticut courts upheld her conviction, rejecting the contention that the state law was unconstitutional.

The Supreme Court struck down the Connecticut birth control law on a vote of 7 to 2. In his majority opinion, Justice william o. douglas announced that the law was unconstitutional because it violated an individual's right to privacy. Douglas asserted that "specific guarantees in the bill of rights have penumbras, formed by emanations from those guarantees that help give them life and substance. Various guarantees create zones of privacy." Thus, these "penumbras" (things on the fringe of a major region) and "emanations" added up to a general, independent right of privacy. In Douglas's view, this general right was infringed by the state of Connecticut when it outlawed birth control. He said that the state cannot be permitted "to search the sacred precincts of marital bedrooms for telltale signs of the use of contraceptives."

The Griswold decision invalidated the Connecticut law only insofar as it invaded marital privacy, leaving open the question of whether states could prohibit the use of birth control devices by unmarried persons. In Eisenstadt v. Baird, 405 U.S. 438, 92 S. Ct. 1029, 31 L. Ed. 2d 349 (1972), the Court reviewed a Massachusetts law that prohibited unmarried persons from obtaining and using contraceptives. William Baird was arrested after giving a lecture on birth control to a college group and providing contraceptive foam to a female student. The Court struck down the law, establishing that the right of privacy is an individual right, not a right enjoyed only by married couples. Justice william j. brennan jr., in his majority opinion, stated, "If the right of privacy means anything, it is the right of the individual, married or single, to be free from unwarranted governmental intrusion into matters so fundamentally affecting a person as the decision whether or not to beget a child."

With Griswold and Eisenstadt, state prohibition of birth control information and devices came to an end. These decisions also enabled schools to give more information to students concerning sex education. Some schools even dispense contraceptives.

In 1997, the food and drug administration (FDA) approved the use of emergency contraceptive, known popularly as the "morning-after pill." Developed by Canadian professor Albert Yuzpe and known as the Yuzpe Regimen, the pill contains heavy dosages of hormones that can prevent pregnancy if taken 72 hours after sexual intercourse. Proponents, including pro-choice advocates in the abortion debate, claim that it is a safe and effective method of birth control. Pro-life advocates and others denounce the pill as a form of abortion. Some critics in the medical field also claimed that repeated use of the pill could have unknown long-term effects due to its high level of hormones.

Abortion

The establishment in Eisenstadt of an individual's right to privacy soon had dramatic implications for state laws that criminalized abortions. Until the 1960s, abortion was illegal in every state, except to save the mother's life. The growth of the modern feminist movement in the 1960s led to calls for the legalization of abortion, and many state legislatures began to amend their laws to permit abortion when the pregnancy resulted from a rape or when the child was likely to suffer from a serious birth defect. However, these laws generally required that a committee of doctors approve the abortion.

State legislation was swept away with the Supreme Court's controversial decision in roe v. wade, 410 U.S. 113, 93 S. Ct. 705, 35 L. Ed. 2d 147 (1973). A class action lawsuit challenged the state of Texas's abortion law. sarah weddington, the attorney for "Jane Roe," argued that the Constitution allows a woman to control her own body, including the decision to terminate an unwanted pregnancy.

The Supreme Court, on a 7–2 vote, struck down the Texas law. Justice harry a. black-mun, in his majority opinion, relied on the prior right to privacy decisions to justify the Court's action. Blackmun concluded that the right to privacy "is broad enough to encompass a woman's decision whether or not to terminate her pregnancy." More importantly, he stated that the right of privacy is a fundamental right. This meant that the state of Texas had to meet the strict scrutiny test of constitutional review. Texas showed a compelling state interest because it had a strong interest in protecting maternal health that justified reasonable state regulation of abortions performed after the first trimester (three months) of pregnancy. However, Texas also sought to proscribe all abortions and claimed a compelling state interest in protecting unborn human life. Though the Court acknowledged that this was a legitimate interest, it held that it does not become compelling until that point in pregnancy when the fetus becomes "viable," capable of "meaningful life outside the mother's womb." Beyond the point of viability, the Court held that the state may prohibit abortion, except in cases in which it is necessary to preserve the life or health of the mother.

The Court rejected the argument that a fetus is a "person" as that term is used in the Constitution and thus possesses a right to life. To find a fetus to be a person would make any abortion a homicide, which would prevent a state from allowing abortions in cases of rape or in which the pregnancy endangers the life of the mother.

The Roe decision elicited a hostile reaction from opponents of abortion. The creation of a "pro-life" movement that sought to overturn Roe was immediate, becoming a new fixture in U.S. politics. Pro-life forces sought a constitutional amendment to undo the decision, but it fell one vote short in the U.S. Senate in 1983. Over time, as the composition of the Supreme Court has changed, the Court has modified its views, without overturning Roe.

In the 1970s, a majority of the Court resisted efforts by some states to put restrictions on a woman's right to have an abortion. In Planned Parenthood of Central Missouri v. Danforth, 428 U.S. 52, 96 S. Ct. 2831, 49 L. Ed. 2d 788 (1976), the Court struck down a Missouri law that required minors to obtain the consent of their husbands or parents before obtaining an abortion. In 1979, in Bellotti v. Baird, 443 U.S. 622, 99 S. Ct. 3035, 61 L. Ed. 2d 797, the Court invalidated a similar Massachusetts law. Both opinions emphasized the personal nature of abortion decisions and the fact that the state cannot give someone else a veto over the exercise of one's constitutional rights.

In Akron v. Akron Center for Reproductive Health, 462 U.S. 416, 103 S. Ct. 2481, 76 L. Ed. 2d 687 (1983), the Court struck down a city ordinance that required that all abortions be performed in hospitals; a twenty-four-hour waiting period must pass before an abortion could be performed; certain specified statements be made by a doctor to a woman seeking an abortion to ensure that she made a truly informed decision; and all fetal remains be disposed in a humane and sanitary manner. The Court held that these requirements imposed significant burdens on a woman's exercise of her constitutional right without substantially furthering the state's legitimate interests.

Opponents of abortion were successful, however, in preventing the payment of public funds for abortions not deemed medically necessary. In Maher v. Roe, 432 U.S. 464, 97 S. Ct. 2376, 53 L. Ed. 2d 484 (1977), the Court upheld a Connecticut state regulation that denied medicaid benefits to indigent women seeking to have abortions, unless their physicians certified that their abortions were medically necessary. The Court found the law permissible because poor women were not a "suspect class" entitled to strict scrutiny review and because the regulation did not unduly burden the exercise of fundamental rights. In 1980, the Court upheld a provision of federal law, commonly known as the Hyde amendment, forbidding federal funds to support nontherapeutic abortions (Harris v. McRae, 448 U.S. 297, 100 S. Ct. 2671, 65 L. Ed. 2d 784).

During the 1980s and 1990s, the conservative majority on the Court showed more deference to state regulation of abortions. In webster v. reproductive health services, 492 U.S. 490, 109 S. Ct. 3040, 106 L. Ed. 2d 410 (1989), the Court upheld a Missouri law restricting abortions that contained the statement, "the life of each human being begins at conception." On a 5–4 vote, the Court upheld a law that forbids state employees from performing, assisting in, or counseling women to have abortions. It also prohibited the use of any state facilities for these purposes and required all doctors who would perform abortions to conduct viability tests on fetuses at or beyond 20 weeks' gestation.

In 1991, the Court upheld federal regulations imposed by the Reagan administration that barred birth control clinics that received federal funds from providing information about abortion services to their clients (Rust v. Sullivan, 500 U.S. 173, 111 S. Ct. 1759, 114 L. Ed. 2d 233). The Supreme Court found the regulation to be a legitimate condition imposed on the receipt of federal financial assistance.

The Court appeared to be ready to overturn the Roe precedent, but it surprised observers when it upheld Roe in Planned Parenthood v. Casey, 505 U.S. 833, 112 S. Ct. 2791, 120 L. Ed. 2d 674 (1992). The Pennsylvania law restricting abortions required spousal notification, parental consent in cases of minors, and a 24-hour waiting period before the abortion could be performed. Similar requirements had been struck down by the Court before.

On a 5–4 vote, the Court reaffirmed the essential holding of Roe that the constitutional right of privacy is broad enough to include a woman's decision to terminate her pregnancy. Though there was no majority opinion, the controlling opinion by Justice anthony m. kennedy, joined by Justices sandra day o'connor and david h. souter, defended the reasoning of Roe and the line of cases that followed it. However, the joint opinion abandoned the trimester framework and declared a new "undue burden" test for judging regulations of abortion. Using this test, the joint opinion upheld the parental consent, waiting period, and record-keeping and reporting provisions, but invalidated the spousal notification requirement.

Pregnancy and Medical Developments

Artificial insemination, in vitro fertilization, and embryo transplants have created new opportunities for conceiving children. With artificial insemination, sperm from a donor is introduced into the vagina or through the cervix of a woman by any method other than sexual inter-course. Originally this technique was used when a husband was sterile or impotent, but it is now available to women regardless of whether they are married. For example, a lesbian couple could

use artificial insemination to start a biological family.

The technique of in vitro fertilization gained international attention with the 1978 birth in England of Louise Brown, the first child conceived by in vitro fertilization. This technique involves the fertilization of the egg outside the womb. The embryo is then transferred to a woman's uterus.

Because sperm and eggs can be frozen and stored indefinitely, there are occasional legal disputes over the rights to these genetic materials when a husband and wife divorce. For example, in Kass v. Kass, 696 N.E. 2d 174 (N.Y. 1998), the New York Court of Appeals determined that the custody of five frozen embryos should be determined by the terms of a contract signed by a couple with a hospital that stored the embryos. The couple had sought to become pregnant through in virto fertilization, but, after several failed attempts, decided to divorce. The husband and wife initially agreed to the terms of a consent decree with the hospital whereby the hospital could retain the right to keep the embryos for research purposes. The wife later changed her mind and wanted custody of the embryos. The court held that the consent agreements constituted valid contracts and must be enforced. The court ruled that under the terms of the contract, the hospital should be awarded the embryos for use in research.

Other courts have considered disputes whereby one spouse wishes to use embryos for the purpose of procreation while the other wants the embryos destroyed. Several state supreme courts have held that the right of a spouse who wishes to avoid procreation is superior to the wishes of spouse who wishes to procreate. In J. B. v. M. B., 783 A. 2d 707 (N.J. 2001), for example, the New Jersey Supreme Court determined that a husband's right to procreate was not disturbed by its ruling that remaining frozen embryos from the husband and wife be destroyed according to the wishes of the wife.

Developments in in vitro fertilization led to surrogate motherhood, which has caused legal battles as well. In these cases, a woman agrees to be either artificially inseminated by a spermdonor father or have a fertilized ovum inserted into her uterus. After giving birth, the surrogate mother legally surrenders the infant to the person or couple who will adopt and rear the child. The idea of surrogate motherhood is attractive to some couples because a child born of a surrogate mother will share half or all the genetic material of the parents who will raise the child.

One of the most publicized cases regarding surrogate motherhood is that of Baby M. In 1985, Mary Beth Whitehead agreed to be inseminated with the sperm of William Stern and, upon the birth of the child, relinquish her parental rights to Stern. But once the child was born, Whitehead found that she did not wish to give up the child, a girl who she named Sara. A court battle ensued, during which Stern, along with his wife, Elizabeth, were granted temporary custody of the child they had named Melissa. The court decided that Whitehead's parental rights were to be terminated, and Elizabeth Stern was granted the right to immediately adopt the child. The New Jersey Supreme Court overturned this verdict in part on February 2, 1988, restoring Whitehead's parental rights and invalidating Elizabeth Stern's adoption, but granting William Stern custody of the infant.

Many surrogate mothers are close friends or relatives of the childless couple. However, the practice of commercial surrogate arrangements has increased greatly since the late 1980s. Many major cities have surrogate agencies, which are often run by doctors and lawyers who maintain lists of potential surrogate mothers and help match a woman with a couple wanting to have a baby. Commercial surrogate agencies typically charge a fee of $10,000 or more to make the arrangements, which is in addition to the surrogate mother's expenses and fees, which may range from $10,000 to $100,000.

Commercial surrogate arrangements are not legal in all states, and there is little case law on the subject. Some states declare surrogacy contracts null, void, and unenforceable because they are against public policy. Opponents of commercial surrogacy believe that such arrangements exploit the surrogate mother and turn children into a commodity. They also are concerned that if a child is born with a disability, the adoptive parents may decline to take the child. Finally, there is the issue of the surrogate mother who may not wish to surrender the child after birth.

Other medical developments have also stirred controversy. In 1997, scientists successfully cloned the first adult animal, leading to speculation that the process could be used to clone human beings. Scientists first successfully inserted DNA from one human cell into another human egg, but they do not expect successful human cloning to be possible for several years. The issue has caused heated debates focusing on the scientific, moral, and religious concerns over the possibility that an adult human could be cloned.

Reproductive Hazards in the Workplace

Legal disputes have arisen when employers have barred pregnant women and women of childbearing age from jobs that pose potential hazards to the fetus. The Supreme Court, in United Auto Workers v. Johnson Controls, 499 U.S. 187, 111 S. Ct. 1196, 113 L. Ed. 2d 158 (1991), ruled that a female employee cannot be excluded from jobs that expose her to health risks that may harm her fetus. The Court found that the exclusion of the women violated Title VII of the civil rights act of 1964 (42 U.S.C.A. § 2000e et seq.) because the company policy only applied to fertile women, not fertile men. Justice Blackmun, in his majority opinion, noted that the policy singled out women on the basis of gender and childbearing capacity rather than on the basis of fertility alone. Concerns about the health of a child born to a worker at the plant were to be left "to the parents who conceive, bear, support, and raise them [the children] rather than to the employers who hire those parents."

further readings

"Genetics, Reproduction, and the Law." 1999. Trial 35 (July).

Hollinger, Joan Heifetz. 1985. "From Coitus to Commerce: Legal and Social Consequences of Noncoital Reproduction." University of Michigan Journal of Law Reform 18 (summer).

"In re Baby M" (colloquy). 1988. Georgetown Law Journal 76 (June).

"In re Baby M" (symposium). 1988. Seton Hall Law Review 18 (fall).

Levy, Stephanie. 2001. "Whose Embryo Is It Anyway? Courts Wrestle with Issues of High-tech Reproduction." Trial 37 (December).

Rahman, Anika. 1995. "Toward Government Accountability for Women's Reproductive Rights." St. John's Law Review 69 (winter-spring).

Ridder, Stephanie, and Lisa Woll. 1989. "Transforming the Grounds: Autonomy and Reproductive Freedom." Yale Journal of Law and Feminism 2 (fall).

Robertson, John A. 1988. "Procreative Liberty And The State's Burden Of Proof In Regulating Noncoital Reproduction." Law, Medicine & Health Care 16 (spring-summer).

cross-references

Abortion; Adoption; Fetal Rights; Fetal Tissue Research; Genetic Engineering; Husband and Wife; Penumbra; Sex Discrimination; Wattleton, Alyce Faye; Women's Rights.

REPRODUCTION

CONCEPT

The term reproduction encompasses the entire variety of means by which plants and animals produce offspring. Reproductive processes fall into two broad groupings: sexual and asexual, the latter being the means by which bacteria and algae reproduce. Many plants reproduce sexually by means of pollination, and some plants alternate between sexual and asexual forms of reproduction. Other creatures, such as bees and ants, reproduce through a form of reproduction called parthenogenesis, which is neither fully sexual nor asexual.

HOW IT WORKS

Asexual Reproduction

Asexual reproduction involves only one organism, as opposed to two in sexual reproduction. It occurs when a single cell divides to form two daughter cells that are genetically identical to the parent cell. This process is known as fission, and it may take the form either of binary fission, in which two new cells are produced, or multiple fission, which results in the creation of many new cells. Since there is no fusion of two different cells, the daughter cells produced by asexual reproduction are genetically identical to the parent cell. Asexual reproduction usually takes place by mitosis, a process during which the chromosomes in a cell's nucleus are duplicated before cell division. (Mitosis, chromosomes, and many other topics referred to in this essay are discussed in considerably more detail in Genetics.)

Whereas sexual reproduction is extremely complex—and human sexual reproduction is much more so, freighted as it is with degrees of meaning that go far beyond mere biology—asexual reproduction is a fairly simple, cellular process. Of course, nothing in nature is really simple, and, in fact, the dividing and replication of DNA (deoxyribonucleic acid, the genetic blueprint material found in each cell) is a complicated subject; however, that subject, too, is discussed in the essay Genetics. DNA is located at the cell nucleus, which is the cell's control center, and the nucleus is the first part of the cell to divide in asexual reproduction. After the nucleus splits, the cytoplasm, or the cellular material external to the nucleus, then divides. The result is the formation of two new daughter cells whose nuclei have the same number and kind of chromosomes as the parent.

The adaptive advantage of asexual reproduction is that organisms can reproduce quickly and by doing so colonize favorable environments rapidly. (See Evolution for more about the importance of adaptation and environment in shaping species.) For example, some bacteria can double their numbers every 20 minutes. In addition to bacteria, which are discussed in more detail in Infection, other life-forms that reproduce asexu-ally include protozoa (varieties of which are examined in Parasites and Parasitology), blue-green algae, yeast, dandelions, and flatworms.

Sexual Reproduction

Sexual reproduction involves the union of two organisms rather than the splitting of one. Like asexual reproduction, it is a process that takes place at the cellular level. In sexual reproduction it is not binary fission that occurs, but the fusion of two cells. Nor are the two cells identical; rather, the cells—known as gametes—can be identified as either male or female according to the makeup of their chromosomes. The male gamete is called a sperm cell, and the female gamete is termed an egg cell. In sexual reproduction, the sperm cell fuses, or bonds, with the egg cell to produce a cell that is genetically different from either of the parent cells. This process of fusion is known as fertilization, and the fertilized egg is called a zygote. Gametes are produced in the male testes and female ovaries by a splitting process called meiosis. (Meiosis and other terms mentioned briefly in these paragraphs are discussed in much more detail in Genetics.)

Meiosis produces haploid cells, or ones that have half the number of chromosomes as are in a normal cell for that species. When the haploid sperm and egg cells fuse at fertilization, however, the chromosomes from both combine, so that the normal number of chromosomes appears in the zygote. The shuffling of the parents' genetic material that happens during meiosis allows for new gene combinations in offspring that account for variations between offspring (which is why you don't look just like your siblings) and which, over time, can improve a species' chances of survival.

REAL-LIFE APPLICATIONS

Examples of Asexual Reproduction

As we noted earlier, bacteria, blue-green algae, most protozoa, yeast, and flatworms all reproduce asexually, as do mosses and starfish. (The last actually reproduce both sexually and asexually by means of alternation of generations, discussed later.) The products of asexual reproduction are known as clones—an example of the fact, discussed in Genetic Engineering, that cloning and the concept of clones are not as new as one might imagine. (See that essay for much more about artificial cloning.) A starfish can regenerate and eventually produce a whole new organism from a single severed appendage, while flatworms divide in two and regenerate to form two new flatworms. This formation of a separate organism is obviously much more complex than the simple splitting of single bacteria cells, but it is still a form of asexual reproduction.

VEGETATIVE PROPAGATION.

Strawberries reproduce by forming growths called runners, which grow horizontally and generate new stalks. At some point, the runner decomposes, leaving a new plant that is a clone of the original. This is an example of vegetative propagation, a term for a number of processes by which crop plants are produced asexually. Vegetative propagation is used for such crops as potatoes, bananas, raspberries, pineapples, and some flowering plants. Its advantage to farmers is that the crops will be more uniform than those grown from seed. Furthermore, some plants are difficult to cultivate from seed, and the vegetative propagation of those plants makes it possible to grow crops that otherwise would not be available for commercial marketing.

In reproducing potatoes through vegetative propagation, farmers plant the so-called eyes to produce duplicates of the parent. With banana plants, the farmer separates the suckers that grow from the root of the plant and plants them. The farmer raising raspberry bushes bends the branches and covers them with soil, whereupon a process not unlike that of the runner growth of mosses takes place: the branches eventually grow into a separate plant, with their own root system, and ultimately can be detached from the parent plant.

Between Asexual and Sexual

The example of vegetative propagation suggests that there is not a sharp dividing line between sexual and asexual reproduction—that is, that many organisms can reproduce either way. This is true even of humans, who, in theory, could be cloned, though the technology to do so—let alone resolution of the ethical issues of the procedure—lies in the far distant future. (See Genetic Engineering for more on this subject.) Even humans, however, can use external fertilization, which is sexual reproduction without sexual intercourse (see Sexual Reproduction).

Plants go through a process known as alternation of generations, in which they alternate as sexual and asexual reproducers, or gametophytes and sporophytes, respectively. In the asexual stage, the sporophyte produces diploid reproductive cells called spores, which develop into gametophytes. These gametophytes produce haploid gametes, which then unite sexually to form a diploid zygote that grows into a sporophyte. In plain English, this means that the asexual "grand-parent" generates a sexually reproducing "child," which in turn produces a "grandchild" that is asexual, like its grandparent.

At one phase in the alternation of generation for mosses, for instance, male and female moss plants grow from spores. Male moss plants produce sperm cells, which, when the moss receives rainfall, are able to propagate because they have a medium (water) in which to move. They fertilize the female plants, producing zygotes. The zygote grows on top of the female moss plant, which helps to store moisture and thus provides a hospitable environment in which the zygote can develop. The zygote eventually produces haploid spores, which it releases into the air. These tiny spores, carried by the wind, float away from their point of origin until they come to rest, and soon the cycle begins once again.

PARTHENOGENESIS.

There are also organisms, including bees, ants, wasps, and other insects, that reproduce in a way that is neither fully sexual nor asexual. This is parthenogenesis, a type of reproduction in which a gamete develops without fertilization. In other words, a sex cell is reproduced without actual intercourse between male and female. The gamete is almost always female—a fact indicated in the name itself, which comes from parthenos, Greek for "maiden."

The Parthenon in Athens, like the city itself, is named after the goddess Athena (also called Minerva), who was known by the nickname Parthenos. She is said to have been born fully formed, having sprung from the head of her father, Zeus, dressed in armor and ready for battle. Thus, her own birth was a form of parthenogenesis, a word whose second half (a name well known from the Bible) means "beginning."

Pollen and Pollination

Pollen is a fine, powdery substance consisting of microscopic grains containing the male gametophyte of certain plants that reproduce sexually. These plants include angiosperms, a type of plant that produces flowers during sexual reproduction, and gymnosperms, which reproduce sexually through the use of seeds that are exposed and not hidden in an ovary, as with an angiosperm. Pollen is designed for long-distance dispersal from the parent plant, so that fertilization can occur. Pollination is the transfer of pollen from the male reproductive organs to the female reproductive organs of a plant, and it precedes fertilization. In other words, pollination is the equivalent of sexual intercourse for seed-bearing plants. Actually, cross-pollination, or the transfer of pollen from one plant to another, would perhaps be analogous to sexual intercourse in animals. Pollination occurs in seed-bearing plants, as opposed to the more primitive spore-producing plants, such as ferns and mosses. Gymnosperms, such as pines, firs, and spruces, produce male and female cones, whereas angiosperms produce flowers containing a male organ called the stamen and a female organ called the pistil. Both types of plants rely on insects and other creatures to aid in the pollen transfer.

DARWIN'S MOTH.

The German physician and botanist Rudolf Jakob Camerarius (1665-1721) was the first scientist to demonstrate that plants reproduce sexually, and he pioneered the study of pollination. One of the scientists influenced by his work was the English naturalist Charles Darwin (1809-1882), who discussed the subject in The Various Contrivances by which Orchids Are Fertilized by Insects (1862). Darwin wrote this book partly to support the ideas on evolution presented in his much more well known book Origin of Species (1859). In Various Contrivances, he suggested that orchids and their insect pollinators evolved by interacting with one another over many generations.

As an example, he discussed Angraecum sesquipedale, an orchid native to Madagascar. Darwin had not seen the plant in its native habitat, however; he had looked only at its dried leaves. The white flower of this orchid has a foot-long (30 cm) tubular spur with a small drop of nectar at its base, and from observing this, he hypothesized that the orchid had been pollinated by an insect with a foot-long tongue. This hypothesis, he wrote, "has been ridiculed by some entomologists," or scientists who study insects. After all, no such creature had been found in Madagascar. But then, around the turn of the nineteenth century—some two decades after Darwin's death—it was found. A Madagascan moth was discovered that had a foot-long tongue that uncoils to sip the nectar of A. sesquipedale as it cross-pollinated the flowers.

PLANTS AND THEIR POLLINATORS.

Angiosperms and gymnosperms are discussed in Ecosystems and Ecology, where each is compared in terms of its degree of adaptation to its environment. Angiosperms seem to be the hands-down winner: by enlisting the aid of insects and other pollinators, they manage to pollinate much more efficiently than gymnosperms, which have to produce vast quantities of pollen for each grain that reaches its target. Typically, pollination benefits the animal pollinator by supplying it with sweet nectar and, of course, benefits the plant by providing direct transfer of pollen from one plant to the pistil of another plant. For this reason, specific plant and animal species have developed a relationship of mutualism, a form of symbiosis in which each participant reaps benefits (see Symbiosis). In many cases, plant and pollinator have evolved together, and it is possible to determine which animal pollinates a certain flower species simply by studying the morphologic features (shapes), color, and odor of the flower.

For example, some flowers are pure red, or nearly pure red, and have very little odor. In most such situations, the pollinator is a bird species, since birds have excellent vision in the red region of the spectrum but a rather undeveloped sense of smell. It so happens that Europe, which has no pure red native flowers, also has no bird-pollinated native flower species. Not all bird-pollinated flowers are red, but they are all characterized by striking, and sometimes contrasting, colors that readily catch the eye. Examples of plants pollinated by birds include the cardinal flower, the red columbine, the hibiscus, the eucalyptus, and varieties of orchid, cactus, and pineapple.

Some flowering plants have a very strong odor but are very dark, or at least drab, in color. These flowers and plants—examples include the saguaro cactus, century plant, or cup-and-saucer vine—are often pollinated by bats, which have very poor vision, are typically active during the night, and have a very well developed sense of smell. The flowers of many plant species are marked with special pigments called flavonoids, which absorb ultraviolet light and appear to direct the pollinator toward the pollen and nectar. These pigments are invisible to humans and most animals, but bees' eyes have special ultraviolet photoreceptors that enable the bees to detect patterns and so pollinate these flowers.

WHERE TO LEARN MORE

"Asexual Reproduction Lab." Lester B. Pearson College of the Pacific (Web site). <http://www.pearson-college.uwc.ca/pearson/biology/asex/asex.htm>.

Canine Reproduction (Web site). <http://www.labbies.com/canine_reproduction_table_of_con.htm>.

CRES: The Center for Reproduction of Endangered Species/ San Diego Zoo (Web site). <http://www.sandiegozoo.com/conservation/cres_home.html>.

Elia, Irene. The Female Animal. New York: Henry Holt, 1988.

"Flowering Plant Reproduction." Estrella Mountain Community College (Web site). <http://gened.emc.maricopa.edu/bio/bio181/BIOBK/BioBookflowers.html>.

Kevles, Bettyann. Females of the Species: Sex and Survival in the Animal Kingdom. Cambridge, MA: Harvard University Press, 1986.

Kimball, Jim. "Asexual Reproduction ." Kimball's Biology Pages (Web site). <http://www.ultranet.com/~jkimball/BiologyPages/A/AsexualReproduction.html>.

Maxwell, Kenneth E. The Sex Imperative: An Evolutionary Tale of Sexual Survival. New York: Plenum, 1994.

The Pollination Home Page (Web site). <http://pollinator.com/>.

Reproduction (Web site). <http://www.factmonster.com/ce6/sci/A0841565.html>.

Topoff, Howard R. The Natural History Reader in Animal Behavior. New York: Columbia University Press, 1987.

Walters, Mark Jerome. The Dance of Life: Courtship in the Animal Kingdom. New York: Arbor House, 1988.

KEY TERMS

ALTERNATION OF GENERATIONS:

A process whereby plant generations alternate as sexual and asexual reproducers—gametophytes and sporophytes, respectively.

ASEXUAL REPRODUCTION:

One of the two major varieties of reproduction (along with sexual reproduction), In contrast to sexual reproduction, which involves two organisms, asexual reproduction involves only one. Asexual reproduction occurs when a single cell divides through mitosis to form two daughtercells, which are genetically identical to the parent cell.

BINARY FISSION:

The process in asexual reproduction whereby a single cell divides to form two daughter cells that are genetically identical to the parent cell.

CLONE:

A cell, group of cells, or organism that contains genetic information identical to that of its parent cell or organism.

CLONING:

A specialized genetic process whereby clones are produced. Cloning is a form of asexual reproduction.

CHROMOSOME:

A DNA-containing body, located in the cells of most living things, that holds most of the organism's genes.

CROSS-POLLINATION:

The transfer of pollen from one plant to another.

CYTOPLASM:

The material inside a cell that is external to the nucleus.

DIPLOID:

A term for a cell that has the basic number of doubled chromosomes.

DNA:

Deoxyribonucleic acid, a molecule in all cells, and many viruses, that contains genetic codes for inheritance.

EGG CELL:

A female gamete.

ENZYME:

A protein material that speeds up chemical reactions in the bodies of plants and animals without itself taking part in or being consumed by those reactions.

FERTILIZATION:

The process of cellular fusion that takes place in sexual reproduction. The nucleus of a male reproductive cell, or gamete, fuses with the nucleus of a female gamete to produce a zygote.

GAMETE:

A reproductive cell—that is, a mature male or female germ cell that possesses a haploid set of chromosomes and is prepared to form a new diploid by undergoing fusion with a haploid gamete of the opposite sex. Sperm and egg cells are, respectively, male and female gametes.

GAMETOPHYTE:

In alternation of generations, a gametophyte is a plant that reproduces sexually.

GERM CELL:

One of two basic types of cells in a multicellular organism. In contrast to somatic or body cells, germ cells play a part in reproduction.

HAPLOID:

A term for a cell that has half the number of chromosomes that appear in a diploid or somatic cell.

MEIOSIS:

The process of cell division that produces haploid genetic material. Compare with mitosis.

MITOSIS:

A process of cell division that produces diploid cells, as in asexualreproduction. Compare with meiosis.

NUCLEUS:

The control center of a cell, where DNA is stored.

OVARY:

Female reproductive organ that contains the eggs.

OVULE:

Female haploid gametophyte of seed plants, which develops into a seed upon fertilization by a pollen grain.

PARTHENOGENESIS:

A type of reproduction that involves the development of a gamete without fertilization. In other words, a sex cell (usually female) is reproduced without actual intercourse between male and female.

POLLEN:

Male haploid gametophyte of seed plants (including angiosperms and gymnosperms), which unites with the ovule to form a seed. Pollen is a fine, powdery substance consisting of microscopic grains.

POLLINATION:

The transfer of pollen from the male reproductive organs to the female reproductive organs of a plant. Pollination precedes fertilization. See also cross-pollination.

REGENERATION:

A biological process among some lower animals whereby a severed body part is restored by the growth of a new one.

SEXUAL REPRODUCTION:

One of the two major varieties of reproduction (along with asexual reproduction). In contrast to asexual reproduction, which involves a single organism, sexual reproduction involves two. Sexual reproduction occurs when male and female gametes undergo fusion, a process known as fertilization, and produce cells that are genetically different from those of either parent.

SOMATIC CELL:

One of two basic types of cells in a multicellular organism. In contrast to germ cells, somatic cells (also known as body cells) are not involved in reproduction; rather, they make up the tissues, organs, and other parts of the organism.

SPERM CELL:

A male gamete.

SPOROPHYTE:

In alternation of generations, a sporophyte is a plant that reproduces asexually.

ZYGOTE:

A diploid cell formed by the fusion of two gametes.

Reproduction

BIBLIOGRAPHY

“Reproduction” in anthropology refers to the processes by which new social members are produced—specifically, the physiological processes of conception, pregnancy, birth, and child-raising. In its larger sense, reproduction encompasses the processes by which societies are reproduced for the future. The term is thus fraught with biological, cultural, and political meanings; power is a central focus in reproductive studies, as those who have the power to influence the process of reproduction can control both individual and large populations for better or for worse.

The maturation of the field of the anthropology of reproduction was marked by the publication of Conceiving the New World Order: The Global Politics of Reproduction (1995), edited by Faye Ginsburg and Rayna Rapp. This collection expanded the meaning of reproduction into the political arena and generated the interface of reproductive studies with wider issues in the politics of women’s health care. From a study of anti-abortion policies in Romania, to China’s one-child policy, to the displacement of thousands of women in India and Pakistan to “purify the national bodies” of both countries, the chapters in this volume called attention to the impact of national and global processes on everyday reproductive experience, most especially through the notion of “stratified reproduction,” which points to transnational reproductive inequalities based on gender, race, and class. In addition, Rapp’s long-term fieldwork on amniocentesis illustrates racial, class, and religious differences in how women make choices about this technology, and demonstrates the linguistic power of genetic counselors to influence these choices in favor of the culturally approved choice of abortion for genetically defective babies.

Since the 1990s, most anthropological studies of reproduction have focused on what have come to be called “the new reproductive technologies” (NRTs)—technologies designed to intervene in human reproduction. From the birth of the world’s first test-tube baby in 1978 to the cloning of a higher vertebrate from an adult cell in 1997, the rapid expansion of the NRTs in the latter half of the twentieth century dramatically redefined the parameters of biological reproduction. The NRTs include, among many others: birth control technologies such as intrauterine devices (IUDs) and the birth control pill; assisted conception technologies such as artificial insemination and in-vitro fertilization (IVF); screening technologies such as ultrasound, amniocentesis, and blood testing; reparative technologies such as fetal surgeries performed in utero; labor and birth technologies such as electronic fetal monitoring, synthetic hormones for labor induction and augmentation, and multiple types of anesthesia; and postnatal technologies such as infant surgeries and high-tech treatment of babies in neonatal intensive care units. All of these technologies are increasingly affected by developments in biotechnology, such as genetic engineering, which have major implications for the control and management of human fertility.

Like the obstetrical forceps developed by the Chamberlen brothers in the sixteenth century, the NRTs have double-edged implications for women and their offspring. While those early forceps did save the lives of babies who otherwise might have died, their overzealous and ill-informed application during childbirth by male midwives and obstetricians often left the mother and baby severely damaged. The NRTs have been equally problematic, often creating as many problems as they solve and causing as much damage as they repair. For example, maternal mortality as a result of ovarian hyperstimulation, and increased congenital abnormality because of multiple births, are but two examples of the downside of in-vitro fertilization (IVF).

Reproductive technology has affected every facet of the reproductive process, from preconception onward. To an extent, these developments respond to specific impediments to fertility: IVF, for example, was originally used to assist women with blocked ovarian tubes. Feminist critics, however, have rightly pointed to other, less woman-centered influences shaping the development of these technologies. For example, Robert Edwards, the research scientist who helped to develop IVF, was trained in embryology and foresaw tremendous research potential from the ability to manipulate the human embryo ex vivo. This potential was extensively exploited in the rapid expansion of human embryo experimentation in the 1980s and the 1990s.

The encounter between a largely male medical and scientific establishment and women’s reproductive capacity is very pointed in the context of IVF, which is often represented as being a response to the “desperate” desires of infertile women but can as readily be interpreted as a response to the irresistible scientific urge to “unveil” and indeed to redesign “the facts of life.” The tremendous value of early embryonic cells—both commercially and in terms of research—has made IVF an important source of human embryonic stem cells. This fact exists in uneasy tension with women’s demands for improved reproductive services. As in other historical periods, the neglect of women’s reproductive needs is most evident in terms of which kinds of services will be developed and prioritized.

While new embryo therapies are used to detect, and even to eliminate, genetic disease, other reproductive priorities remain devalued and underfunded. For example, while ever more sophisticated technologies are developed to deal with the complications of labor and birth, the normal physiological needs of laboring women remain understudied and unfulfilled. The scientific evidence that does exist supports simple technologies like eating and drinking during labor, woman-centered, supportive care, and upright positions for delivery as being of far more help to birthing women than high-tech machines. Nevertheless, the hegemonic global influence of what Davis-Floyd (2004) calls “the technocratic model of birth” has resulted in rapidly rising cesarean rates in many countries and has simultaneously precluded adoption of more humanistic and physiologic techniques for supporting normal birth. A growing body of anthropological literature reveals the systematic deconstruction of traditional birthing systems around the world. These systems are being replaced by biomedical care that disregards women’s individual needs in favor of standardized approaches (DeVries et al. 2001), and that, in the developing world, often suffers from such drastic underfunding that basic supplies, clean facilities, and sufficient numbers of trained caregivers are regularly unavailable (Allen 2002; Davis-Floyd and Sargent 1997; Feldman-Savelsberg 1999; Hunt 1999; Luckere and Jolly 2002; Ram and Jolly 1998; Van Hollen 2003).

Two major influences continue to shape the development of reproductive technology in ways that are not in women’s interests. One is the continuing, and indeed worsening, effects of global inequality that are borne most heavily by women and young children, especially infants. Adequate, or indeed any, access to basic contraceptive technology remains out of reach of the majority of the world’s female population (despite concerns about population growth, and largely as a result of U.S. anti-abortion policy). Consequently, resource-intensive and largely private fertility care is provided to a predominantly wealthy world elite. Meanwhile, enduring tragedies of high maternal and infant mortality from preventable causes such as malnutrition and lack of a clean water supply, inadequate access to safe abortion and contraceptives, and limited, nonexistent, or ineffective reproductive health care are the main issues affecting the majority of the world’s women. In sum, proper sanitation, adequate nutrition, improved vaccination programs, access to culturally appropriate forms of birth control, access to community midwives backed by adequate transport systems, and above all increased literacy and education rates among women remain the most important and lifesaving “reproductive technologies.”

At the other end of the spectrum, at the cutting edge of twenty-first-century medical science, is the resurgence of a new genetic essentialism. Reproductive technology is shifting its focus in the direction of germline gene therapies (therapies that can be genetically transmitted because they modify reproductive cells). Annexed to the project of mapping the human genome, reproductive science and medicine are increasingly aimed at both the elimination of genetic pathology and the effort to reengineer the genomes of humans and other life-forms. In addition to existing means of technologically assisting conception, the effort to alter human genealogy is the single most important influence on contemporary reproductive technologies. This effort is driven by enormously competitive economic forces and by an “if we can do it, we must do it” technocratic mentality, resulting in rapidly escalating and largely unregulated technological innovation.

While some commentators argue that reproductive technologies such as the freezing of eggs, cloning by nuclear transfer, germline gene therapy, and embryo biopsy will have a radical effect on gender roles and kinship definitions, the majority of evidence demonstrates a reverse effect: the restabilization of traditional and conservative family ideologies in the face of their potential disruption. At the same time, other influences, such as the lesbian and gay movement, the increase in transnational adoption, rising divorce rates, and greater economic independence for women, have proven more influential in the redefinition of family and parenthood. Consequently, although some uses of reproductive technology have created more parenting options, such as the use of artificial insemination by lesbians, the overwhelming pattern of access to NRTs is defined by the goal of enhancing conventional parenting arrangements by married, heterosexual, and middle-class couples.

Feminist concern about reproductive technologies in the twenty-first century will increasingly overlap with the criticisms of biotechnology and genetic engineering raised by environmentalists and the general public. Concern about genetically modified organisms in the food chain and in medical applications will increase, particularly as the human-animal border becomes ever more permeable. The extensive feminist literature on NRTs anticipates with great precision many of the profound social, ethical, and political concerns surrounding new forms of genetic and biological determinism arising out of the attempt to alter the human genome. In addition to the effort to redefine medical and scientific priorities in relation to women’s reproductive health worldwide, feminist anthropological scholarship will continue to insist upon the primacy of fully informed reproductive decision making, in its widest sense, as a fundamental component of human rights.

SEE ALSO Abortion; Abortion Rights; Anthropology; Birth Control; Childlessness; Demography; Fertility, Human; Genetic Testing; Limits of Growth; Malthusian Trap; Marriage; Multiple Births; Population Growth; Reproductive Rights; Sexual Orientation, Social and Economic Consequences; Women’s Movement

BIBLIOGRAPHY

Allen, Denise Roth. 2002. Managing Motherhood, Managing Risk: Fertility and Danger in West Central Tanzania. Ann Arbor: University of Michigan Press.

Davis-Floyd, Robbie. 2004. Birth as an American Rite of Passage, 2nd ed. Berkeley: University of California Press.

Davis-Floyd, Robbie, and Carolyn Sargent. 1997. Childbirth and Authoritative Knowledge: Cross-Cultural Perspectives. Berkeley: University of California Press.

Davis-Floyd, Robbie, and Joseph Dumit. 1998. Cyborg Babies: From Techno-Sex to Techno-Tots. New York: Routledge.

DeVries, Raymond, Edwin van Teijlingen, Sirpa Wrede, and Cecilia Benoit, eds. 2001. Birth by Design: Pregnancy, Maternity Care and Midwifery in North America and Europe. New York: Routledge.

Feldman-Savelsberg, Pamela. 1999. Plundered Kitchens, Empty Wombs: Threatened Reproduction and Identity in the Cameroon Grassfields. Ann Arbor: University of Michigan Press.

Franklin, Sarah, and Helene Ragoné. 1997. Reproducing Reproduction: Kinship, Power, and Technological Innovation. Philadelphia: University of Pennsylvania Press.

Ginsburg, Faye, and Rayna Rapp, eds. 1995. Conceiving the New World Order: The Global Politics of Reproduction. Berkeley: University of California Press.

Hunt, Nancy Rose. 1999. A Colonial Lexicon of Birth Ritual, Medicalization, and Mobility in the Congo. Durham, NC: Duke University Press.

Luckere, Vicki, and Margaret Jolly, eds. 2002. Birthing in the Pacific: Beyond Tradition and Modernity. Honolulu: University of Hawaii Press.

Ram, Kalpana, and Margaret Jolly. 1998. Maternities and Modernities: Colonial and Postcolonial Experiences in Asia and the Pacific. Cambridge, U.K., and New York: Cambridge University Press.

Taylor, Janelle, Linda Layne, and Danielle Wozniak, eds. 2004. Consuming Motherhood. New Brunswick, NJ: Rutgers University Press.

Van Hollen, Cecilia. 2003. Birth on the Threshold: Childbirth and Modernity in South India. Berkeley: University of California Press.

Robbie Davis-Floyd

Sarah Franklin