Male Reproductive Systems (marine mammals)


Studies of the reproductive biology of male marine mammals have not received the attention that has been focused on their female counterparts. In part this is due to the limited numbers of male marine mammals kept in captivity, but also to the difficulty of measuring the anatomical and physiological parameters of free-ranging males. This account focuses on the anatomy of male reproduction, with emphasis on features unique to the various marine mammal groups. Aspects of reproductive life history and behavior, such as mating systems, territoriality, and sociobiology, are covered elsewhere. The effects of environmental and pharmacological factors on reproduction are also briefly reviewed here.

I. Cetaceans

Genitalia are internal in whales, dolphins, and porpoises (Fig. 1); this contributes to hydrodynamic efficiency. There is no os penis (baculum). The penis is fibroelastic (Fig. 2), similar to that in artiodactyls, such as cows, pigs, and antelopes (Cetacea are included in the Artiodactyla, or Cetartiodactyla, by some taxonomists). It originates in two crura from the caudal part of the free pelvic bones or from the entire surface of these bones (Fig. 3). The two arms fuse into a long rope-like body, round or oval in cross section. In large rorquals it may be 2.5-3 m long and 25-30 cm in diameter. The distal part of the penis tapers smoothly to the tip and is covered with ordinary skin; this may be homologous with the glans penis of some terrestrial mammals. When retracted the penis rests in an S-shaped horizontal loop. Because enlargement through engorgement with blood is limited by the tough tunica albiginosa (modified skin covering) during arousal, this loop allows protrusion of the organ without its lengthening. A flat retractor penis muscle runs from its ligamental or rectal-wall origin to insert on the ventral surface of the penis; it serves to withdraw the penis back into the penile slit. The prostate is primitive among eutherian mammals, resembling that of marsupials and monotremes in consisting of diffuse urethral glands unlocalized to form a discrete prostrate gland.

The testes are intraabdominal (or cryptic) and mesial/ ventral in position, a condition known as secondary testicondy. This feature is thought to be synapomorphic in Cetacea but is shared with some marsupials. The position varies among the cetacean taxa, from nearly renal in some odontocetes to ventral in baleen whales. In Mesoplodon spp., the organs are sunk in recesses of the abdominal cavity connected to the main cavity by short vagioperitoneal canals. The organs are long and cylindrical with a smooth shiny white surface. Relative testis size varies widely among the cetacean groups, being greater in those species thought to engage in sperm competition, such as right whales (Eubalaena spp.), than in polygynous species such as the sperm whale (Physeter macrocephalus). Odontocetes in general have testes 7 to 25 times larger than would be predicted for “average” mammals of their size, ranging to 8% of body weight in the dusky dolphin (Lagenorhynchus ohscurus), as compared to 0.08% in humans. The largest mammalian testes known are found in right whales, weighing up to 900 kg in combination. Testicular activity (and size of some muscles associated with the penis) varies seasonally, and weight increases substantially with breeding season in at least some del-phinid odontocetes, e.g., the spinner dolphin (Stenella lon-girostris). In many cetacean species, the spermatic tubules (vasa differentia) are more highly convoluted than in most terrestrial mammals. A distal spiral valve exists in the blue whale (Balaenoptera musculus), and mucosal folds have been described in the pygmy sperm whale (Kogia breviceps).

The scrotum functions in terrestrial mammals in part to lower ambient temperature to ensure viability of the sperm. Loss of the scrotum in Cetacea in the interest of hydrodynamic efficiency thus introduces a new thermoregulatory problem. This has been addressed by localized cooling through a cardiovascular countercurrent mechanism. Blood cooled in superficial veins of the dorsal fin and flukes feeds directly into a deep venous plexus closely juxtaposed to a similar arterial plexus that supplies the testis. Thus heat is drawn into the venous blood from the arterial blood before it reaches the testis, cooling the testis to below body core temperature.

Cetacean male reproductive system.

Figure 1 Cetacean male reproductive system.

II. Pinnipeds and Other Carnivores

All pinnipeds, die polar bear (Ursus maritimus) and the sea otter (Enhydra lutris) possess a baculum, or penis bone, which is the ossified anterior end of the corpus cavernosuni of the penis. The baculum is largest in the walrus (Odobenus rosmarus) and smallest in otariid pinnipeds, or eared seals and sea lions. The distal shape varies widely among species and is more complex in phocids (true or earless seals) than in otariids. As most of the phocids are aquatic copulators, relatively large bacula may function in preventing water damage to sperm after copulation or to facilitate sperm competition in species where the females mates with more than one male. Bacular size may also be adaptively constrained by a large body size in terrestrial copulators due to the risk of bacular fracture. The penis is vascular, as in terrestrial carnivores (Fig. 4). In phocids, the baculum is surmounted by a fleshy claviforni glans. In otariids, it is cov ered by only a thin layer of epithelium. The prostate gland is bulky, weighing up to 760 g in the southern elephant seal (Mirounga leonina) and is similar in anatomy in all seals.

Phocid seals lack a scrotum; the testes are external to the abdominal muscles but covered by the posterior part of a superficial muscle. Otariid pinnipeds possess a scrotum, but in some species, e.g., the Antarctic fur seal (Arctocephalus gazella), the testes are usually withdrawn into the inguinal position and the scrotum is visible only as two areas of hairless skin; the testes descend into the scrotum only during the need to avoid hyperthermia. Seasonal changes in testis and epididymis size and function occur with breeding season in pinnipeds in which this has been examined (Fig. 5). The testes in the sea otter and polar bear are scrotal.

III. Sirenians

Sirenians do not possess a baculum. The penis is vascular and retracted when not engorged. The testes are abdominal. The prostate is lacking in the dugong (Dugong dugon) and is composed of erectile muscle tissue in the manatees (Trichechus spp.).

IV. Maturity and Seasonality

Testosterone is the main androgen in male mammals and stimulates spermatogenesis. Testosterone concentrations have been measured in many odontocetes and pinnipeds. In all species for which there are published data, testosterone concentrations increase around the time of sexual maturity, making it a useful diagnostic tool. A seasonal pattern of circulating testosterone concentrations exists with elevated concentrations during the breeding season (typically in spring, but a few species are autumnal or multiseasonal breeders). In species with a short, tightly synchronized breeding season, testosterone concentrations are increased for 1 to 3 months at the start of the season but decline to baseline levels after breeding ends. Seasonality is also apparent in most male marine mammals in increased size of the testes and accessory reproductive glands (even muscles in some cetaceans) and increased spermatogenesis. Increased size of the testes is due to an increased diameter of the seminiferous tubules and epididymes, resulting in increases in the volume of sperm. Spermatogenesis usually lags behind testosterone production, as production of testosterone by testicular Leydig cells is necessary for germ cell differentiation in the seminiferous tubules.

The erect fibroelastic penis of the gray whale can often be seen on the breeding grounds in Baja California.

Figure 2 The erect fibroelastic penis of the gray whale can often be seen on the breeding grounds in Baja California.

Pelvis and male genitals of bowhead whale (Balaena mysticetus) in ventral view (top of drawing is anterior). This figure shows the close relation between the internal hindlimb bones (pelvis, femur, and tibia), the rectum, and the penis.

Figure 3 Pelvis and male genitals of bowhead whale (Balaena mysticetus) in ventral view (top of drawing is anterior). This figure shows the close relation between the internal hindlimb bones (pelvis, femur, and tibia), the rectum, and the penis.

A few marine mammals, such as dugongs and sea otters, lack a distinct breeding season. A few older male drrgongs that were examined were found to be aspermic, suggesting long periods of sterility.

Male reproductice tract of an otarid in ventral view (top is anterior).

Figure 4 Male reproductice tract of an otarid in ventral view (top is anterior).

 Weight of nonspermiogenic testes of walrus in relation to age.

Figure 5 Weight of nonspermiogenic testes of walrus in relation to age.

During seasonal quiescence, spermatogenesis ceases, although the testes retain relatively large seminiferous tubules with spermatocytes present. Shrinkage of anterior pituitary cells that produce gonadotrophins is thought to be ultimately responsible for the seasonal testicular regression.

V. Effects of Environmental Factors

Some environmental factors simply cue physiological events, whereas others have the potential to hasten or disrupt the system. The three most important are photoperiod, nutrition, and social factors.

Seasonal reproduction requires that males have adequate numbers of viable sperm when the females enter estrus. Hence the spermatogenic cycle must be initiated months before breeding. Photoperiod is the most commonly cited environmental cue for synchronizing reproductive processes in both males and females; it appears to function months before the breeding season begins. The pineal gland is responsible for the neuroendocrine communication of photoperiod to the rest of the body. Melatonin secretion, which is activated during short photope-riods, acts to relay photoperiodic cues to the target organs. In many species, melatonin is inhibitory to the gonadotrophic-releasing hormones (GnRH) that stimulate testosterone production and spermatogenesis. Thus reproductive processes in most species are stimulated during increasing daylength (i.e., spring). Conversely, increased melatonin concentrations due to a decreased photoperiod lead to inactivation of the testes.

Both sea otters and sirenians lack a defined breeding season, and the Australian sea lion (Neophoca cinerea) has a nonan-nual, nonseasonal reproductive pattern. Spermatogenesis in these species may be continuous. The lack of correlation between testicular activity and season in the dugong may relate to the absence of a pineal gland. No published studies have accounted for the lack of a defined breeding season in sea otters.

There is little published information of nutritional effects on the reproductive biology of male marine mammals. A high plane of nutrition is known to advance the onset of puberty in females and could be expected to have the same effect in males. It is also safe to assume that the plane of nutrition of an individual male will affect its position in a dominance hierarchy. For species in which there can be severe natural impacts on food resources, adult males may have lower blubber thickness during years of poor feeding, resulting in reduced stamina during the breeding season. Although the functional or mechanistic nature of the nutrition-reproduction relationship remains unclear, it can safely be concluded that the measurement of body condition and its effects on various reproductive events, especially during natural environmental perturbations, will continue to be important areas of marine mammal research.

Physiology and the environment influence the development of mating systems by affecting the relative distribution and availability of males and females, thereby altering the reproductive success of an individual male. After sexual maturation, serum testosterone concentrations may vary independent of testis weight, indicating that social factors play a role in reproductive processes. It is not uncommon to find captive situations with cetaceans that are of the same age but at very different reproductive states (i.e., one or more males remain sexually immature much longer than the others). Changing the social structure in an enclosure will often stimulate puberty in those lagging behind in sexual development.

VI. Effects of Pharmacological Agents

The most common reason for prescribing pharmacological agents is to reduce fertility. The three species for which this has been needed in captivity are the common bottlenose dolphin (‘Tursiops truncatus), the California sea lion (Zalophus califor-niantis), and the harbor seal (Phoca vitulina). All of these can be prolific breeders in captivity, and the need regularly arises to control numbers in some facilities. Until recently, physical separation and contraception of females were the only practical methods. Now GnRH agonists and antiandrogens are being used, with varying success.

A second reason to prescribe pharmacological agents is to suppress aggression among males. The need to control behavior in the captive setting is obvious, especially with adult male bottlenose dolphins during the breeding season. It is less obvious but equally if not more important in the management of the Hawaiian monk seal (Monachus schatiinslandi), a declining species in which males attempt mass matings, usually with a breeding-aged female, sometimes to the point of killing her.

GnRH agonists work by stimulating the anterior pituitary to release GnRH, which stimulates the testes to produce testosterone and initiate spermatogenesis. Paradoxically, the pituitary quickly becomes refractory and ceases its production of GnRH, which inhibits the testes. Injections of GnRH agonists have been used with some success with harbor seals and effectively decrease circulating testosterone concentrations to prepubertal levels in Hawaiian monk seals. Antiandrogens have been tried unsuccessfully with bottlenose dolphins.

Marine top predators are likely targets for xenobiotic compounds that act eidier as estrogens or antiandrogens. The most common of these are the polychlorinated biphenyls (PCBs) and dichlorodiphyenyltrichloroethanes (DDTs). These compounds bioaccumulate up the food chain, making marine mammals highly susceptible to their biological effects. Male marine mammals continue to accumulate organochlorines throughout their lives, whereas females tend to reduce their body burden via transplacental transfer and lactation. The range of PCB concentrations reported for arctic marine mammals is highest in the walrus (Odobenus rosmams), although the absolute concentrations are highest in polar bears. The effects of organochlorines on male reproductive physiology have not been well studied, as most research has focused on females. The known effects are pathologies related to structural changes and thickening of tubules in organs such as the kidneys, adrenals, and reproductive tract. The most striking possible example has been the occurrence of pseudoher-maphroditic polar bears with a normal vaginal opening, a small penis with baculum, and no Y chromosome. The syndrome is hypothesized to be due to either excessive androgen secretion by the mother or endocrine disruption from environmental pollutants. The impacts of all the detected pathologies are unknown. However, there are widespread reports that xenobiotic compounds are also strongly immunosuppressive, rendering contaminated animals more vulnerable to bacterial and viral infections. Experimental studies using minks (mustelids such as the sea otter) indicate that the enzymatic pathways that metabolize steroids are disrupted, but the detailed biosynthetic pathways of the or-ganismal response have not been elucidated.

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