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Functional morphology of venous structures associated with the male and female reproductive systems in Florida manatees (Trichechus manatus latirostris)†
Version of Record online: 30 OCT 2001
Published 2001 Wiley-Liss, Inc.
The Anatomical Record
Volume 264, Issue 4, pages 339–347, 1 December 2001
How to Cite
Rommel, S. A., Pabst, D. A. and McLellan, W. A. (2001), Functional morphology of venous structures associated with the male and female reproductive systems in Florida manatees (Trichechus manatus latirostris). Anat. Rec., 264: 339–347. doi: 10.1002/ar.10022
This article is a US Government work and, as such, is in the public domain in the United States of America.
- Issue online: 30 OCT 2001
- Version of Record online: 30 OCT 2001
- Manuscript Accepted: 25 AUG 2001
- Manuscript Received: 31 JAN 2001
- thermo- regulation
The reproductive organs of Florida manatees (Trichechus manatus latirostris) are surrounded by thermogenic locomotory muscles and insulating fat. Manatees are reported to maintain core body temperatures of 35.6°–36.4° C, temperatures known to interfere with production and maturation of viable sperm in terrestrial mammals. We describe two novel venous plexuses associated with the manatee epididymis. Each epididymis is located in a hypogastric fossa at the caudolateral extremity of the abdominal cavity. Each hypogastric fossa is lined by an inguinal venous plexus that receives cooled blood from a superficial thoracocaudal plexus. We conclude that male manatees may prevent hyperthermic insult to their reproductive tissues by feeding cooled superficial blood to venous plexuses deep within their bodies. Female manatees also possess hypogastric fossae and venous structures similar to those found in male manatees. The ovaries, uterine tubes, and distal tips of the uterine horns are located in the hypogastric fossae. We suggest that the thermovascular structures we describe also prevent hypothermic insult to female manatee reproductive tissues. The venous structures in manatees are functionally similar to structures associated with reproductive thermoregulation in cetaceans and phocid seals. Thus, these thermovascular structures appear to be convergent morphological adaptations that occur in three clades of diving mammals with independent evolutionary histories. Anat Rec 264:339–347, 2001. Published 2001 Wiley-Liss, Inc.
Manatees are large, slow, herbivorous marine mammals. Although they have relatively low metabolic rates (Galivan and Best, 1980; Irvine, 1983; Scholander and Irving, 1941), both their large body size and extensive countercurrent heat exchange systems (Scholander, 1958) permit them to maintain relatively high (35.6°–36.4° C) body core temperatures (Galivan et al., 1983; Irvine, 1983). Most mammalian tissues tolerate limited fluctuations in temperature, and some tissues, such as muscle, perform better at higher temperatures. However, mammalian reproductive tissues are particularly susceptible to hyperthermic insult.
In terrestrial mammals, production and storage of viable sperm appear to require a relatively narrow range of temperatures. Temperatures of 35°–38° C, which are common mammalian core temperatures, are reported to inhibit spermatogenesis (Blumberg and Moltz, 1988; Cossins and Bowler, 1987; VanDemark and Free, 1970). The scrotal position of the testes and epididymides (singular, epididymis) in many mammals compensates for this temperature sensitivity. The skin of the scrotum is well vascularized, has an abundance of sweat glands, and is highly innervated with temperature receptors (Evans, 1993; Guyton, 1976). Muscles in the scrotal wall involuntarily contract and relax in response to cold and hot temperatures, respectively. The exposed surface area of the scrotum provides a thermal window through which heat may be transferred to the environment to help regulate temperature of reproductive tissues. Because manatees have intra-abdominal testes and epididymides (Murie, 1872), high core temperatures may pose a thermal threat to spermatogenesis and sperm maturation.
Pregnancy may increase the maternal metabolic rate by 20%–40% (Power et al., 1984). Heat associated with fetal growth must be transferred from the fetus to the mother to prevent elevated fetal temperature and to avoid hyperthermic insult (Power, 1989). In terrestrial mammals, about 85% of the fetal metabolic heat is transferred by convection via the maternal circulatory system. The remaining 15% of the fetal metabolic heat is transferred by conduction across the uterine wall and through the abdominal wall (the abdominal wall thermal window) to the environment (reviewed in Rommel et al. (1993)). Additionally, because the primary locomotory muscles of terrestrial mammals are appendicular, much of the muscle heat of locomotion is transferred to the environment rather than directed into the body cavities. This is not the case for manatees because their locomotory muscles are axial and thus surround the abdominal and pelvic cavities; additionally, these muscles are insulated by thick layers of fat.
We have previously shown that cetaceans and phocid seals possess vascular structures to regulate the temperatures of their reproductive organs despite their positions deep within the body (Rommel et al., 1992, 1993, 1995). Our goal in this study was to investigate the anatomy of Florida manatees (Trichechus manatus latirostris) to determine whether these marine mammals possess vascular structures similar to those found in cetaceans and phocid seals.
MATERIALS AND METHODS
We used nine Florida manatee carcasses (five male, four female) necropsied by the Florida Fish and Wildlife Conservation Commission's manatee salvage program at the Marine Mammal Pathobiology Lab in St. Petersburg (Table 1). Individuals ranging in life history stage from perinatal to adult were investigated. Necropsies were performed with the carcass dorsally recumbent (Fig. 1). The ventral skin, fat, and abdominal muscles were removed slightly ventral to the distal tips of the ribs to expose the abdominal organs (Bonde et al., 1983; Rommel and Reynolds, 2000).
|Animal ID||Total body length (cm)||Age (yr)||Sex|
Each hypogastric fossa (Murie, 1872) can be identified as an abrupt reduction in thickness of the body wall at or near the distal tips of the last two or three ribs (Fig. 1). To determine how this feature influences the physical characteristics of the body wall, we measured body-wall thicknesses, excluding skin (epidermis and dermis), to the nearest mm by placing a ruler on the cut surface of the body wall.
We injected colored latex into the veins of the caudal abdomen by passing a catheter from one of the caudal venae cavae into the veins radiating laterally from the median (valves are rare in manatee veins). Arteries were injected via the aorta. Veins and arteries were identified by dissection, photographed, and drawn to record size, shape, and position (Rommel et al., 1992, 1993, 1995).
All illustrations were created using FastCAD (Evolution Computing Inc., Tempe, AZ).
The manatee's intra-abdominal testes lie on the ventral aspects of the hemidiaphragms (as described in Rommel and Reynolds (2000)) and are positioned on the caudolateral margins of the kidneys (Fig. 1). The epididymides originate along the craniolateral margins of the testes. The tails of the epididymides extend caudolaterally and slightly ventral to the testes and are positioned in the hypogastric fossae, shallow diverticulae of the abdomen between the last two or three ribs (Murie, 1872; Rommel and Reynolds, 2000). In female manatees, the distal uterine horns, uterine tubes, and ovaries are positioned caudolateral to the kidneys in the hypogastric fossae (Fig. 1).
The body-wall thickness decreases dramatically in the region of the hypogastric fossae (Fig. 1); these recesses in the body wall formed by an abrupt change in thickness of intercostal and abdominal-wall muscle and connective tissues. Thus, hypogastric fossae result from a reduction of body-wall thickness by as much as three to four times (6–8 cm in the regions just cranial to the fossae vs. 1.5–2 cm at the lateral margins of the fossae).
The dorsal roof of each hypogastric fossa is lined with two relatively flat, bilaterally paired, vascular plexuses; one of these plexuses is arteriovenous and consists of relatively small-diameter vessels, and the other plexus consists of relatively large-diameter veins. The dorsal-most layer is the (arteriovenous) iliac vascular bundle1 (Fig. 2) described, in part, by Fawcett (1942) and Murie (1872). This vascular plexus consists of triads (Fawcett, 1942) of one small-diameter artery and a juxtaposed pair of veins; these vessels are approximately 0.75 mm in diameter. Positioned on the ventral aspect of the iliac vascular bundle is another plexus called the inguinal venous plexus. This plexus is formed by anastomoses between relatively large (3–6 mm in diameter) veins. These veins extend from the dorsolateral margins of the hypogastric fossa (Fig. 2, arrows) to the ipsilateral vena cava. Additionally, a few of the large veins of the inguinal venous plexus anastomose with the smaller-diameter veins of the iliac vascular bundle. Occasionally, a few triads of the iliac vascular bundle course ventral to, rather than dorsal to, the inguinal plexus. Unlike most other veins in this region, though, the veins of the inguinal venous plexus are not associated with parallel arteries.
Each inguinal venous plexus is supplied by a fan-shaped array of veins that drains toward the last two or three ribs. This fan-shaped venous plexus is immediately deep to the dermis on the dorsolateral aspect of the abdomen or flank (Fig. 3). The veins at the vertex of each fan pass through the body wall at the level of the hypogastric fossa and feed the lateral margins of the ipsilateral inguinal venous plexus (see arrows, Figs. 2 and 4). We have named these vascular structures the superficial thoracocaudal plexuses because they are subdermal and extend approximately from the level of the 13th thoracic vertebra to the 5th caudal vertebra (typically, manatees only have a single lumbar vertebra; Fig. 1). Cooled blood, which drains from this superficial plexus, enters the body at the lateral margins of the hypogastric fossae and feeds the inguinal venous plexus.
The tails of manatee epididymides are distant from the testes,2 a condition typical of mammals with intra-abdominal testes (Bedford, 1977). The tails of manatee epididymides are located in the hypogastric fossae, relatively superficial diverticulae of the abdominal cavity that are overlaid by the inguinal venous plexuses. The hypogastric fossae extend the abdominal cavity close to the dermis, where cooled venous blood feeding the inguinal plexuses returns from the periphery via the superficial thoracocaudal plexuses. This geometry suggests that the epididymides can be cooled by heat transfer to the inguinal venous plexus—i.e., that cooled venous blood returning from the periphery could provide direct, local cooling of specific deep body tissues.
One could argue that manatees would not be subject to hyperthermic insult but must cope only with the potential for hypothermic insults because they are aquatic mammals with very low metabolic rates. Although manatees do possess mechanisms to prevent excessive heat loss (Scholander, 1958), their testes and epididymides are deep within their bodies and their core temperatures are in the range known to inhibit spermatogenesis (Jameson, 1988; Setchell, 1978).
In most mammals, the question of whether or not both the testes and the epididymides need to be kept at below-core temperatures cannot be addressed easily because the two structures cannot be separated without major surgical effort. Bedford (1977) strongly argued that it is the epididymides and not the testes that require relatively low temperatures, although at that time little information on the reproductive anatomy and physiology of marine mammals was available. Interestingly, Carrick and Setchell (1977) hypothesized that the reproductive tissues in dolphins and seals must be cooled, but they argued for testicular, rather than epididymal, cooling. The gross vascular anatomy of the Florida manatee suggests that only the epididymides are cooled in this species. Physiological observations, similar to those made on phocid seals and dolphins (Pabst et al., 1995; Rommel et al., 1994, 1998) may shed light on this question. Additionally, reexamination of the placement of the epididymides, as well as the testis, in relation to the thermovascular adaptations in seals and dolphins may also help address this question.
The need for reproductive cooling in diving female marine mammals has been reviewed in Pabst et al. (1999). Interestingly, we have found similar vascular structures in both male and female manatees (Fig. 3). The ovaries, uterine tubes, and distal uterine horns are located in the hypogastric fossae of female manatees. Thus, the inguinal venous plexuses have the potential to help thermoregulate these female reproductive tissues. Unfortunately, the large amount of insulating fat in pregnant female manatees almost assures that these carcasses are too badly decomposed for us to accurately define the vascular anatomy of their reproductive organs. Vascular structures that could help female manatees prevent an increase in fetal temperature would be beneficial.3 We have shown that the thermovascular adaptations found in male dolphins and some of the vascular adaptations found in male seals are also found in females (Rommel et al., 1993, 1995). Further work is necessary before we can more completely describe this portion of the vascular system in female manatees.
Our previous work describes vascular adaptations that can dramatically redistribute the blood in response to physiological demands in dolphins and seals (reviewed in Pabst et al. (1999) and Rommel et al. (1998)). These adaptations are modifications that feed superficially cooled venous blood to a specific region for use in local thermoregulation of reproductive structures—before it is mixed with the central circulation. In dolphins, cooled venous blood traveling through superficial veins can be fed to the lumbocaudal venous plexus4 that is juxtaposed to an spermatic arterial plexus supplying the testis (Rommel et al., 1992). Countercurrent heat exchange between the juxtaposed plexuses can cool the arterial blood reaching the testis and epididymis. Thus, cooled venous blood indirectly cools the dolphin's reproductive structures. In contrast, phocid seals have cooled venous blood returning from the superficial surfaces of the hind flippers, which is delivered to an inguinal venous plexus that lies on the deep surface of their para-abdominal testes. Thus, venous blood directly cools the testes and epididymides in these marine mammals (Blix et al., 1978; Rommel et al., 1995).
The thermovascular adaptations we describe for manatees are functionally similar to those we have previously described for dolphins and phocid seals. We believe these similarities can be identified as convergences across these three diving mammalian clades with independent evolutionary histories. Our observations suggest that some marine mammals require connections between superficial vascular beds and deep vascular plexuses that surround or are near reproductive structures, that function as safety devices to prevent hyperthermic conditions at the testes or epididymides in ascrotal diving mammals.
The superficial thoracocaudal plexuses in the manatee are similar in position and extent to the dorsal-most superficial branches of the deep circumflex iliac veins found in terrestrial mammals (Evans, 1993; Schummer et al., 1981; Fig. 5A). Additionally, the superficial thoracocaudal veins of the manatee feed the veins of the inguinal venous plexus (internal plexus) that subsequently anastomose into a single vessel that joins the vena cava near the first lumbar vertebra. This position in manatees is similar to where the deep circumflex iliac vein joins the vena cava in terrestrial mammals (Fig. 5B).
Interestingly, the superficial veins that feed the manatee inguinal venous plexus are also similar in position to the superficial veins that feed the lumbocaudal venous plexus (internal plexus) in adult dolphins (Rommel et al., 1992, 1993; Fig. 5C) and the superficial lumbocaudal veins in a cleared and stained harbor porpoise (Phocoena phocoena) fetus (Fisher and Harrison, 1970). Unlike the manatee, the internal plexus of the cetaceans is also supplied by veins from the caudal peduncle and flukes. Based upon positional data, it appears that abdominal branches of the deep circumflex iliac vein of terrestrial mammals could be homologous to the dorsal portion of the abdominal wall plexus (internal plexus) of phocid seals (Rommel et al., 1995; Fig. 5C). The internal plexus of the seal is supplied by cooled blood from the hind flippers, which have been shown to be a major site of heat loss (Galivan and Ronald, 1979). It is not yet known whether superficial branches of the deep circumflex iliac vein in the seal feed into the plexuses that cool the reproductive organs.
Thus, we suggest that the superficial thoracocaudal plexus in manatees is homologous to the dorsal-most elements of the superficial branches of the deep circumflex iliac vein in terrestrial mammals. We also suggest that the inguinal venous plexus (internal plexus) is a modification of the abdominal portion of the deep circumflex iliac vein. In both the cetaceans and the phocid seals, the internal plexuses, at least in part, appear to be homologous to the internal plexus of the manatee.
Clearly, vascular adaptations in diving mammals (reviewed in Elsner (1999)) have evolved for more than conservation of oxygen reserves during diving—they are also elegant adaptations for the distribution, conservation, and dissipation of heat energy in animals that have widely varying thermal requirements.
We thank Meghan Bolen, Judy Leiby, Tom Pitchford, and Dr. James Quinn at the Florida Marine Research Institute, Dr. John Reynolds at Eckerd College, Dr. Joy Reidenberg at Mt. Sinai School of Medicine, Dr. Alastair Watson at Oklahoma State University, and Jennifer Dearolf and Dr. Howard Evans at Cornell University for their helpful comments on the manuscript. We thank Llyn French for help with Figure 3.
Murie (1872) generally referred to this structure as the “lumbar or hypogastric rete”; he was more specific in his subdivisions of it, labeling the cranial portion as the “uterine plexus” for his female illustrations and the caudal portion as the “rete mirabile of the loins and pelvo-generative region” for his male illustrations. Fawcett (1942) referred to this structure as the iliac plexus; he made it quite clear that “rete” should not be used in this context. Instead, he adopted the term “vascular bundle,” which was in use for describing a particular kind of vascular plexus. A vascular bundle is defined by an immediate branching from the parent stem into a large number of small, equal-caliber arteries that run parallel for significant distances without further divisions (Fawcett, 1942). In the typical vascular tree, branching usually results in an increase in the number of distal elements, each growing smaller and their branching more frequent; in contrast, vascular bundles resemble a broom. To be consistent and to minimize confusion, we refer to the intercostal and iliac plexuses as vascular bundles. In contrast, we keep the more general term “plexus” for two other vascular structures we describe—the iliac venous plexus and the superficial thoracocaudal plexus. A plexus is defined here as a network of interlacing or anastomosing vessels.
In contrast, the juxtaposition of the extratesticular sperm store (i.e., the epididymis) and the testis is the result of testicular descent (White et al., 1977).
It is possible that evaporative cooling in the lungs will influence temperatures of some parts of the manatees' reproductive systems; however, more research is needed to address this suggestion.
Note that the thoracolumbar region of the dolphin and seals is about 50% ribs and 50% lumbars, whereas in manatees it is almost all ribs. In seals, the hind limb is also part of the abdominal wall. Thus, the caudal abdomen of the dolphin is bordered by muscle, that of the manatee by ribs, and that of the seal by the hind limb.
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