A brief look at the family Leporidae (hares and rabbits)

Keywords: Leporidae, Oryctolagus, Lepus, Sylvilagus, anatomy, physiology, reproduction, uterus, ovaries, tract, vagina, rabbits, hares

A fascinating group of mammals, some familiar to veterinary and animal science, others not. Note that  rabbits and hares belong to the order Lagomorpha, of which there are two families: Leporidae and Ochotonidae (pikas, mouse hares, or conies)

As mentioned in the LORI entry on semen collection in rabbits, rabbit farming is underdeveloped in North America compared with Europe, Asia and South America. Therefore rabbits are superficially addressed in most animal science and veterinary curricula in North America. However, rabbits deserve attention as important sources of meat and fiber and their unique value as subjects for scientific study (See: Foote and Carney, 2000). 

Vocabulary:

Lagamorph: A member of the order Lagamorpha

Leporid: A member of the family Leporidae, comprising the rabbits and hares.

Kindling: The name given to parturition in rabbits and hares.

Kits: Perinatal rabbits and hares (the term "pup" is reserved for rats, mice and dogs).

Doe: Adult female Leporid

Buck: Adult male Leporid.

Nests and burrows: Hares (always wild) live in nests, above ground. Wild rabbits such as Cottontails live in burrows.

Introductory notes: Rabbits and hares are all members of the family Leporidae.  This family includes the domestic rabbits (Oryctolagus cuniculus), hares (many Lepus spp) and brush rabbits (many Sylvilagus spp). They share similar reproductive characteristics but as donkeys are to horses, they are also distinctively different. For example, hares and brush rabbits have 48 chromosome and precocious neonates with open eyes, able to ambulate efficiently. By contrast, rabbits have 44 chromosomes and altricial young, blind, hairless and unable to ambulate. Their eyes open at about 10 days postpartum. In the course of this entry, the author will entertain other differences between hares and rabbits.

Figure 1. The reproductive tract of a Snowshoe hare (Lepus Americanus) that was approximately 14 days pregnant. The ~20 day old fetus at left is that of a domestic rabbit (Oryctolagus cuniculus).  The 14 day pregnancy shows the bulbous embryo-placental units typical of rabbits and hares. Note too, that the ovaries are not covered by ovarian bursae. Corpora lutea of pregnancy are visible within the ovaries. Finally, note the double cervix (inset at right); typical for all Leporids (as well as rats and mice). The vagina (not shown) is about 10 to 12 cm long. Image size: 1344 x 831 px

A crash course on rabbit and hare reproduction:  1. Puberty occurs between 4 and 7 months of age; later in large rabbit breeds such as the Flemish White.  2. Although commercial rabbits breed throughout the year, hares and wild rabbits (Sylvilagus spp; Cottontails) are like cats. i.e. they respond to increasing day length and breed mostly during spring and early summer.  3. Like cats, rabbits and hares do not have discrete estrous cycles. Instead, as reflected by vaginal cytology, follicle waves mature every 4 to 5 days (~ 7 days in hares).  4. Although spontaneous ovulation can occur, ovulation is generally induced by copulation (mounting in the absence of intromission is also thought to be important). Ovulation occurs about 10 hours post copulation. GnRH treatment is essential for satisfactory pregnancy rates when AI is used. 5. Pregnancy diagnosis is accurate at 10 to 14 days post-breeding using transabdominal palpation. Optimal first service conception rates should be greater than 70%  i.e. 70% of does should be pregnant after a single breeding. 6. Gestation is longer in hares than rabbits; about 42 days vs. 30 days. This explains why hares have precocious young and rabbits, altricial young.  7. Parturition occurs in the morning. Anterior, posterior and even breech presentations are normal. Usually kindling is complete in less than 30 minutes but occasionally, kits (like kittens) may be born hours or even one or two days apart. Kits are usually born separated from their umbilical cords but maternal biting of cords has been described. 8. Cannibalism (infanticide) is fairly common in young rabbits, especially under stressful conditions. 9. Rabbits have an average of six to 10 kits per litter. Does have 8 to 10 mammary glands and nurse their kits once per day. 10. Pseudopregnancy occurs after sterile mating in both hares and rabbits but does not normally occur in the absence of mating as in dogs and cats. Like pregnancy itself, pseudopregnancy is slightly longer in hares than rabbits i.e. 24 days vs. 17 days. As is sometimes seen in bitches, nesting behavior will occur during pseudopregnancy. In the case of Leporids this involves pulling of abdominal hairs and gathering of straw etc.  11. Pregnancies with one or two fetuses may be significantly longer than otherwise (as is the situation with cats and dogs). One can usually diagnose retained fetuses by palpation. Cesarean section may be required in such cases. 12. Rabbits can have fertile copulation soon after birth and become pregnant in under a week after parturition (kindling ). This is possible because rabbits have active ovaries at the time of kindling and uterine involution is largely complete within 48 hours of parturition. Consider that other domestic animals have ovaries devoid of significant follicle growth at parturition. 13. Conception soon after parturition is remarkable in light of the intimate placentation in Leporids. It is hemochorial i.e. more intimate than any other domestic animal (see figure 2). In commercial operations, does are re-bred between 2 and 6 weeks after kindling. This will provide 4 to 6 litters per year. 14. Weaning in commercial operations usually occurs at approximately 6 weeks, when the doe has already been pregnant for some time. 15. Rabbits are usually processed for meat production at 3 to 4 months of age and breeding stock  rabbits are seldom kept for longer than 3 to 4 years in commercial units.

Figure 2. Placentation typical of a rabbit or hare; a modified amalgum from several sources. Placentation is bi-discoidal then discoidal and intimate, developing mesometrially (although anti-mesometrial in early gestation). Placentation is hemochorial (also referred to as hemobichorial) with giant cells forming in the endometrium, similar to equine eCG-producing cells. Note the large exocelom, similar to that in carnivores. Image size: 896 x 733 px

Selected references:

Benirschke. K. Comparative placentation. http://placentation.ucsd.edu/rabbits.htm

Chavatte-Palmer P. et al. 2008. In utero characterization of fetal growth by ultrasound scanning in the rabbit. Theriogenology. y 69: 859–869

Dickie, E. 2011.Dystocia in a rabbit (Oryctolagus cuniculus). Can. Vet. J. 52: 80-83.

Boumahdi, Z. et al. 20009  Behavior at birth and anatomo-histological changes studies of uteri and ovaries in the post partum phase in rabbits. European J. of Scientific Res. 34: 474-484

Foote, R.H. and Carney E.W. 2000.The rabbit as a model for reproductive and developmental toxicity studies 

Foxcraft, G.R. and Hasnain, H. 1973. Effects of suckling and time to mating after parturition on reproduction in the domestic rabbit. J. Reprod. Fert. 33:367-377

International rabbit reproduction group. 2005.Guideline for the handling of rabbit bucks and semen. World rabbit.Sci. 13:71-91

Roellig, K. et al 2010. Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season. Nat Commun. 2010 Sep; 1(6): 1–7.

Torres, S. et al. 1977. Fertility factors in lactating rabbits mated 24 hours and 25 days after parturition. Ann. biol. anim. Biochem. Biophysics. 17:63-69

Weisbroth et al Eds. 2013. The Biology of the Laboratory Rabbit. ISBN 1483270319

Zebra mare reproductive tract

Keywords: Equus, chapmani, Chapmans, Zebra, Equus quagga chapmani, uterus, ovaries

Note: Both zebra and zebras are widely accepted words as plurals for the singular form "zebra". The author has chose to use the term zebras for the plural form in this entry.

Although some disagreement exists on the taxonomy of Zebras there appear to be seven extant species of Zebras and a few subspecies within some of those species. Equus grevyi is the largest zebra and has a diploid chromosome number of 46. Plains zebras such as the Equus quagga chapmani featured in this LORI entry, have 44 chromosomes while Mountain zebras (Equus zebra zebra) have 32. Some zebras have finer striping than others, some differ in dentition, conformation and so on.

The reproductive biology and anatomy of horses and zebras are remarkably similar. 

Below, see an image of the reproductive tract of a mature (exact age unknown) Equus quagga chapmani. The parity of the mare was also unknown but examination of the tract suggested that she had been pregnant at least once. In this image, the cervix appears to be shorter than that of a domestic mare. However, detailed examinations of the reproductive tracts of 310 Equus quagga showed an average length of 4.9 cm; similar to than of domestic mares.

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The image below accentuates the remarkable similarity between this animal and domestic mares with regard to the vestibulovaginal seal (arrows) i.e. the remnants of a hymen.

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Again, below, the ovaries and adnexa of a Chapman's zebra are remarkably similar to those structures in domestic mares in both size and architecture. The author's fingertips have been inserted into the ovarian bursa.

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This mare was examined in early January (in the northern hemisphere) when most domestic mares would have been in winter anestrus. This probably explains the lack of activity in her ovaries. Multiple ovulations are rare in zebras (twins being virtually unknown) but secondary ovulations do occur during pregnancy and accessory corpora lutea form as is the case in domestic mares.

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The author was struck by the similarity of the clitoris in this zebra and those in domestic mares. There was also at least one well developed clitoral sinus within dorsal surface of the clitoris. This led the authhor to contemplate the potential for Taylorella equigenitals or or other Taylorella species to cause reproductive failure in zebras.

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General commentary: Like Equus caballus, Zebras are seasonal breeders, responding to increased day length. However, there appears to a remarkable effect of increased energy availability in modulating that response to day length. From numerous observation by many authors, zebra mares appear to have standing estrous periods that are similar in duration to those in domestic mares. Their gestation is however, substantially longer. Although gestation as short as 336 days has been recorded, most zebras foal after gestations of approximately 370 days. Normal gestation can be as long as 425 days. Progesterone, eCG and estrogen profiles are similar to those in mares and certainly, urine estrogens shed during urination in sand bedding can be used to diagnose pregnancy. Similarly, assays for eCG in urine may hold promise for pregnancy diagnosis. Indeed, the latter has shown to be the case in domestic mares. Mammary development, foaling, "foal heat" and neonatal physiology in zebras are similar to the same features in domestic horses but weaning of zebra foals only occurs after 10 to 12 months. Interestingly, zebra of all stripes (!) can interbreed with domestic horse and donkeys and produce normal, live offspring. In many cases, those hybrid offspring are fertile as well.

Selected references:

Allen, W.R. and Short, R.V. 1997. Interspecific and extraspecific pregnancies in

equids: Anything Goes. J.Heredity 8:384-392

Asa, C.S. et al. 2001. Patterns of excretion of fecal estradiol and progesterone and urinary chorionic gonadotropin in Grevy’s zebras (Equus grevyi): Ovulatory cycles and pregnancy

Zoo Biology. 20: 185–195

Smuts, G.L. 1976. Reproduction in the zebra mare Equus burchelli antiquorum from the Kruger National Park Koedoe.19: 89-132

The reproductive tract of a pilot whale Globicephalus melas.

Keywords: cetacean, whale, pilot, tract

This reproductive tract was obtained from a dead, beached long finned pilot whale (Globicephalus melas) found in New Brunswick in November 2013. The time of death was unknown but postmortem changes were minimal.

The vagina and vulva were absent but the reproductive tract was otherwise complete. The gross appearance of the reproductive tract showed many similarities between this species and our domestic animals; specifically cattle and horses. The uterus was most like that of a mare, being approximately T-shaped with a long uterine body. There was a small inter-cornual ligament and two long horns. Proportionally, these horns were almost twice as long as those in a mare or cow, presumably to accommodate an elongated calf that weighs approximately 100 kg at birth.

The uterus was suspended by a mesometrium that did not contain a obvious dominant uterine artery such as that seen in mares in cows.

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As mentioned, the vulva and vagina were absent. However, the cervix had been retained and was a source of fascination for this author. This macroscopic image of the cervix  shows large numbers of folds and complex folding within folds, giving the mucosa and almost feather-like appearance.

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The reader is encouraged to click on this image to appreciate the nature of those folds. It is tempting to suggest that the structure forms a sperm reservoir in the living animal. Similar folding in other species, together with the cervical mucus has certainly been proposed as reservoirs in other species. The reader is encouraged to click on this image to fully appreciate this anatomy.

The cervix itself was more reminiscent of that of a mare than a cow, having no interlocking transverse ridges but instead, a series of longitudinal folds leading to the uterus. Interestingly, the cervix became narrow in its most cranial portion as shown by the light black arrows in the image below. In both of the images in this amalgam, an accumulation of tenacious mucus can be seen in the cranial portion of the cervix. This has been seen by the author in other marine mammals (the grey seal and a dolphin). It is possible that this cervical mucus play a role in protecting the contents of the uterus under conditions of high water pressure in these deep diving animals.

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The endometrium was very similar in gross appearance to that of the mare with no evidence of multiplex (ruminant-type) placentation. This suggests that the Pilot whale has diffuse placentation like that of the mare. The bifurcation of the uterus occurs about 10 to 12 cm cranial to the internal os of the cervix (see yellow arrows) again, more similar to the uterus of the mare than that of a cow.

On the other hand, the ovaries as seen below, are reminiscent of those of a cow in both scale and function.

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They were approximately 5 x 2.5 cm (left) and 8 x 2.5 cm (right). Although a fairly robust tunica albuginea was present, ovulation appeared to occur through the surface of the ovaries. The crown of a corpus luteum (yellow arrow) with a small depression in its center was seen in the right ovary.

On close examination, there were a total of 7 or 8 corpora albicanti in both ovaries combined. Some of these were very small and presumed to be older than others. The age of marine mammals is sometimes determined by the number of corpora albicanti in the ovaries but several hundred sections of each ovary must be examined to determine the number of corpora albicanti with any accuracy. Also, the incidence twin ovulations, lactational anestrus, break-through ovulation during suckling (see below) and nutritional effects cannot be discounted. Therefore growth rings in the teeth (see below) are usually used to age cetaceans instead.

Literature reviewed in Cetacean Societies: Field Studies of Dolphins and Whales (Ed.Janet Mann ISBN-13: 978-0226503417) suggests that toothed whales (Odontocetes, such as this pilot whale), unlike the baleen whales (Mysticetes) do not generally ovulate or conceive in early lactation. As mentioned, this whale was lactating at the time of his death and one of the whales found together with the female was presumed to be her calf. Because whales may suckle for many years, it is unlikely that this female had ovulated recently; consistent with the absence of a corpus luteum in either ovary.

To one who is used to the appearance of ovarian structures in domestic animals, the dominance of the corpora albicanti is remarkable because corpora albicanti are usually difficult to see in domestic animals except for a period of days or weeks after ovulation. In many marine mammals however, corpora albicanti persist for years, probably because of their remarkable fibrotic structure. Although the term corpora albicanti or corpus albicans is used in our domestic animals, true "white bodies" (as the Latin name suggests) is not nearly as obvious as in marine mammals.

This image shows the remarkable fibrosis present in one of the corpora albicanti from this whale.

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The histologic appearance of the corpora albicanti (CA) are shown at upper and lower left in the composite image below. The degree of fibrosis is obvious. Also of interest in this image are the following:

• The collapsed theca interna of the Graafian follicle adjacent to the CA in the upper left image. The resemblance between these follicles and those of land mammals is striking. 
• At upper right there is section of the cortex of the ovary taken from a younger whale that accompanied this one, possibly her calf. There were no corpora albicanti on those ovaries, supporting the contention that this was a juvenile (pre-or peripuberal) animal. However, large numbers of primary, secondary and tertiary follicles are present in this section. Fine detail is absent because of significant autolysis in the specimen but their presence is certain. This is supported by the macroscopic image that follows this one.
• At lower right in the image is a cross section of the uterine wall of the juvenile whale. The resemblance between this section and a uterine biopsy in a mare is remarkable. In this case gland complexity and cross sections were minimal, also suggesting that this uterus had not been under the influence of progesterone in the recent past i.e. the animal had not yet begun to have estrous cycles.

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In the image shown below, a cross section of the ovary of the ovary of the mature whale is seen at left and that of the juvenile at right. A corpus albicans can be seen in the mature whale's ovary, just under the cortex, presumably displaced to medullary region by physical constraints. In both ovaries, the delineation between the medulla and the oocyte-rich cortex is amazing to this author. Such a clear delineation in not present in any domestic animal. Also striking is the thickness of the cortex (white bars) in the juvenile compared to that of the older animal. Histologically, the cortex of the adult was sparsely populated with oocytes suggestion that absolute ovarian senescence may occur in this species.

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Aging of the whale and the adolescent were determined by counting the layers of dentine that had been added from the pulp cavity over the course of the animal's life; approximately one each year. This procedure was conducted by Mr Yves Morin Yves.Morin@dfo-mpo.gc.ca courtesy of the Department of Fisheries and Oceans, Canada.

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The age rings in the adult at left in this image show that it was approximately 15 years old when it beached itself. Female Pilot whales may breed for 50 years, making it somewhat surprising that the cortex appeared to be so depleted of oocytes at only 15 years. By comparison, the adolescent was shown to be approximately 14 months of age, Accordingly, the ovarian cortex to be as well populated with oocytes.

An interesting finding in this whale was the structure of the ovarian adnexa. The larger of the two images in this amalgam serves as a key for the following discussion.

A large ovarian bursa was present and in the illustration below, it was filled with the tip of a rubber glove stuffed with paper towel to demonstrate its volume. The black arrow shows the entrance to the bursa.

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The uterine tube (fallopian tube) was a source of amazement. The entrance to the uterine tube (in effect the infundibulum) had, relatively speaking, an enormous opening and unlike fallopian tubes in domestic species, did not  narrow rapidly distal to the ovary. This structure was identical on the left and right sides of the tract and showed no evidence of fibrosis or hydropsalpinx suggesting that it may be abnormal. The physiological and anatomical basis for this structure could be the basis for a fascinating discussion!

Notes: http://en.wikipedia.org/wiki/Long-finned_pilot_whale

Gestation lasts approximately 12 to 15 months and calving occurs once every 3 to 5 years. Calves are generally 1.8 m (5 ft 11 in) at birth, and weigh about 102 kg (225 lb). The calf nurses for up to 27 months, with some evidence for longer lactation and extensive mother calf bonds. Most calves are born in the summer, though some calving occurs throughout the year. The males may compete for mates with fights involving butting, biting, and ramming. Mating also involves these activities, and some females carry scars from bites inflicted by males during the breeding season. Females have been observed to have calves as late as 55 years old, and lactate as late as 61. This evidence indicates that females may nurse their last calf until puberty (up to 10 years in males).