Anna King

2001

Knowledge can be obtained and conveyed in a variety of ways. One can

spend hours upon hours hidden away in the corner of a library, reading the

thoughts and discoveries of other researchers and writers. Or, one can allow

himself to make his own discoveries through experiments and observations that

he makes himself.

Both methods are necessary in order to come to a complete understanding

of a topic. An experimenter cannot fully appreciate the things that she

observes without having a background in that area. In the same way, a man does

not truly use the knowledge he has gained from book research without applying

it to the real world in some way.

Knowledge of marsupial reproduction is this way. There is much to be

learned from the writings of scientists of the past, while at the same time

there are many new discoveries to be made as researchers of the present apply

this knowledge to answering new questions. The purpose of this paper is to

compile knowledge that has already been written on marsupial reproduction,

including the topics of: marsupial characteristics, reproductive anatomy,

sexual behavior, development of young, hormonal control, and ecological

implications of reproductive patterns, so that it can be used as a basis for

new insights and discoveries.

Many biologists of the past and present have been intrigued by a group of

animals known as marsupials. Marsupials are a subdivision of mammals with

several defining characteristics. First, marsupials generally have more

incisor teeth than eutherian (placental) mammals. In most marsupials, as in

most primates, the first toe of the hind foot is opposable to the other four,

and it always lacks a claw. Interestingly, most terrestrial marsupials have

lost this toe altogether. Marsupials also tend to have a smaller brain than

eutherians of equivalent size and their body temperature and rate of metabolism

are slightly lower than eutherians. (Gould, 52)

Other important characteristics of marsupials come from their unique

reproductive patterns and reproductive system. Externally, differences

include ìsuch interesting anatomical features as a prepenal scrotum and biparte

penes and vaginae in most groups and typically, but not always, a pouch over

the teats.î (Bronson, 187) The major difference is the dramatically

abbreviated period of gestation marsupials have adopted and the function of

this phenomenon. Few marsupials have a gestation period longer than their

oestrous cycle. This means that all marsupials give birth to highly altrical

(relatively underdeveloped) young that are less than 1g in size. (Bronson,

187) Instead of completing the majority of development inside the uterus,

attached to a placenta, marsupials do most of their developing attached to an

external teat.

These unique reproductive characteristics are reflected in the anatomy

of marsupials. First, there are several key differences between males and

females. Males tend to be larger and have darker fur than females of the same

species. Also, contrary to a common misconception, only females have pouches.

Marsupial females may have pouches that open on their back, on their front

side, or no pouch at all.

The female reproductive system of marsupials is distinctive from that

of female eutherians. The name ìdidelphidî given to marsupials is derived from

the paired lateral vaginae, which function to transport sperm upward, but not

to deliver young downward. (Hunsaker, 405) Birth occurs through a midline

pseudovaginal canal that functions as a shortcut to the outside. This shortcut

is formed where each lateral vagina loops around a ureter at the base of the

uteri. In most marsupials, it opens and closes with each birth. (Dawson,

63) This system is different than the singular vaginal opening found in

eutharian females.

The ovary, which produces the egg, is enclosed by the membranous

fimbria, which acts as an extension of the oviduct. Eggs pass through the

ampulla, an area where fertilization is most likely to occur, and a convoluted

area of the oviduct known as the isthmus, which leads to the uterus. At the

junction of the oviduct and uterus, there is a sphincter muscle, which allows

passage of the egg, but prevents backflow into the oviduct. (Dawson, 63)

Female marsupials have two discrete uteri that often have separate

openings into a combined cul-de-sac. The uteri have two basic layers: an

internal glandular endometrium, which produces secretions and a myomterium

layer of muscles whose function is to expel the young at the appropriate time.

(Dawson, 63) This system of two uteri differs from the single uterus found in

eutherian mammals.

As in many animals, the nearby excretory system fuses to make a

combined urogenital tract. The bladder of marsupials functions as a site to

concentrate urine and empties into the common urogenital sinus in both females

and males.

Male marsupials also have interesting reproductive anatomical

features. Male anatomy is generally similar to eutherians, with the exception

of a few features. The most notable is the location of the scrotum cranial to

the penis. (Knobil, 105) As noted by Dawson, ìWhen relaxed, the penis is S-

shaped in structure and enclosed in a preputial sac formed by an invagination

of the skin at the base of the cloaca. When erect during sexual arousal it is

extended downward and forward.î (Dawson, 71)

The scrotum has little fur and numerous sweat glands, which aid in

temperature regulation. It is essential for proper sperm production that these

organs are kept several degrees cooler than body temperature. A muscle

surrounds the scrotum and holds it tight against the body during cold weather

and times of stress, but relaxes and allows the scrotum to hang down during

periods of warm weather and after strenuous activity. (Dawson, 71)

Other definitive characteristics of male anatomy include a large

prostate gland and Cowperís gland. It is also notable that a few marsupials,

including kangaroos produce a copulatory plug of coagulated semen in the female

tract shortly after it has been ejaculated. It is thought that the plug may

function to block the passage of spermatozoa from other matings or to help in

sperm transport. (Dawson, 73)

After gaining an understanding of the reproductive anatomy of

marsupials, it is important to see how these parts function during the series

of reproductive events. Researchers have observed many different marsupial

species, including various species of kangaroos. This discussion of

reproductive events will focus on the processes carried out by kangaroos.

The breeding cycle begins with the proesterous phase in which the

ovaries enlarge and egg follicles grow and mature. The hormone, oestrogen

regulates this stage of reproduction and comes to a peak at the time a female

comes into ìoestrusî or ìheat.î During oestrus, the female becomes receptive

to copulation with males and ovulation occurs 1-2 days after oestrus. The post-

oestrus phase is followed by a secretory, or luteal phase, controlled by the

hormone progesterone. During this phase, the corpus luteum grows and

implantation may occur. Implantation does not affect the oestrus cycle, but

hormones released from lactation do. If lactation to nurse another young does

occur, the hormone, lactin, inhibits growth of the corpus luteum, thereby

delaying development of the blastocyst. (Dawson, 64-65)

This delay is known as ìembryonic diapauseî a phenomenon that occurs in

a number of animals. During diapause, the embryo is carried in the uterus for

long periods of time (many months) with its development arrested in the

blastocyst stage. This embryo functions as a ìbaby on holdî until hormonal

signals convey the message that the mother is able to nurse it.

When there is no young clamped to the teat, a surge of progesterone

occurs which triggers the development of the embryo. The gestation period for

kangaroos is nearly the same as the time of the oestrus cycle (about 38 days.)

This time period allows for the development of important features that the

altrical young uses as it journeys to the teat once it is born. (Dawson, 65)

Because the gestation period is nearly the same length as oestrus,

mating and fertilization occur in some species merely a day or two after

birth. This completes one element of the reproductive cycle. The other phase

of the reproductive cycle occurs with the baby attached to the teat and lasts

about 8 months until the mother returns to oestrus.

The young is attached to the teat for about 70 days until it is first able to

voluntarily release the nipple. After 100 days the baby begins to move

around. At 130 days it first opens its eyes and after 4-5 months its head

first emerges from the pouch. It isnít until the joey is 6 months old that it

makes its first emergence from the pouch. After several months of living in

the pouch and gathering nourishment from its mother, the young is eventually

permanently expelled from the pouch and begins its to show reproductive

behaviors of its own.

Among the reproductive behaviors of kangaroos are several

characteristic mating patterns. In a study conducted by McCullough, many

observations were made about these behaviors. In his study, McCullough noted

the occurrence of ìconsort pairsî consisting of a male, a female nearing

estrous and sometimes a young-at-foot. (McCullough, 183)

These bonds are formed as a male notices that a female is nearing

oestrus, and thus follows her closely to be sure that he is near the moment she

becomes receptive to mating. Timing is crucial for a male so he periodically

sniffs the female to see if she is ready for mating.

McCullough observed males ìtendingî females. He noted that the tending male

remained within close proximity (about 2 m.) of the female and shifted in every

direction she did. The female proceeded in normal movements, ignoring the

presence of the shadowing male. McCullough observed that the male periodically

approached the female, sniffing her tail. At first she ignored him and walked

away. However, if she didnít move away, the male grasped her tail, pawed at

her shoulders, and put on a display in front of her. During this display, he

moved in front of her and assumed an erect body posture. She rose up and made

nose-to-nose contact with him. He palpated his penis and she smelled it.

After this display, the female either rejected the male by returning to normal

feeding, or accepted him by hunching down and allowing mounting. (McCullough,

184)

During kangaroo copulation, the female stands crouched with her back

arched and the male standing semi-erect behind her. He clasps her with his

forearms and places his hindlegs outside of hers. He gives a sequence of slow,

rocking thrusts lasting only 10-40 seconds. There are often frequent quiet

pauses of 2-5 minutes and the entire act of copulation generally lasts 15-30

minutes.

\

As noted by Dawson, this process might seem simple, but it becomes

anything but casual due to the continued interference of other males and

attempts to drive them away. Dawson reported the observations of David Croft,

who observed an extended act of copulation that lasted over an hour. He

watched as an attendant male was displaced by a larger dominant male. The size

and strength of the dominant male were too intimidating for the attendant male

to challenge. (Dawson, 75)

Dominant males are often the most aggressive and large males in a

particular area. They succeed by searching for tending bonds held by the

largest males that they can easily displace without a serious fight. This

strategy maximizes their copulatory success, by allowing them to mate with many

females without having to spend as much time in tending bonds. (McCullough,

192)

The time in which a male is dominant varies according to species. The

role is extremely energy consuming and it is not uncommon for a male to die

shortly after he loses his status. There have been cases noted where a

dominant male will ìgive up his positionî for a period of time when

environmental conditions are poor and offspring are not likely to survive and

later reassume the dominant position. In this way, he can conserve his own

energy, while leaving chancy breeding to smaller males. (Dawson, 76)

McCullough noted that the existence of a hierarchy with a dominant male

is dependent on the population of an area. If the population is low and widely

spread out, it is less likely that a dominant male will be as successful as a

dominant male in a condensed population. (McCullough, 186)

During copulation, the relatively large oocyte becomes fertilized.

Sperm are rapidly transported through the lateral vagina and fertilization

occurs in less than 48 hours. The zygote undergoes the general stages of

embryonic development, with the exception of the morula stage. (Knobil, 110)

As described in detail earlier, there is great hormonal control over

this part of the reproductive process. If the right hormone signals are

present, the blastocyte develops within the uterus and it becomes connected to

the mother through a placenta.

There are no visible signs that a female is pregnant. However, as

birth nears, she is seen cleaning her pouch. The pouch secretes a waxy

compound that dries into a dark scale when it has been unoccupied. The female

holds the pouch open and licks this scale away. This cleaning begins 1-2 days

before birth and is most extensive 1-2 hours before birth occurs. (Dawson, 70)

When birth is about to occur, the female adopts a birth position that

is different for each species. In all positions, the pelvis is twisted to

bring the cloaca closer to the pouch. Just before birth, a small yellow yolk

sac appears at the urogenital opening. Then a clear allantois appears, and

finally the baby enclosed in the amnion is born. The newborn is still for only

10-15 seconds before it begins its journey to the pouch. (Dawson, 71)

Though the newborn is blind and has many underdeveloped features, it

has several characteristics that help it survive. The nostrils of the neonate

are well developed to allow it to engulf air as it travels. Also, the forearms

are also well developed and used grasp clumps of fur in an

alternating ìswimmingî motion. (Dawson, 71)

The mother plays no active role during this process, except for an

occasional licking of the pathway. It was originally thought that she did this

to guide her young, however, it is now believed that this functions to keep the

young from drying out. It is likely that the young uses its well-developed

nostrils and sense of smell to guide it to the pouch. (Frith, 114) It takes

about three minutes for the young to reach the pouch and once inside, it is

guided by its sense of smell to one of the four nipples. Research by curious

scientists has shown that there is no preference shown for right or left

nipples. (Dawson, 71)

The mother plays little active role in the early development of her

young. She periodically cleans her pouch and the joey by licking. It is

believed that licking the baby stimulates excretion of waste materials through

the skin. The mother is then able to consume its waste, while in the process,

able to recycle nearly 1/3 of the water from milk production.

Lactation is a crucial part of the development of the young. Studies

have shown that the composition of the milk changes over the course of

development to give the young more of the nutrients it needs. In a study by

Green in 1984, it was shown that milk was high in carbohydrates during the

initial stages of development, but the percentage of milk that was carbohydrate

decreased over time. The proportion of milk that was lipid showed an opposite

effect, as it was low initially, but steadily increased. In contrast, the

proportion of milk that was protein remained constant over the period after

birth. (Bronson, 189) These values show the importance of different nutrients

at various stages in development and the ability of the mother to provide the

nutrients that her young needs during development.

It is also interesting to note that cases have been observed where both

a young-at-foot and a neonate will nurse at the same time, but receive milk

with compositions suited for their own needs. (Bronson, 189)

Milk aids in the development of many features and it is during this

stage that sex differentiation occurs. Scientists have hypothesized that a

bias can be seen towards the sex of the offspring in kangaroos. Scientists,

Sunnucks and Taylor, conducted an experiment to determine whether maternal

weight had an impact on this bias. According to their results, there was a

correlation between maternal weight and offspring sex. Lighter females tended

to have female young, while heavier females had males. The researchers noted

that a subtle sex bias is seen in many species and it functions as a natural

way to select for the offspring that will best survive under environmental

conditions. (e.g. ñ sons will survive better and be able to reproduce more

themselves under good environmental conditions.) (Taylor, 576)

The manner in which sex is chosen is not fully known. It could be that

offspring of a non-favored sex die and are then replaced with another offspring

or the sex of the offspring could be determined before birth by a sperm

selection intrauterine process. Based on their conclusions, further research

needs to be conducted to learn more about this fascinating phenomenon. (Taylor,

577)

After spending about six months completely living in the pouch, a joey

makes his first adventure out. Several muscles line the edges of the pouch,

enabling the mother to close it tight enough to make a water-proof seal, or

relax it so much that the baby can purposely fall out.

Before allowing the young out, the mother cautiously looks around

making sure the environment is safe to let her vulnerable young one venture

into. When she is satisfied that all is clear, she relaxes the muscles of her

pouch. Sometimes she purposely tips the joey out of the pouch, while other

times he stretches and ìoozesî out.

The first venture out is quite short. The young stands just where he

was dropped and immediately climbs back in. As he gets older, ventures out

become longer. An affectionate relationship is formed between the mother and

joey. Observers have noted play boxing between a mother and joey and have even

seen a mother hug her young. If the young is lost while he is out, the mother

runs looking for it and calling loudly. The young also calls loudly, which

brings not only the mother, but other females up to it. (Bronson, 118)

In order to get back into the pouch, cooperation between the mother and

joey is required. The mother bends down, bringing her pouch lower to the

ground. The young approaches from the front and grabs the top of the pouch.

He then goes in head first, turns a complete somersault and ends up with his

head toward the entrance. The process of re-entry gets more and more difficult

as the joey gets bigger and often a tail or leg ends up awkwardly hanging out

of the pouch too.

At the end of pouch life (about 8 months after birth), the female

prevents her young from entering the pouch again by grasping it firmly with her

forepaws or moving away as it tries to enter. The young continues to suckle

from outside until it is a year old, and it continues to associate with its

mother for a considerable amount of time after weaning.

The stages of kangaroo reproduction as just described, comprise a good

overall model of marsupial reproduction. One major difference between

kangaroos and other marsupials is the number of offspring that are born at a

time. Due to its large size, the kangaroo is restricted to giving birth to one

offspring at a time. Among smaller marsupials, larger litters are often

observed. Opossums usually have six or more young at a time, bandicoots

commonly carry three or four, and six to ten offspring are seen in some

dasyurids. Also, some marsupials give birth to more young than can be

accommodated on their teats. An example of this phenomenon is seen in the

Virginian opossum, which is known to have produced an excess of at least nine

offspring. (Gould, 65)

Ecological Significance of Marsupial Reproduction

While studying marsupial reproduction, many scientists have analyzed

the ecological significance of their mode of reproduction. There has been the

idea that marsupials are inferior, or primitive, to eutherian mammals. This

theory, based on the appearance of a simpler reproductive system, is largely

discredited today.

The seemingly primitive female reproductive tract is now understood to

be more specialized than the eutherian anatomy. (Gould, 64) It is also known

that even though the initial energy investments of female marsupials in

reproduction are low, the energy cost after the young is weaned is similar to

that of a eutherian mother. As Gould states, ìThere is no evidence that

marsupial reproduction is inferior to that of eutherians; as in other aspects,

marsupials are simply different.î (Gould, 65)

Some evidence would support the hypothesis that marsupial reproduction

is quite well adapted. The period that the joey spends in the pouch gives him

time to see the world without actually having to independently survive in it.

During the youngís brief excursions out of the pouch, he learns many behaviors,

such as social patterns, how to run from danger, and how to find food. This

adaptation is very useful for the survival of the offspring.

Another successful adaptation of kangaroos and some other marsupials is

embryonic diapause. In this process, a female kangaroo can have three young at

once, each in different stages of development. She may have a young-at-foot, a

neonate suckling in her pouch, and a 'blastocyst on hold' all at the same

time.

There has been a great deal of speculation on the ecological significance

of this process. Some scientists have pointed out that embryonic diapause is

useful to rapidly replace young that are accidentally lost. This is certainly

true, but Frith points out that, ìunder normal conditions, the females return

to oestrus very quickly and the advantage would be slight.î (Frith, 109)

Another proposed advantage of embryonic diapause is that it functions as a way

to prolong the amount of time at the end of dry periods in which a female can

have pouched young. This effect has been observed in the red kangaroo, which

during favorable conditions will support a young-at-foot. However, if a

drought occurs and the amount of available food declines, there is a high

mortality rate of the pouched young and of the young-at-foot.

ìIf poor conditions prevail, the diapausing blastocyst, like a reserve player

is called into action, resumes development and is born. But if the drought

persists, it will survive in the pouch for only about 2 months and a cycle of

replacement of the young every 6-8 weeks until conditions improve after rain.

(Austin, 37)This method ensures that there will be an offspring ready to develop as soon as

conditions improve. Thus, energy and nutrients are saved in the process.

These insights into the ecological significance of marsupial

reproduction, as well as knowledge of marsupial characteristics, reproductive

anatomy, hormonal regulation, sexual behavior, and the development of young

create a solid basis for understanding marsupial reproduction. Now, it is time

to apply this knowledge and make further discoveries in the future.

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Press,1982.

Bronson, F. H. Mammalian Reproductive Biology. Chicago: University of Chicago

Press, 1989.

Dawson, Terrence J. Kangaroos: Biology of Largest Marsupials. New York:

Cornell University Press, 1995.

Frith, H. J. and J. H. Calaby. Kangaroos. New York: Humanities Press, 1969.

Gould, Edwin and George McKay. Encyclopedia of Mammals. San Diego: Academic

Press, 1998.

Hunsaker, Don. The Biology of Marsupials. New York: Academic Press, 1977.

Johnson, Martin H. and Barry J. Everitt. Essential Reproduction. Boston:

Blackwell Scientific Publications, 1984.

Knobill, Ernst and Jimmy D. Neill ed. Encyclopedia of Reproduction. V. 3 New

York: Academic Press, 1998

McCullough, Dale R. and Yvette McCullough. Kangaroos in Outback Australia:

Comparative Ecology and Behavior of Three Coexisting Species. New York:

Columbia University Press, 2000.

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