Part 3

A biennial reproductive cycle was found for the copperhead in Kansas (Fitch, 1960:162), the prairie rattler in Wyoming (Rahn, 1942:239) and in South Dakota (Klauber, 1956:688), the great basin rattler in Utah (Glissmeyer, 1951:24), and the western diamondback rattler in northwestern Texas (Tinkle, 1962:309). Klauber's (1956:687) belief that the reproductive cycle of rattlesnakes varies with climate, being biennial in the north and annual in the south, is supported by similar climatic variation in the reproductive cycle of the European viper which was discussed by Volsøe (1944:18, 149).

If data for a large number of females were arranged as are those in Table 8, they might reveal whether the breeding cycle is annual or biennial. The figures presented in Table 8 are misleading if viewed separately because of the small number of individuals included in some of the size classes.

The smallest reproductive female found measured 455 millimeters in snout-vent length. Conant (1933:43) reported that a female raised in captivity gave birth to two young at an age of two years and ten months. The size classes represented by gravid females found by Barbour (1956:38) in Kentucky indicate that breeding occurs at least by the third year.

The ovaries of female cottonmouths examined revealed ova in various stages of development. In individuals less than 300 millimeters in snout-vent length the ovaries are almost completely undeveloped; in immature individuals from 300 to 450 millimeters in length the follicles are from one to two millimeters in length; in post-post females follicles vary in size, the largest being about seven millimeters. Reproductive females also contain follicles of various sizes. One or two sets are less than three millimeters in length, and large ova that soon are to be ovulated are present. Ovarian ova found in April ranged in length from 23 to 35 millimeters. No embryonic development was observed in most individuals until June or later.

TABLE 8.--Percentage of Gravid Females of _A. p. leucostoma_ in 50 Millimeter Size Classes.

===================================== |Snout-vent |Number |Total |Percentage| | | of |number| | | length |gravid | in | gravid | | |females| size | | | | |class | | |-----------+-------+------+----------| | 450-499 | 3 | 14 | 21.4 | | 500-549 | 7 | 17 | 41.2 | | 550-599 | 8 | 17 | 47.1 | | 600-649 | 5 | 7 | 71.4 | | 650-699 | 2 | 9 | 22.2 | | 700-749 | 2 | 3 | 66.7 | | 750-799 | 1 | 1 | 100.0 | | 850-899 | 1 | 1 | 100.0 | | Totals | 29 | 69 | 42.0 | -------------------------------------

Increase in length of testes appears to be correlated with length of the individual rather than cyclic reproductive periods (Fig. 4).

The reproductive cycle in cottonmouths resembles that illustrated by Rahn (_op. cit._:237), in which the ovarian follicles of post-partum females begin to enlarge in late summer and autumn, with ovulation occurring the following spring. By means of retaining sperm successive broods possibly are produced after only one mating. In captivity, at least, some females may not follow this biennial cycle; Stanley Roth (M.S.), biology teacher in high school at Lawrence, Kansas, had a female of _A. p. piscivorus_, from Florida, that produced broods of 14 and 12 young in two consecutive years.

Embryonic Development

After ova are fertilized a three and one-half to four-month period of development begins which varies somewhat depending on the temperature. In almost every instance the ova in the right uterus outnumber those in the left. Embryos usually assume the serpentine form in the latter part of June and are coiled in a counterclockwise spiral with the head on the outside of the coil. At this time the head is relatively large and birdlike in appearance with conspicuous protruding eyes. Sex is easily noted because the hemipenes of males are everted. By late July scales are well developed and the embryo is more snakelike in appearance, but pigmentation is still absent. By mid-August the color and pattern are well developed, the egg tooth is present, the snake shows a considerable increase in size over that of the previous month, and much of the yolk has been consumed. Some females that contain well developed embryos also contain eggs that fail to develop. Sizes of ova vary irrespective of size of female and stage of embryonic development. Lengths of ova ranged from 22 to 51 millimeters in May to 35 to 49 millimeters in July and August. A two-yolked egg was found in one female.

Birth of Young

Accounts in the literature of 15 litters of cottonmouths fix the time of birth as August and September. Conant (1933:43) reported the birth of a litter in mid-July by a female that had been raised in captivity, and one female that I had kept in captivity for two months gave birth to a litter between October 19 and October 25. The conditions of captivity undoubtedly affected the time of birth in both instances.

Wharton (1960:125-126) reported the birth and behavior of a brood of seven cottonmouths in Florida. I was given notes of a similar nature by Richard S. Funk of Junction City, Kansas, on a brood of five cottonmouths. The mother of the brood was caught in June, 1962, in Tarrant County, Texas, by Richard E. Smith, and was 705 millimeters in snout-vent length. The first young was found dead in an extended position a few inches from the fetal membranes at 11:05 p.m. on August 22. The second young was born at 11:07 p.m. The intervals between the successive births were three, seven, and four minutes; and time until the sac was ruptured in each instance was six, five, eight, and 11 minutes. The time interval between the rupture of the sac and emergence of each individual was 41, 92, 154, and 34 minutes. The mother's actions in giving birth to the last four young were essentially as described by Wharton (_loc. cit._), except that the intervals between successive births did not increase. Within one minute after rupturing the sac and while its head was protruding, each of the four living young opened its mouth widely from three to seven times, then took its first breath. Breaths for the first three hours were steady at three or four per minute but then decreased to two or three per minute. Pulse rate for the four averaged 38 per minute while at rest but increased to 44 per minute after voluntarily crawling.

Number of Young per Litter

Records of from one to 16 young per litter have been reported (Ditmars, 1945:330; Clark, 1949:259), but the average is probably between six or seven. Most accounts in the literature present information on number of ova or embryos per female rather than the number of young. Size and age of the mother (Table 9) influence the number of ova produced. Allen and Swindell (1948:11) recorded three to 12 embryos in 31 cottonmouths varying in total length from 26 to 44 inches. An average of 6.5 embryos per female was found.

TABLE 9.--Number of Ova Produced by Fecund Cottonmouths.

====================+============+====================== Snout-vent length | Number | Number of ova, in millimeters | in sample | average and extremes --------------------+------------+---------------------- 450-549 | 10 | 4.1 (2 to 7) 550-649 | 11 | 4.9 (1 to 8) 650-749 | 4 | 6.3 (4 to 8) 750-849 | 1 | 5 850-949 | 1 | 14 --------------------------------------------------------

Mortality at birth has been recorded for almost every litter born in captivity (see Allen and Swindell, _loc. cit._; Conant, 1933:43; Wharton, 1960:125). A female that I kept in captivity gave birth to seven young. Three never ruptured their sacs, and another died soon after leaving the sac. The effects of captivity on females may result in higher rates of deformity and mortality in young than is common in nature. Klauber (1956:699-700) estimated that the defects brought about by conditions of captivity on rattlesnakes eliminate about three young per litter.

Population Composition

No investigator has yet analyzed the composition of a population of cottonmouths according to age, sex and snout-vent length. Barbour (1956:35) did sort 167 snakes into size classes, but did not determine sex ratio, size at sexual maturity, reproductive cycles, or snout-vent length. He recorded total lengths from which snout-vent lengths cannot be computed because of differential growth rates and different bodily proportions of the two sexes. I judge from my findings that he included immature individuals in his three smallest size classes (45.5 per cent of the population). I found at least 32.5 per cent immature individuals (Fig. 5) in my material, but it was not a natural population.

The sex ratios of several small collections from natural populations varied, and no conclusions could be drawn. Females comprised 53 per cent of the specimens included in Fig. 5 and in a group of 48 embryos which represented eight broods. That percentage may not be the percentage in a natural population but is used in making assumptions because I lack better information.

Reproductive Potential

If data in Fig. 5 are representative of a natural population and if 61 per cent of the females are sexually mature, the reproductive potential can be estimated as follows: assuming a cohort of 1000 cottonmouths contains 530 females, 61 per cent of the females (323 individuals) probably are adults. If 42 per cent of these females produce 6.5 young per female in any season (Tables 8 and 9), 136 females will produce 884 young. But if 50 per cent of the adult females are reproductive (as would be assumed if reproduction is biennial), 1050 young will be produced. Actually the number of young required per year to sustain a population is unknown, because mortality rates at any age are unknown.

GROWTH AND DEVELOPMENT

Size at Birth and Early Growth

Size at birth depends on the health of the mother. According to Fitch (1960:182), many litters of copperheads born in captivity are stunted. Seven young cottonmouths (two males and five females) born in captivity were each 185 millimeters in snout-vent length and 40 millimeters in tail length. Weights of the three living young were 10.0, 10.1, and 11.1 grams. Another litter of five young measured by Richard S. Funk were larger, and differences in the proportions of the tail length and snout-vent length suggest the sexual dimorphism found in larger individuals. However, sex of these young snakes was not recorded. Snout-vent length and tail length in millimeters were 232, 41; 243, 47; 229, 40; 240, 48; and 225, 40 in the order of their birth. These snakes are considerably smaller than the nine young of _A. p. piscivorus_ reported by Wharton (1960:127) that averaged 338 millimeters total length and 28.7 grams. The yolk of one young _piscivorus_ was 11.7 per cent of the total weight. Yolk is used up in about two weeks if its rate of utilization resembles that of the copperhead as reported by Gloyd (1934:600).

Early rates of growth of three living young are shown in Table 10. On the 56th day after birth, each was fed one minnow less than two inches long. Between the 80th and 120th days three additional small minnows were fed to each snake. Young cottonmouths increase nearly 50 millimeters in length by the first spring if they inhabit warm areas and feed in autumn or winter.

Variation in size of newborn cottonmouths may be less in nature than in captivity. Average size at birth can be determined accurately by the size of young captured in early spring, at least in northern parts of the range where winter feeding and growth do not occur at all or are negligible. Total lengths of 19 juveniles thought by Barbour (1956:38) to be seven to eight months old do not differ markedly from lengths of the five newly-born young measured by Funk.

TABLE 10.--Rate of Growth of Three Young Cottonmouths.

========+================================================= | | Snout-vent length/tail length--weight in grams | | Age +----------------+----------------+----------------| |in days | Female No. 1 | Female No. 2 | Male | |--------+----------------+----------------+----------------| | 2 | 185/40--11.1 | 185/40--10.1 | 185/40--10.0 | | 7 | 192/40-- | 190/40-- | 189/40-- | | 22 | 195/40--10.3 | 200/41.5--10.6 | 197/40-- | | 80 | 204/40--11.7 | 203/42--10.4 | 218/48--14.3 | | 88 | .... | 204/44-- | .... | | 143 | 215/40.5--13.3 | .... | 225/48--15.1 | --------+----------------+----------------+----------------

The Umbilical Scar

The umbilical cord is broken at birth and the navel closes within a few days; but the scar, involving from two to four ventral scales, remains throughout life. Position of the scar was found by Edgren (1951:1) to be sexually dimorphic in the eastern hog-nose snake (_Heterodon platyrhinos_), but nothing has been published on this matter concerning the cottonmouth. Consequently, I counted the scales of several individuals from the anal plate, and there was no marked difference in the position of the scar in males and females; it varied in position from the 10th to the 18th scale. When counted from the anterior end, the scar ranged from ventral number 115 to 122 (average, 119) in 28 females and from number 117 to 126 (average, 121) in 14 males. The difference between male and female cottonmouths is not nearly so great as in _Heterodon_.

Later Growth and Bodily Proportions

The only records of growth increments in a natural population of cottonmouths are those in Table 11. The period of growth is mostly the period of activity, and differences are expected between northern and southern populations. As size increases, determination of growth rate becomes more difficult because age classes overlap in size. Growth of any individual depends not only on climate and food but also on disease and parasitism and the innate size potential. Stabler (1951:91) showed weight and length relationships in two cottonmouths for a period of six and one-half years.

TABLE 11.--Growth Increments in Cottonmouths (Barbour, 1956:38-39).

============================================= | Number of | Total |Estimated| Estimated | | | length | age | growth | | | | | from | | | | | preceding | | | | | year | |individuals| in |in months| in | | |millimeters| |millimeters| |-----------+-----------+---------+-----------| | 19 | 260-298 | 7-8 | 25 | | 11 | 312-337 | 19-20 | 45 | | 40 | 355-485 | 31-32 | 95± | | 83 | 500-1000 | 43-44+ | ? | ---------------------------------------------

My study failed to reveal any secondary sexual difference in growth rate and maximum size. Of the 306 cottonmouths measured by me, 16 males and five females exceeded 700 millimeters in snout-vent length. Two males were more than 850 millimeters long. One cottonmouth lived in captivity for 18 years and 11 months (Perkins, 1955:262). The maximum total lengths were reported by Conant (1958:186-187) to be 74 inches (1876 mm.) in _A. p. piscivorus_ and 54 inches (1370 mm.) in _A. p. leucostoma_.

Proportions of various parts of the body vary considerably depending on age, size and, in some instances, sex. Heads are proportionately larger in young than in adults (Fig. 6), as is true of vertebrates in general. This larger head has survival value for the cottonmouth in permitting more venom to be produced and in permitting it to be injected deeper than would be the case if the proportions were the same as in adults. Relative to the remainder of the snake the head is considerably larger than in the copperhead (Fitch, 1960:108) and slightly larger than in the rattlesnake, _Crotalus ruber_ (Klauber, 1956:152).

In general, tails are relatively longer in males than in females of the same size (Fig. 7), except that there is little or no difference at birth. Growth of the tail in males proceeds at a more rapid rate. In certain individuals sex cannot be recognized from length of the tail relative to snout-vent length because overlapping occurs, especially in medium-sized individuals. Similar changes of proportions with increase in age occur in copperheads (Fitch, 1960:106) and rattlesnakes (Klauber, 1956:158-159), but the tail of the cottonmouth is relatively much longer.

SHEDDING

The Shedding Operation

Shedding of the skin is necessary to provide for growth and wear in snakes. The milkiness or bluing of the eyes, which causes partial blindness, marks the initial stage of shedding and is caused by a discharge of the exuvial glands that loosens the old _stratum corneum_ from the layer below. In four to seven days the opaqueness disappears, and the snake sheds after an additional three to six days (Table 12). Young snakes first shed within a few days after birth and generally shed more frequently than adults, but the interval is variable. The eyes of three young cottonmouths observed by Wharton (1960:126) became milky on the fourth day but cleared on the seventh day, and the skin was shed on the eighth day. The eyes of three young kept by me became milky two to three days after birth, cleared on the seventh to tenth days, and the skin was shed on the thirteenth day. Possibly the relatively long interval in this instance resulted from low relative humidity in the room where the snakes were kept. According to Fitch (1960:134), litters of young copperheads usually shed within three to ten days after birth; but under unusually dry conditions shedding did not occur for several weeks.

TABLE 12.--Duration of Preparatory Period (in days) to Shedding in 11 Cottonmouths.

============================== |Duration | Time |Time from | | of |between |beginning | |cloudiness|clearing| of | | | and |cloudiness| |of eyes |shedding| until | | | | shedding | |----------+--------+----------| | 5 | 6 | 11 | | 7 | 3 | 10 | | - | - | 6 | | - | - | 6 | | 5 | 3 | 8 | | 4 | 6 | 10 | | 7 | 3 | 10 | | 5 | 6 | 11 | | 5 | 3 | 8 | | 7 | - | - | | 7 | 3 | 10 | | ---- | ----| ---- | |[=X] 5.4 |[=X] 3.8| [=X] 9.0 | ------------------------------

Cottonmouths as well as other snakes usually do not feed until after the skin is shed and are generally quiescent during the period preceding shedding, except that immediately before shedding they become active and rub their snouts on some rough object and may yawn several times seemingly in an attempt to loosen the skin along the edges of the lips. After the skin is loosened from the head, more rubbing against rough surfaces and writhing serves to pull the old skin off, turning it inside out. Once the old skin has passed over the thick mid-body, the snake often crawls forward using rectilinear locomotion until the skin is completely shed. It normally comes off in one piece; but, if the snake is unhealthy or has not had sufficient food or water, the skin may come off in patches. Frequently one or both of the lens coverings are not shed immediately and impair the sight. Bathing or swimming ordinarily causes dried skin to peel off; and, because of the cottonmouth's aquatic habits, its chances of shedding successfully are much greater than those of less aquatic snakes. Cottonmouths that have recently shed have bright and glossy patterns, in contrast to the dull and dark appearance of those that are preparing to shed.

Frequency of Shedding

Most of our knowledge concerning the frequency of shedding is based upon observations of captives. It is known that the intervals between exuviations are largely dependent upon the amount of food taken and the rate of growth. Unless laboratory conditions closely resemble those in the field, shedding frequencies in captives probably differ much from those of free-living snakes.

Only two of my captives shed twice. The intervals between exuviations in the two snakes were eight and five months, lasting from August to April and from December to May, respectively. Ten other snakes shed once in the period from January through July. Stabler (1951:91) presented data concerning shedding of two cottonmouths kept 12 and 14 years in captivity. One shed 25 times in 12 years and the other shed 37 times in 14 years, giving an average of 2.1 and 2.6 per year, respectively. Neither of the snakes shed from December through March, but the period of shedding corresponded to the period of greatest activity and growth. In Florida, cottonmouths shed four to six times a year, according to rate of growth (Allen and Swindell, 1948:7).

FOOD HABITS

Methods of Obtaining Prey

Food is obtained by a variety of methods depending on the type of food, age of the cottonmouth, and possibly other factors. Some captives lie in ambush and others crawl slowly in active search. At the first cue of possible prey, either by sight, scent, or differential temperature detection by the pit, the snake appears to become alert and flicks its tongue out at fairly rapid intervals.