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The Pigmy Rattlesnake (Sistrurus miliarius)

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Pigmy rattlesnakes are vipers (family Viperidae). All vipers are venomous with hinged fangs. The Viperidae is divided into two subfamilies, the Viperinae and Crotalinae (the pit vipers). Pit vipers evolved from a viperine ancestor. In addition to the traits characteristic of the Viperinae they also have facial pits that detect heat energy (infrared light). Vipers are apparently a recent addition to the fauna of the new world. About 20-30 million years ago it appears a pit viper crossed over between Siberia and Alaska and thereby colonized this hemisphere (Greene, 1992). In the years since the new world was colonized, the pit vipers have undergone an adaptive radiation (evolved into many species with diverse niches).

One advanced group of pitvipers evolved a rattle attached to the tip of the tail. There are two genera of rattlesnakes--Sistrurus with three species and Crotalus with 23 species (Campbell and Lamar, 1989). Members of the genus Sistrurus appear to be similar to the ancestral rattlesnakes since they have nine large plates on the top of the head like most other pitvipers instead of many small scales (as in Crotalus). Some aspects of the circulatory system of Sistrurus are also intermediate between other pit vipers and the genus Crotalus (Lillywhite, 1992). The genus Sistrurus consists of three extant species, the pigmy rattlesnake (Sistrurus miliarius), the massasauga (Sistrurus catenatus), and the Mexican pigmy rattlesnake (Sistrurus ravus). The massasauga and pigmy rattlesnakes are clearly more closely related to each other than they are to other rattlesnakes. The relationship of the Mexican pigmy rattlesnake to the other species of Sistrurus and Crotalus is not clear at this time (Knight et al., 1993). There are three subspecies of S. miliarius, the Carolina Pigmy rattlesnake (S. m. streckeri), the dusky pigmy rattlesnake (S. m. barbouri), and the western pigmy rattlesnake (S. m. streckeri).

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Pigmy rattlesnakes are short, relatively thick-bodied snakes. They have a dark line through the eye on each side of the face and a series of dark, roughly circular spots running down the center of the back. These dorsal spots interrupt a thin reddish-orange stripe that runs along the midbody line. This line may be weakly formed, especially in the western subspecies. A row of dark blotches that are slightly smaller than the dorsal spots is located along each side of the body. The tail of young snakes is yellow, but darkens as the snakes reach maturity. Compared to other species of rattlesnakes, the rattle of S. miliarius is extremely small and is often broken back to only one or two segments. The background color of pigmy rattlesnakes varies both geographically and within populations. In S. m. barbouri the background varies from a pale gray to almost black, it is often stippled with many small light dots. In S. m. miliarius the background is often a light gray or brown, but individuals may also have pinkish or reddish background coloration--particularly in eastern North Carolina (Conant and Collins, 1991). In the western subspecies, S. m. streckeri the background is light gray or light brown. In all subspecies the belly is white with many dark spots.

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The genus Sistrurus is found in North American and Mexico. It consists of three extant species, the pigmy rattlesnake (Sistrurus miliarius), the massasauga (Sistrurus catenatus), and the Mexican pigmy rattlesnake (Sistrurus ravus). The massasauga is found in a wide band across the United States, ranging from Arizona in the southwest to New York and Ontario in the northeast (Campbell and Lamar, 1989). The pigmy rattlesnake is found in the southern quarter of the United States (North Carolina, South Carolina, Georgia, Florida, Alabama, Mississippi, Kentucky, Tennessee, Louisiana, Arkansas, Texas, Oklahoma, Missouri)

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Methods of Study

Our study of pigmies in central Florida has relied on mark-recapture techniques in which individually-marked animals in four somewhat separate populations are censused on a regular basis. At the Hog Island site, we have been conducting an average of 2-3 population censuses per week over the last six years, involving over 1000 individually-marked snakes. Mark-recapture studies of snakes are a bit more difficult than those of most vertebrates, as many of the marking techniques used to identify individuals of other species (ear clips, toe clips, drilling shells, attaching tags, etc.) are either not possible or not practical on snakes. We use PIT-tags (Passive Integrated Transponders) to individually identify our animals that are a year of age or over; these small glass-encapsulated microchips are implanted hypodermically into the snakes' body cavities, and when scanned with a reading device, transmit a signal containing an unique 8-digit number displayed by the scanner. Animals younger than one year of age are individually marked with unique color combinations of spots of nail polish; however, this technique is not permanent as the snakes lose the color combination when they shed. Prior to about a year of age (and approximately 20g in weight), we feel that injection of a PIT-tag has too high a potential for permanent damage to the snake, and we therefore withhold that procedure until they are clearly capable of receiving a PIT-tag with minimal effect (Jemison et al., 1996).

Our population censuses involve a group of 3-8 observers thoroughly combing the habitat for snakes that are visible without disruption of cover. Once located, these snakes typically remain in their hunting coil, or become immobile if they were moving when found, and can be identified by scanning for a PIT-tag or looking for a color combination on a younger snake. Once a snake is located, it is only handled for data collection if that individual has not been measured within the previous month. If it has been recently handled, its location in the habitat, substrate type, and activity (moving or coiled) are noted and the snake is left undisturbed where originally found. Most individuals, either coiled or moving, will allow an observer to approach very closely without fleeing. Most individuals that are not handled remain in the spot where first sighted after we determine their identity and leave them. For individuals that have not been recently sighted, we pick them up using a combination of pinning with a hook and handling with heavy leather gloves, and collect a variety of morphological, behavioral and physiological data, which include sex, length, weight, body temperature, presence of recently ingested prey, rattle characteristics, reproductive status, and defensive responses (rattle, flee and/or strike). Along with these regular censuses of marked individuals in our field-populations, we have also conducted a variety of studies on other aspects of pigmy biology; these studies are often individual projects that participating Stetson University students are conducting for classes, independent research, or senior projects.

Another useful technique for studying snakes is radio telemetry (Reinert, 1992). In this technique, radio transmitters are surgically implanted into the body cavity of a snake. The transmitted signal allows a researcher to find the snake even when they are hiding beneath cover or in dense vegetation. Some transmitters have a pulse frequency that is a function of temperature. With these transmitters biologists can study the thermal biology of the snake without bothering it each time body temperature data is collected. There has been very little work done on radio telemetry of pigmies. The only two studies that used radiotelemetry on Sistrurus miliarius were preliminary, involving a few snakes for short periods of time (Jacob, 1981; Holder, 1988).

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Foraging Behavior

Like most pitvipers, pigmy rattlesnakes are sit-and-wait (or ambush) predators. These snakes coil in spot and wait for their prey to come to them. In Florida over 90 percent of the snakes we find are coiled and immobile when located, and individual snakes have been observed to remain in the same location for as long as 2-3 weeks (May et al., 1996). At our study sites, pigmy rattlesnakes feed nearly exclusively on other herps, primarily Anolis lizards and several species of frog, including Hyla spp. (tree frogs) and Rana utricularia (leopard frogs). We have observed pigmies envenomating prey, tracking recently envenomated prey, or consuming prey on over a dozen occasions, and the prey in question has consisted of the species named above, as well as one ribbon snake (Thamnophis sauritus). The proportion of snakes with prey in the gut at the time of capture varies from less than 10 percent during the winter months to 20-25 percent in the late spring and fall. Though many pit vipers feed primarily on mammals as adults, the snakes at our sites apparently do so relatively rarely. Our dissections of museum specimens from the University of Florida Museum of Natural History indicate pigmy rattlesnakes in other habitats or areas may rely more heavily on other prey, such as small mammals as adults, and surprisingly, centipedes as juveniles.

There doesn't seem to be a great deal of variety in the prey taken by pigmies in our populations, but there is quite a bit of variation in foraging postures and techniques used by individual snakes. Although the most frequent foraging location is coiled on the ground in some type of leaf litters, some snakes forage from "arboreal" positions, elevated several inches to several feet above the ground on branches, fallen logs, or palm fronds. At times, especially during flood periods, some snakes move as high as 8-12 feet up into palm trees or saplings. Some individuals, in fact, seem to prefer feeding on a particular substrate type, so that we have some individuals that we know as "log pigs" who are consistently found elevated on logs in a foraging coil. As has been observed in other pit vipers, we have seen a number of pigmies using the "Reinert posture"(Reinert et al., 1984), with the body positioned at the side of a fallen log, and the head oriented upwards towards the top of the log, presumably waiting for a prey animal to use the log as a runway. In grassy areas of our study sites, pigmies typically position themselves at the edge of a small clearing in the grass, backed up to a grass clump, with their head orienting towards the middle of the opening or" arena".

Pigmy rattlesnakes, like other ambush predators, often have low prey capture rates since they must literally wait for the prey to come to them. Pigmies use their tail as a lure to increase the frequency that prey come within striking distance (Rabatsky and Farrell, 1996).

Luring behavior may have also influenced the form and function of the rattle of pigmy rattlesnakes. In contrast to their larger relatives in the genus Crotalus and even S. catenatus, the massasauga, and S. ravus, the Mexican pigmy, the rattle of pigmies is relatively small and quite easily broken. An adult snake with a rattle string of 6-8 segments produces a faint whirring sound when it rattles (a colloquial name for pigmies is "buzz worms") that can scarcely be heard from further than a few feet away broken their rattle back to the basal segment, so no noise production at all is possible, since at least two interlocking segments are needed to rattle against each other. Well over half of the snakes have rattles of 3 segments or less, so finding snakes by listening for them to rattle (which they do less than 10 percent of the time when disturbed) is not a very efficient technique. Patrick Cook and his co-workers at Appalachian State University in Boone, N.C. have shown that the rattles of pigmies are very small and the sounds produced by pigmies rattling are far fainter than those produced by other rattlesnakes, beyond what would be expected based on their small body size alone (Cook et al., 1994). They suggest that pigmies may have evolved a smaller, less effective noise-producing rattle because smaller, thinner rattles are more effective as luring devices.

One interesting result of feeding primarily on cold-blooded as opposed to warm-blooded prey is the rapidity with which the venom takes effect. Like many other pit vipers, pigmies release their prey after the strike, and then scent-track the prey after it has died. Feeding trials with captive pigmies have shown that while a mouse struck in the head or neck may be immobilized by the venom within 30-45 seconds, lizards and frogs may remain relatively mobile for 15-20 minutes after being struck. It is perhaps then no coincidence that on numerous occasions we have found dead Anolis lizards and tree frogs at our study sites with what appear to be fang marks and necrotic tissue, but no sign of a snake nearby. Apparently some of these ectothermic prey are able to escape beyond the range over which a pigmy can scent-track its prey. In one case we observed a pigmy orienting to a dead Anolis that had climbed several feet up a tree trunk and died, hanging by one claw. Though the snake apparently knew where the prey was, it could not have reached it unless the lizard became dislodged and fell.

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Defensive Behavior

Pigmy rattlesnakes first line of defense is to remain motionless. Their color pattern makes them hard to see in grass or leaf litter, especially when they are coiled. Pigmy rattlesnakes almost never warn approaching people by sounding their rattle. They are likely to remain motionless until stepped on or over. When molested with a gloved hand coiled pigmies usually remain motionless, but occasionally flee (16.4 percent of encounters), strike (2.5 percent) or flee and strike when grabbed (3.3 percent). Snakes that are stretched-out when approached are far more likely to flee (39.5 percent), or flee and then strike when grabbed (21.1 percent) than are coiled snakes. Pigmies with high body temperature are far more likely to strike than cool snakes (May et al., 1996). Hudnall (1979) also found pigmies were unlikely to strike when harassed by a moving boot. It would be interesting to see how pigmy rattlesnakes react to more natural predators. The nasty reputation of pigmy rattlesnakes (for example in Allen and Neill, 1950) may be a result of people often finding warm, moving pigmies in the road were they are likely to react very aggressively to people. Pigmies are more like to warn predators by rapid head twitches (side-to-side, with the head moving only a centimeter or two) than by rattling.

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Thermal Biology

Our studies of the thermal biology of pigmy rattlesnakes have shown these snakes are active over a wide range of temperatures. They are active in air temperatures as low as 13-14 degrees centigrade (with body temperatures only a few degrees higher); it's a rare winter day in central Florida when temperatures don't get at least that high for several hours a day. We rarely find pigmies with body temperatures of more than 35 degrees C. (May et al, 1996). Pigmies held in the sun actively seek shade (even ignoring threatening humans) when their body temperature is over 37 degrees. In Tennessee, Jacob (1981) found that pigmies placed in a thermal gradient avoided body temperatures above 36 degrees C and preferred a body temperature near 28 degrees C.

Bill Richardson, a recent Stetson graduate, found that pigmies in central Florida do not appear to use microsite temperature to chose foraging sites. Few pigmies, other than gravid females or some individuals that have recently fed, appear to bask in warm microhabitats.

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Seasonal Activity

In the mild year-round climate of central Florida, pigmy rattlesnakes are found active during all months of the year, though densities in the middle of winter are on average 2-3 times lower than in other months of the year (May et al. 1996). Chamberlain (1935) found pigmies year-round in South Carolina, but reported a peak in activity from May-October. Similarly, Dalrymple et al. (1991) and Hudnall (1979) found pigmies throughout the year in south Florida with a fall peak in activity. In southwest Missouri pigmies are above ground from mid-April to early November (Holder, 1988). Peaks in activity in fall are also reported by Dodd and Franz (1995) and Jacob (1981). These peaks in fall activity are observed in studies where authors depend on the snake moving to be observed (by going into traps or crossing roads). The peak in fall activity is probably a result of males hunting for females in the fall mating season, and young snakes dispersing from where they were born (Dalrymple et al., 1991)

In central Florida the proportion of snakes with prey in the gut at the time of capture varies from less than 10 percent during the winter months to 20-25 percent in the late spring and fall. Shedding also occurs throughout the year in this population (May et al., 1996). Unlike northern crotalids, pigmy rattlesnakes in Florida that are not active during cold weather do not migrate and congregate at hibernacula; rather, they apparently simply go under shallow cover within their active-season home range, and reemerge when temperatures are warmer.

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Reproductive Behavior

Though the birth of nearly all pigmy rattlesnakes at our sites begins in the month of August, the courtship and mating behaviors leading to the production of these offspring take place, surprisingly, nearly a year earlier. In the six years of our study, all of the cases of male-female reproductive interactions we have observed have occurred between late August and January, with the bulk of these observations taking place in October to December. Pigmy rattlesnake mating behaviors consist of several distinct components; like many pit vipers, male pigmies reportedly (Carpenter, 1972; Palmer and Braswell, 1995) engage in male-male combat rituals, in which a pair of competing males each attempts to physically dominate the other by twining around his rival's body and pinning the head and anterior trunk to the ground. We have not yet observed this behavior in our Florida populations. Male-female interactions have been observed on nearly 50 occasions, though, and consist of two phases. Pigmy rattlesnake males, like many other crotalids, perform mate-guarding behavior or prolonged courtship in which they remain in close physical proximity to a reproductive female for extended periods of time. These associated pairs may remain in contact, often with one snake coiled on top of the other, for several days at a time, without leaving their trysting spot. Large males are significantly more likely to be in a pair with a female than smaller adult males (Bishop et al., 1996). The 40-plus observations we have made of associated pairs have been between September and January. Less frequently, copulating pairs are observed. This process may take several hours to complete; we have collected six pairs of snakes so engaged for later data collection, and it can take up to several hours for them to disengage. After this fall-winter mating season, there is no further association between mated pairs, and the female apparently stores the sperm of her mate or mates until about April of the following year, when fertilization of eggs occurs, and development of the young begins. By early April, we begin detecting gravid females by palpation of the abdominal cavity. As the development of embryos proceeds, these gravid females frequently become more obvious, as they often choose relatively exposed sites in which to bask and elevate their body temperature, which accelerates the development of embryos. Unlike many other crotalid species, gravid female pigmies will feed until late in the gestation process.

Like most crotalids and viperids, pigmy rattlesnakes bear their young alive, and as parturition nears, we begin collecting gravid females and housing them in field cages until they give birth. In an average year, during the last two weeks of July we collect 20-30 gravid females, who are maintained in captivity until they give birth. Typically females are in captivity two weeks or less before parturition; we also normally find several recently-born litters in the field, near their mothers, each season. Litters of neonate pigmies normally remain tightly clustered within a few feet of their mother for several days after birth, until they complete their first shed. After shedding, they disperse to begin their mostly solitary lives. Though the mother is often quite near her babies when we find them, we have never seen active defense of the young when we gather up the litter for data collection. We have collected data on over 100 litters thus far, and all but 4 or 5 were born in August, with the remainder occurring in late July or early September (Farrell et al., 1995, 1996).

In central Florida, litter sizes range between 2 and 12, with an average litter size of around six. Pigmies in North Carolina have litter sizes that range from 3-9 with an average litter of 5.3 babies (Palmer and Braswell, 1995). In Arkansas litters ranged from 6=14 offspring (or oviductal eggs) with an average of 10.0 offspring (Carpenter, 1960).

As in many other snakes, larger females generally produce more offspring, but not bigger offspring. A newborn pigmy rattlesnake is an amazingly miniaturized animal, especially by crotalid standards. In central Florida they average about 4-5 grams in weight, and when tightly coiled, are scarcely larger in diameter than a quarter (Farrell et al, 1996) . In the western part of their range newborn snakes may even be smaller than they are in Florida (Fleet and Kroll, 1979) Young pigmies are so small and endearing in appearance that we have to resist the temptation to handle them without gloves.

Where pigmy rattlesnakes do differ from other crotalids, however, is in the frequency of reproduction. They can produce their first litter in as little as two years, though three to four years is a more typical age of first reproduction (Farrell et al., 1996). A two-year old pit viper bearing young is even more remarkable when one considers that such a female would have engaged in courtship and copulation when just slightly over one year of age. Not only can maturity come relatively early, but in addition, some females (about 25 percent) give birth in consecutive seasons, in some cases for at least three years in a row. They are not able to produce two litters in a single season, as they lose a significant fraction of their body weight (40-60 percent) with each litter (Farrell et al, 1995). Unlike most pit vipers, however, many females are able to recover the resources lost in reproduction rapidly enough to reproduce the following season.

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The growth of pigmy rattlesnakes has also been studied extensively in central Florida. Newborn pigmy rattlesnakes generally quadruple their weight within the first year of life, and can reach mature sizes by two to three years of age. The adult size of pigmies one Florida population varies quite a bit - reproductive individuals have ranged in weight from 50-150 grams, and 36-60 cm in length. Contrary to the commonly held belief that snakes grow throughout life, our snakes appear to do most of their growth in the first 2-3 years of life, after which growth slows appreciably, to less 1 cm per year (Farrell et al., 1996). It appears that adult snakes allocate most of their energy to reproduction, not continued growth. The adult size of most snakes appears to be relatively stable, and there are no differences in growth rates or body size between male and female pigmy rattlesnakes Bishop et al., 1996. There is, however, plenty of variation in growth rates and adult size between individuals, both in wild snakes and in captive snakes. A couple of pigmies that we have kept in captivity since they were a couple of months old in the fall of 1991 reached weights of 200-300 grams in less than two years, larger than any snake of any age we have ever found in the field. Sniffty, a captive male pigmy owned by Emmett Snellings Jr. of South Carolina reached a maximum weight of almost 660 grams (Snellings and Collins, 1996). It had a total length of 83.2 cm (svl=73.8cm) Clearly, growth rates of individuals are highly dependent on their specific environmental conditions.

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Population Biology

In Missouri pigmies appear to prefer "south-facing, rocky and partially wooded hillsides" (Johnson, 1987) , while in Tennessee pigmies appear to be found in riparian habitats (Jacob, 1981). In South Carolina we have found pigmies in pine woodlands. Palmer and Braswell (1995) state that in North Carolina pigmies are found in sandhill with pine and scrub oaks or in pine flat-woods. In Florida pigmies are found in a very diverse set of habitats. We have found exceptionally dense rattlesnake populations in isolated patches of semi-evergreen broad-leaved woodland (referred to as hammocks in Florida) that are surrounded by freshwater floodplain marsh (May et al., 1996). While pigmies in both Florida and other parts of their range occur in a variety of habitat types, including xeric uplands, our populations are found in moist forest subject to extended flooding for sometimes several months at a time. The specific characteristics of these floodplain habitats probably strongly influences many aspects of the biology of pigmies occurring there, so it is hard to know how the findings from our study apply to populations of pigmies occurring in other areas or habitat types.

It appears that pigmies are by far the most abundant venomous snake in the state of Florida. Other herpetologists have found them in areas far from permanent bodies of water in sand pine scrub habitat (H. Tiebout).

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