Chapter 7 Hot Behavior
7. Hot Behavior
While cooling, the snakes moved about
restlessly, trying to find shelter, and were capable of motion until bodily
temperatures were at least one degree below freezing. However, they were soon
immobilized and then gave the appearance of being anesthetized until they were
warmed to several degrees above freezing.
Henry S. Fitch, 1965
It
had been a cold spring punctuated with a few warm days in suburban Chicago. I
was walking across a frozen pond on Saint Patrick’s Day and an Eastern Garter
Snake (Thamnophis sirtalis), a neonate from the previous fall, was stretched
out on the ice about 20 feet from the shoreline. Using a ball point pen, I
chipped the snake off the surface of ice and put it my pocket. Upon returning
home, it was soon crawling around its new cage tongue flicking and exploring. How
long the snake had been on the ice I can’t be sure, but it had been several days
since the last warm period.
The
introductory quote is from Henry Fitch’s classic study of the Eastern Garter
Snake and it is a reminder that snakes have successfully adapted to temperate
latitudes by finding ways to spend the winter in hibernation. Surprisingly,
some snakes, particularly North America natricids, can spend the winter in
relatively shallow hibernacula and, even more astounding, they can spend the winter
submerged. Underwater hibernation will be discussed in Chapter 11. This chapter
looks at temperature relationships and social behavior in snakes. Behavior in
squamates is very dependent upon temperature: too cold and squamates are unable
move; too hot and they suffer heat stress and die. In between these extremes,
snakes hunt for food, search for mates, avoid predators, and spend much of
their lives shuttling between warm and cool microenvironments. Endotherms
(birds and mammals) tolerate a broader range of temperatures, so they spend
less of their time escaping uncomfortable temperatures.
The Importance of Heat
It has been known for some time that
temperature affects virtually all biochemical processes. Species adapted for
extreme cold or extreme heat have modified enzymes and chemical reactions so
that life processes can be maintained in extreme environments.
Snakes, like other reptiles, are
ectotherms and they usually heat their body with energy obtained from the
environment rather than maintaining a constant body temperature using energy
obtained from food, as birds and mammals do. Thus, snakes have lower energetic
requirements than endothermic animals. It also means snakes need to bask to
warm up if they live in environments with changing temperatures, and they may
have to seek refuge should the temperature get too warm or too cool. Most
snakes are active between 20–35º C, but some are active at 14º C, and some may
stay active up to temperartures as high as 41ºC. The majority of snakes,
however, prefer body temperatures between 27–34ºC, and the preferred
temperature is frequently close to 30º C.
For much of the 18th and 19th centuries,
it was generally believed that snakes (and all reptiles) were thermally passive
and the animal assumed the temperature of its environment. By the mid 20th
century, however, scientists understood that snakes were regulating their body
temperature behaviorally by moving between cool and warm locations. Basking in
the sun to warm up or moving into shade, a burrow, or water to cool off. Not
surprisingly, the elongated body possesses advantages and disadvantages when it
comes to gaining or loosing heat. A snake stretched out presents a high
surface-to-volume ratio that will allow rapid heat gain, but it also can lose heat
quickly should the temperature drop. By coiling, the snake reduces its surface-to-
volume ratio and can slow heat loss or heat gain. Staying warm for a snake
means being able to digest food and react to predators, and cold snakes can do
neither. A snake with a gut full of food that loses heat is also going to lose
the meal. If bacteria on the prey are capable of growing faster than the snake
can digest the meal, as may occur in cool conditions, the snake will
regurgitate whatever is in its stomach. Similarly, a snake that has lost
considerable body heat is unable to defend itself against predators.
There are snakes that rarely bask or don’t
bask at all, and these live in thermally stable tropical environments.
Homalopsid snakes have rarely been reported to bask, and the reason appears to
be a preferred body temperature of about 30º C, a temperature that can be
easily found in shallow, tropical waters. Regardless of whether air
temperatures have spiked to midday highs of more than 50º C , or dipped to
night time lows of 22º C , the shoreline, water, and mud maintain a much more
constant temperature, which hovers at 30º C and provides an acceptable
microclimate for the snakes. However, not all tropical snakes conform to environmental
temperatures. The Checkered Keelback (Xenochrophis flavipunctatus), which shares
the Southeast Asian wetland with homalopsids, move in and out of the water
looking for food. Once, a keelback chased a frog into our work area at mid day
when the temperature was pushing 40º C. The keelback must have been regulating its
body temperature using an alternative mechanism, possibly by moving to a
microhabitat that was substantially cooler than the air when it got too warm [Figure
7–1].
INSERT
FIGURE 7-1.
Figure 7–1. The graph shows five Rainbow
Mud Snakes (Enhydris enhydris) (represented by the thin lines) stayed within
the thermal envelope, and avoided the environmentally extreme temperatures of
southern Thailand. Below the graph is the highly aquatic, fish-eating
homalopsid Enhydris enhydris from Lake Songkhla, Thailand. From Murphy, et al.
(1999).
Considering the number of studies which
demonstrate that small, Australian elapids are nocturnal and rarely seen in the
open, sunny locations, Jonathan Webb and Martin Whiting asked the question, why
don’t small snakes bask? They placed 900 plasticine models of juvenile
Broad-headed Snakes (Hoplocephalus bungaroides) in the microhabitats where the
snakes occur. The model snakes were placed under rocks or in exposed
situations. Predators attacked 13.3% of the exposed models and 1.6% of models
under rocks. Birds were responsible for 75% of attacks on exposed snakes. On
sunny days, basking snakes could have been at their preferred body temperature
for more than four hours, but by staying in the shade they attained preferred
body temperatures for only two hours, a reduction of 50%. The young snakes were
trading thermal benefits for safety, and may have been prolonging their growth
and maturation while avoiding predatory birds.
The cost of basking suggested by the
Broad-headed Snake study is the greater risk of predation, but is this true for
adult snakes? Jinelle Sperry and Patrick Weatherhead radio tracked 63
Lindheimer’s Ratsnakes (Pantherophis obsoletus lindheimeri) in central Texas.
They found female snakes had a lower survival rate than males, and that
decreased survival of both sexes was associated with basking. Most male
mortality was in the spring while most female mortality occurred in the summer
and fall, after the eggs had been laid. Females were rebuilding their energy
reserves after egg deposition, and this required increased foraging and basking
and made the females more susceptible to predation. Twenty-three snakes were
confirmed dead, 13 (of 38) males and 11 (of 25) females; 11 of the 23 deaths
were probably from hawks, and two were killed on roads by vehicles while the
others were of unknown causes.
Heat is also important to female snakes
carrying eggs because it affects the rate of embryonic development. The
widespread North American Northern Water Snake (Nerodia sipedon) has
populations in southern Canada, a highly seasonal environment. Gregory Brown
and Patrick Weatherhead collected more than 326,000 temperature readings from
38 snakes over three years. Captive snakes from their population had a
preferred body temperature of 27.1ºC; the same preferred temperature was found
in free-living snakes. Snakes were active over a range of body temperatures but
did not often use opportunities to warm to the preferred body temperature. There
was one exception, however. Pregnant female water snakes regulate their body
temperature with more care than females that were not pregnant during the
July-August gestation period. Interestingly, males thermoregulated less accurately
than non-gravid or gravid females, which may have contributed to the slower
growth and smaller size of the males.
However, the same does not appear to be
true for some egg-laying species. Rob ert
Willson and Ronald Brooks collected body temperature data on the Eastern Fox Snake
(Pantherophis gloydi) in semi-natural enclosures and found no differences
between gravid and non-gravid female body temperatures or basking habits. The
difference between live-bearing and egg-laying species may be due to egg-laying
females retaining the eggs for a shorter period of time.
After eating, snakes will select warmer
environments which they use to raise their body temperature. This has been termed
postprandial thermophily; it decreases digestion time and this is thought to
increase the amount of food an individual snake consumes over time. Lynett Bontrager
and colleagues tested Corn Snakes (Pantherophis guttatus) to see if meal size
effected body temperature. Using 12 Corn Snakes housed in cages with a linear
thermal gradient in the floor, snakes were monitored during fasting and after
eating prey that was 5% and 10% of their body mass. The authors found that prey
size did influence temperature selection but the snakes that ate prey that was
5% of their body mass did not select warmer temperatures. The selection of
higher temperatures has the cost of increasing the snake’s metabolism and, at
the same time, decreases the digestion time and the time when the snake would
be vulnerable to predators because of the extra weight of the prey in its body.
Severe winter weather would be expected to
increase snake mortality, and that is exactly what Res Altwegg and co-workers
found in a long term study of the Aspic Viper (Vipera aspis) in the Jura
Mountains of northern Switzerland. Six populations containing 415 individuals
were monitored for 6 to 17 years. They found winter temperatures affected
population growth rates through juvenile survival. Adult survival was not
impacted by severe winters. They proposed that juveniles were less experienced
at finding over-wintering sites and that sites they do select may not provide
the protection needed to survive severe conditions.
Human activity near snakes may interrupt
snake basking, altering snake behavior and impacting their life history.
Christopher Parent and Patrick Weatherhead studied the Eastern Massasaugua
(Sistrurus c. catenatus) at Killbear Provincial Park in Ontario. The park has
more than 200,000 visitors per year, something Parent and Weatherhead belive
may provide enough foot traffic to disturb the snakes’ natural behavior. The
researchers had 30 of the park’s snakes surgically implanted with radio
transmitters. The disturbed areas had high human traffic (vehicles and
pedestrians); the undisturbed areas had very low human traffic. Comparing snake
movements between disturbed and undisturbed areas, they found exposure to
humans caused gravid females to spend more time sitting between moves. The
research also demonstrated the snakes in the disturbed area made shorter moves
than snakes in the undisturbed areas.
Joanna Burger tested Northern Water Snakes
(Nerodia sipedon) and Eastern Garter Snakes (Thamnophis sirtalis) that were
basking along a canal running through a park for flight distance. The water
snakes responded to pedestrians at a greater distance (2 to 4 m) than did
garter snakes (1.50 m), and she suggests that the paths should be at least 4 m
from the water to prevent disrupting basking snakes. Reduced basking time may
mean less time to eat, search for mates, or incubate developing embryos.
Infrared Receptors
Edward Tyson was the first person to dissect
a rattlesnake and produce a detailed description for 17th century science;
during the dissection, he did not miss the facial pits. He wrote,
Between the nostrils and eyes are two
other orifices which at first I took to be Ears, but after found they led into
a Bone that had a pretty large cavity, but no perforation.
Tyson recognized these were unique and
unlike anything he had seen in European vipers. In 1824, Johann Wagler applied
the name Bothrops to vipers with pits and large shield-like scales on top of
their heads. Bothrops means hole or pit. Constant Duméril and Richard Owen
considered the pits secreting follicles and by the mid 19th century, pits were discovered
on the labial scales of boas and pythons, but it was not until the 1950’s when
Theodore Bullock and F. P. J. Diecke experimentally demonstrated the pits were
in fact heat sensors [Figure 7–2].
INSERT
FIGURE 7-2.
Figure 7–2. Infrared sensing pits. A: The
loreal facial pit and its inner membrane are visible in this South American
Bushmaster (Lachesis muta). B: Labial pits can be seen on the scales bordering
the mouth of this Australian Carpet Python (Morelia spilotes).
Snake heat sensors come in two types: the
boa-python type pits have the infrared-sensing cells in grooves on the labial
scales or chin scales, and pitvipers have the infrared-sensitive cells on a
membrane suspended in the pit organ located on the loreal scale. Thus, facial
heat sensing organs have evolved at least three times in snakes: once in boas,
once in pythons, and once in pit vipers.
While pitvipers (Crotalinae) have a
distinct pit organ, other vipers (Azemiopinae and Viperinae) lack distinctive heat-detecting
structures. Despite the absence of distinct anatomy, some authors have proposed
that other vipers may also possess infrared imaging capabilities, possibly
using the supranasal sacs located under the supranasal scales. To test this
hypothesis, Adam Safer and Michael Grace used Western Diamondback Rattlesnakes (Crotalus
atrox) and Copperheads (Agkistrodon contortrix) to represent the pitvipers
(Crotalinae). Puff Adders (Bitis arietans), a Gaboon Viper (Bitis gabonica),
and a Rhinoceros Viper (Bitis nasicornis) represented the Viperinae. Each snake
was presented with two targets: a water balloon at 20–24ºC (the cool target)
and a water balloon at 32–35ºC (the warm target). In another set of trials,
they added mouse scent to the balloons. The results were dramatic. Pitvipers
actively tongue flicked the targets, turned toward the targets and struck the targets
(almost always the warm one) while the viperine snakes rarely showed interest
in either of the targets. Despite its relatively small sample sizes, the study
suggests infrared sensors are not widespread in snakes and that the viperine
snakes do not have a hidden heat sensor.
In a similar set of experiments, Corey
Roelke and Michael J. Childress tested pitvipers, Fea’s Viper (Azemiops feae),
true vipers (viperine), a natricid, and a colubrid for infrared reception using
suspended water filled packs. The water was either at room temperature or 50ºC.
Only the three species of pitvipers distinguished between the targets. The true
vipers (viperine snakes), Fea’s Viper, the natricid, and the colubrid oriented
toward both targets or showed no orientation at all, suggesting they lacked the
ability to detect infrared. When they did orient toward the target, it was
often with defensive behavior. This was the first time Fea’s Viper had been
tested for heat sensors, and it is of interest that they did not respond like
the pitvipers, since they are considered the sister to the pitvipers.
Heat-sensing pits allow snakes to
accurately strike prey in total darkness, even when their other senses have
been disrupted. A pitviper with its eyes covered with tape and nostrils filled
with cotton can still accurately strike a warm target. The heat receptors produce
an image in the snake’s brain.
Andreas B. Sichert and co-workers found
the opening for the pit too large to form a high- quality image on the pit
membrane, probably due to the snake’s need to gather heat information in a
short amount of time. The pit works like a pin-hole camera and, with an
over-sized hole, the snake’s brain must reconstruct the distribution of heat. Sichert
and colleagues provided a mathematical model that allows scientists to
reconstruct the heat pattern viewed by the snake.
George Bakken and Aaron Krochmal also
found the quality of the image produced on the pit membrane to be relatively
poor and low in contrast, suggesting background heat may partially obscure
prey. Snakes may, therefore, have difficulty targeting the strongest signal to
accurately strike prey. In order to account for the heat detection and striking
behavior seen in snakes, the pit must respond to temperature contrasts of
0.001º C or less. As a result, foraging snakes probably select ambush sites
that have a uniform thermal background and a strong thermal contrast. All of
this suggested to Bakken and Krochmal that the ancestral facial pit had lower
angular resolution and less sensitivity than the pit organs in living snakes; Bakken
and Krochmal proposed snakes first used the organ to find locations for thermal
regulation or possibly to locate roosting birds against the sky or mammals in
burrows with cool walls.
The brain is sensitive to fluctuations in
temperature, and the ability to selectively cool the central nervous system
during heat stress can be life saving. Brendan Borrell and colleagues used
infrared thermography to locate warm and cool regions in the Western
Diamondback Rattlesnake (Crotalus atrox), Blacktailed Rattlesnake (C.
molossus), and the Rock Rattlesnake (C. lepidus). Borrell and colleagues
demonstrated that the snakes use evaporative cooling in their respiratory
passages to cool the region around the mouth, nostrils, and facial pits when
the air temperature exceeds 20º C. Head and body temperature differences were
greatest at low relative humidity which supports the idea that snakes use
evaporative cooling. Of interest here is that, in addition to cooling the
snake’s brain, the behavior may also increase the resolution of the image the
snake creates with the heat-sensing pits. The authors reported that a complex
network of capillaries on the pit membrane is suggestive of a counter-current heat
exchange system. Previous work found the membranes functioned best between 17
and 29º C and, because of the respiratory cooling a temperature of 25º C can be
expected in the pit organ―a temperature within the limits of the pit’s optimal
functioning temperature range.
The evolutionary origin and purpose for
the facial pits has been the subject of considerable speculation. Recent
experiments by Aaron Krochmal and colleagues using Western Diamondback Rattlesnakes,
12 other pitvipers, and one viperine snake (the Puff Adder) have provided an
additional hypothesis for the natural history of the organ. The authors
provided each snake with an opportunity to navigate a plastic pipe Y-maze housed
in a chamber of 40º C, a temperature stressful for snakes. One of the terminal
Y refuges was kept at 40º C while the other was reduced to 30º C, the preferred
temperature for many snakes. They then tested the snakes with functional pits against
snakes with blocked pits. The results were telling. All of the pitvipers
located and chose the cooler (30º C) refuge. The Puff Adder tested was unable
to locate the cooler refuge (with or without the supranasal sacs blocked). The
researchers raised the temperature on one side of the maze to 50º C for the
Puff Adder because it sometimes inhabits extremely hot environments, but this
did not change the results. Apparently, pitvipers use their pits not only to
find food, but to locate areas of suitable temperature for thermoregulation as Korchmal
and colleagues hypothesized that this was the original function for the
infrared receptors in pitvipers.
Infrared receptors are poorly studied in
boas and pythons. Pits are absent in two species of pythons, but present in the
other 23 species. Richard Goris and colleagues found a Ball Python (Python regius),
a species with pits, responded within one millisecond to an infrared laser.
Ball Pythons have U-shaped labial pits that have an array of infrared receptors
at the bottom. The opening to the pit is always narrower than the bottom,
suggesting the pits are focusing the infrared onto the receptors.
In the boids, pits are present in the seven
species of Corallus, but are found in only one of the 10 species of Epicrates, and
they are absent in the related anacondas (Eunectes). Snakes of the genus Boa
also lack pits. Pits are present in both species of the arboreal Madagascar
boa-like snakes, but absent from the lineages of smaller snakes often
considered boids. The absence of pits may not mean that infrared receptors are
absent, however. Theodore Bullock and Rob ert
Barrett detected responses to infrared in the Green Anaconda (E. murinus), the
Rosy Boa (Lichanura trivirgata), and the Common Boa (Boa constrictor). Other
types of infrared receptors await verification.
Sexual Selection and SSD
Charles Darwin realized that the overall
phenotype of an individual was instrumental in determining reproductive success
when he wrote in the Origin of Species,
…sexual selection will give its aid to
ordinary selection, by assuring to the most vigorous and best adapted males the
greatest number of offspring.
Michael Whitlock and Aneil Agrawal have proposed
that healthy males are likely to sire more offspring than less healthy
individuals, and they viewed sexual selection as a mechanism to reduce the
frequency of harmful mutations. They note an absence of direct evidence to
address the key issue of the problem: is sexual selection in males stronger
than selection in females? Because female vertebrates usually make a larger
investment in offspring, most sexual selection is considered to be on the
males. That is, females thought to be selecting males for some trait that
translates into quality DNA.
The evolution of large males and smaller
females in snakes is generally attributed to selection for body size in
male-male combat, or other types of contests or displays that increase access
to females. The evolution of small males and larger females is usually thought
to be associated with males that have to search out females, the partitioning of
resources so the sexes exploit different food, or the selection of larger
females for increased number or size of eggs and offspring. However, evolution
of smaller males may also be the result of environmental factors, time spent
basking, foraging, or the nutritional quality of food eaten.
The
Black Ratsnake (Pantherophis obsoletus) is a widespread species in eastern
North American forests. The species engages in male combat and has male-biased
sexual size dimorphism (SSD). Gabriel Blouin-Demers and colleagues used
microsatellite DNA studies of 375 hatchlings from 34 clutches of Black Ratsnakes.
They found multiple paternity occurred in 88% of the clutches, despite the fact
that snakes do not mate near communal dens. They were able to identify 34 males
as fathers for 144 of the hatchlings. Males that sired the most offspring had
larger body sizes, but not longer tails, than males that were not as successful.
Larger males were successful by siring more offspring per clutch rather than
more offspring in many clutches, and the authors suggest this may have resulted
from sperm competition, assuming larger males producing more sperm.
Sylvain
Dubey and co-workers obtained similar results when studying Australia’s
Slatey-Grey Snake (Stegonotus cucullatus), another species with a male biased
SSD. They combined a long-term mark and recapture field study with a
microsatellite analysis. Examining 24 clutches and 219 offspring, they
discovered large Stegonotus males sired more offspring than smaller males
because they fathered more offspring per clutch, not because they mated with
more females. Presumably, larger body size means larger testicles, and larger
testicles means more sperm.
There
are studies that show that even in species in which females are larger than males;
the larger males sire more offspring. This appears to be the case in garter
snakes (Thamnophis), water snakes (Nerodia), grass snakes (Natrix), and sea
kraits (Laticauda). A recent survey of sexual size dimorphism in snakes done by
Rob ert Cox and colleagues suggested
that snakes are female-biased when it comes to large body size and the only
family that shows predominately larger males across most of its members are the
viperids, although the snakes they considered colubrids (includes multiple lineages)
showed a considerable number of species with large males. However, the worm
snakes, blind snakes, boas, pythons, natricids, xenodontids, and elapids tended
to have small males and large females. So what is responsible for SSD in
snakes? There does not currently seem to be an explanation for the diversity of
patterns seen in SSD in snakes, snake SSD will be better understood as the
patterns and phylogeny for snakes are further studied.
Pre-parental Behavior
Selfish genes and kin selection are
responsible for the parental behavior seen throughout the animal kingdom.
Parents increase the probability their genes will survive into the next
generation and beyond by going to extreme measures. These tactics may be
producing huge litters of offspring or clutches of eggs, or spending large
amounts of energy on a single offspring. Both of these extreme strategies occur
in squamates and, while parental care is often affiliated with actions taken
after birth, it really starts well before the eggs have formed or mating has
occurred.
Snakes can be capital breeders or income
breeders, or combine aspects of both strategies. Capital breeding females store
energy prior to egg production in the form of large fat bodies from which eggs
are then made. Once fertilized, all of the molecules and calories available to
the embryo are in the egg. During
gestation, the female does not eat, the eggs or embryos take up a substantial
amount of space in her body cavity. Capturing food and getting the prey through
her digestive system becomes, in theory, impossible because of the lack of
space. Once the eggs are laid or the embryos are born, capital breeding female
snakes are often severely weakened, left with depleated fat reserves and
emaciated bodies.
Other snakes are income breeders. They
accumulate stored food and energy, make their eggs, fertilize them, and get
development started. The female continues to feed during gestation and some of
the calories and nutrients are passed to the embryos to supplement what is
already in the egg. Food consumed during gestation is income for both the adult
snake and her offspring. After birthing the female is left with some food
reserves.
Xiang Ji and colleagues used hormonal
manipulation and ovarian follicle ablation to study how female snakes balance
these two alternatives. Female Chinese Cobras (Naja atra) were given follicle
stimulating hormone (FSH) and produced more eggs, but the eggs were smaller.
Other female cobras had some follicles ablated so they produced fewer,
relatively larger eggs. A control group of female cobras was also used and Ji
and colleagues found the clutch mass from all three groups did not
significantly differ. Body size (mass and snout-vent length) and egg mass at
laying played no role in offspring survival or growth. Of 48 hatchlings (21
males and 27 females) the females were more likely to die soon after hatching,
although nine of these deaths resulted from competition for food (presumably
they sustained envenomation from their siblings). They found a non-linear
continuum of egg size and egg number tradeoffs; hatchling survival and growth
was unrelated to egg size, and females grew more slowly than males. There
appeared to be a fixed upper limit to egg size for a female of a given body
size, and they found females that had follicle ablation did not produce larger
eggs.
Food availability as well as energy
storage also appears to play an important role in an individual’s ability to
reproduce. Emily Taylor and co-workers fitted 26 Western Diamondback
Rattlesnakes with radio transmitters before re-releasing them. Eight
individuals were offered dead rodents 1–4 times per week during two active
seasons while the other 18 served as controls. The fed snakes gained more body
mass per month than the control snakes. During the two study seasons, only one
of the 18 control snakes reproduced while seven of the eight snakes that
received food supplements reproduced. Food availability is likely a limiting
factor in how frequently a female snake reproduces.
Females
of some snakes (the Annulated Treeboa, Corallus annulata; Green Anaconda,
Eunectes murinus; and the Rainbow Boa, Epicrates cenchris) have been reported
to consume their unused yolks and dead embryos at birth. This same behavior was
reported in rattlesnakes, and Estrella Mociño-Deloya and co-workers used the
Mexican Lancehead Rattlesnake (Crotalus polysticus) to study maternal
cannibalism in 190 gravid females. About 68% of the females consumed some or
all of the non-viable offspring that composed, on average, 11% of the weight of
the litter. The authors suggested this allowed the female to recycle lost
calories and nutrients and speed her recovery from the demands of reproduction
more quickly than females who did not consume the non-viable offspring.
Mociño-Deloya and colleagues wrote,
Viperids in general are prepared to eat
carrion, and for this reason it is not so strange that they consume the
non-viable sections of their clutches after going through the great energy
expenditure caused by reproduction.
The condition of a female snake before she
reproduces can have a great impact on her ability to produce offspring. The
same is undoubtedly true for male snakes. Richard Shine and Rob ert Mason studied male Red-sided Garter Snakes
(Thamnophis sirtalis parietalis) at communal den sites in Manitoba, Canada and
examined their fitness based upon their body weight-to-length ratio when they
emerged from hibernation. Shine and Mason found male garter snakes that were 50
cm long varied in mass from 30 to 50 grams, and dissection revealed that, in
addition to small, fat bodies, body weight was due to lean mass, muscle, bones,
and organs. They found males were more likely to stay at the dens (and
therefore court females) if they were heavy-bodied and they lost mass slowly. Male
snakes were sometimes frenetic when they emerged from the dens, moving up to six
meters per second while they courted females. These snakes lost more than 10%
of their body weight at the dens and, combined with the fact that they had
small fat reserves, this behavior suggests that male garter snakes may rely on
muscle mass to fuel their reproductive activity.
Christopher Winne and colleagues encircled
a 10 hectare dried-up wetland with a drift fence to study the Black Swamp Snake
(Seminatrix pygaea), a small natricid that enters the mud when its aquatic habitat
dries up. They studied the snake at Ellenton Bay, in South Carolina in 2003, as
the isolated wetland was recovering from an extreme multi-year drought
(2000–2003). Winne and colleagues collected 69 females; of these 49 were
pregnant and had been pregnant for the 2.5 years they spent trapped in the mud.
The gravid snakes were individually housed in the lab and fed on salamander
larvae, often consuming 20% of their body mass at a single meal. Non-gravid
snakes consumed even larger meals. Despite the extended period of inactivity,
the females showed no signs of being malnourished. Winne and co-workers asked
the question, what allows the Black Swamp Snake to feed while pregnant? The
answer seemed to lie in the facts that Black Swamp Snakes don’t bask, they are
usually in close proximity to their prey, and their densely vegetated aquatic
habitat reduces predation risk during foraging and gestation. When the wetland
recovered from the drought, larval amphibians would soon be abundant and available
as a food source. The overall state of health of both male and female snakes is
closely associated with their ability to reproduce.
Viviparous or Oviparous
Squamates
can be oviparous or egg-laying while others are viviparous or live-bearing.
Egg-laying is the likely ancestral condition and this means lizards and snakes
have independently evolved live birth about 108 times. About 20% of squamate
species are viviparous. In fact, evolution of live-birth is known to have occurred
in species that belong to egg-laying genera, and among populations of species
that are otherwise egg-laying species. Therefore, the mechanism involved from
switching from egg-laying to live-bearing may be relatively simple. It is also
of interest that there are no clear-cut, documented reversals where a
live-bearing group evolves and then reverts back to egg-laying. However, there
are two likely candidates; both are New World pitvipers.
All
New World pitvipers are live-bearing with the exception of the four egg-laying
species of bushmasters (Lachesis) which also engage in female egg guarding.
And, the poorly known Colombian Toadheaded Pitviper (Bothrocophais
colombianus), a high-elevation species from Colombia, is rumored to lays eggs
and attend to them. These egg-laying species are nested well within the clades
of otherwise live-bearing lineages, and it seems likely they represent a
viviparous to oviparous transition―instances of retro-evolution.
In a survey of embryonic development in
reptiles, Rob in Andrews and Tom
Mathies found that many squamate eggs were laid once the embryos were about
one-third of the way through development, but there is considerable variation among
species; while some deposit eggs in very early stages, others deposit eggs
within days of hatching. Other reptiles (tuatara, turtles, and crocodilians) generally
deposit their eggs in earlier stages of development and this is possibly the
reason why there are no turtles or crocs that have live birth.
Pythons are egg-layers and show well
documented maternal behavior; therefore, pythons may be predisposed and
pre-adapted for viviparity, an idea explored by Olivier Lourdais and colleagues.
Using the Children’s Python (Antaresia childreni) as a model, they attempted to
determine if pregnancy is associated with changes in thermoregulation. Their
female Children’s Pythons laid eggs at an advanced stage of development when
compared to most other snakes; the embryos had pigmented eyes and well defined
lower jaws at oviposition. Using temperature- sensitive data loggers surgically
implanted in the snakes, the researchers documented pregnant females maintaining
higher and less variable body temperatures than non-gravid females. They also
observed the gravid females inverting their bodies 95 times during basking
while non-gravid females did this only eight times. This behavior is well known
to people who keep and breed pythons, and it seems likely gravid female snakes were
optimizing their body temperatures for the developing embryos prior to egg
laying by lying on their side and exposing their belly to the heat source.
Lourdias and colleagues hypothesized that the thermal requirements of egg
formation and embryonic development likely differ and report a significant
amount of embryonic development occurs in the oviduct. Body temperature differences
between non-pregnant and pregnant snakes were most pronounced in the three
weeks immediately preceeding egg-laying. Egg retention as a method for
controlling embryo temperature may be a major step in transitioning from
egg-laying to live-bearing.
So what kinds of environments select
snakes (and other squamates) with the genes to evolve from oviparity to
viviparity? The cold climate hypothesis was proposed in 1929 by Rudolf Mell and
later gained support from others workers. Many of the viviparous squamate
lineages are also high-altitude or high-latitude species and females living in
these cool habitats may be better able to control embryo temperatures. By
shuttling the developing young from one location to another, rather than
depositing them in a nest with a fluctuating daily temperature regime, the
embryos can be kept at more optimal temperatures. Females may also be better
able to defend the embryos from predators if they are retained in her. Aquatic
species also tend to evolve viviparity, possibly because nesting sites are in
short supply or because the female may be required to travel some distance to
lay the eggs.
Despite the many advantages of viviparity,
retaining embryos until birth comes at a cost. The female is burdened with the
extra mass of the embryos and her ability to escape predators may be reduced. Energy
costs for daily movement are likely increased because of the extra weight.
Gravid females may have to bask more frequently, again increasing exposure to
predators.
Exceptions are as common as patterns are among
oviparous and viviparous squamates. Tropical species are sometimes viviparous
and cold climate species are sometimes oviparous, some aquatic species are
viviparous and others are oviparous, and some snakes deposit their eggs and
leave them while others guard them. Among the squamates, there is a wide range
of reproductive adaptations and strategies ― a point previously made in Chapter
2.
When switching from egg-laying to live-bearing,
the loss of the egg shell is important because a shell would restrict the
exchange of gases and the development of a placenta. A placenta facilitates the
transport of nutrients and oxygen to the embryo and the removal of CO2 and
nitrogenous wastes. Placentas were once thought to occur only in mammals, but
today are know to occur in squamates, too. Placentas evolve from modified embryonic
membranes (chorion, amnion, allantois, and the yolk sac) [Figure 7–3]. But,
other changes are needed for a viviparous reproductive mode. Alterations are
needed in the lining of uterus to allow an embryo to implant into multiple
layers of epithelial tissue that are usually covered with non-adhesive
glycoproteins.
INSERT
FIGURE 7-3.
Figure 7–3. Puff-faced water snake
(Homalopsis buccata) embryos near full term are surrounded by membranes that
provide protection, nutrients, and exchange gases via the female’s circulatory
system.
Murray Thomson examined the research on
how the uterus could be adapted for embryo implantation. In mice the HoxA10
gene is important because it regulates the development of the uterus during
embryonic development, but it also is involved with the formation of
domed-shaped extensions of the uterine lining called uterodomes. No one ever
accused science of being overly creative when it comes to naming structures. The
uterodomes are thought to form the fusion of microvilli, small projections or
folds on cell membranes. Uterodomes have been observed in a variety of mammals,
including humans. The egg trapping structures have also been found in two viviparous
lizards, but were absent in two oviparous lizards, investigated to date.
Preliminary experiments with mice suggest that HoxA10 activity is associated
with uterodomes. Mice with the HoxA10 gene removed produce normal embryos, but
they could not implant on the uterine wall. Most Hox genes are active only
during embryological development, but HoxA 9, 10, 11, and 13 are the
exceptions. These genes are known to be active in the uterus of some mammals
and may be involved in the female reproductive cycle that prepares the uterus
to receive the blastocyst. It appears that an understanding of the switch from
oviparous reproduction to viviparous reproduction may lie in the understanding
of the regulation of the Hox10A gene.
If cool climates favored viviparous
reproduction in snakes, then the climate change from the Eocene “greenhouse” to
the Oligocene “icehouse” may have been an important period in snake evolution.
It was during this transition (late Eocene and early Oligocene, about 34 MYA) that
the mean global temperature decreased by 8–12ºC in less than 1 MY, and possibly
in as little as 0.4 MY. Vincent Lynch plotted the number of live-bearing and
egg-laying snake lineages through the Cenozoic and discovered increased rates
of speciation are associated with viviparity. Live-bearing snake species
increased 1.4 times during the Eocene-Oligocene temperature transition. At the
same time egg-laying species diversification declined about four times. He
wrote,
“…live-bearing vipers were likely able to
buffer similar negative effects on offspring survival, providing a reproductive
advantage over oviparous species, particularly during the dramatic climatic
cooling that marked the Oligocene and the Cenozoic in general.”
Female Attendance
Egg
brooding by female pythons using body heat to regulate the temperature of their
eggs was first reported in 1832 when M. Lamarre-Picquot presented a description
of python maternal care to the French Academy of Sciences. The acceptance of Lamarre-Picquot’s
claim took time because it ran contrary to the idea that snakes were completely
“cold blooded.” While at least some female
pythons (including the Burmese Python, Python molurus bivittatus) generate heat
for developing eggs, most python species are known to attend to their eggs. The
female wraps the developing eggs in tight coils of her body.
Fabien
Aubret and colleagues used gravid female Ball Pythons (Python regius) taken
from the wild and manipulated their nest attendance, allowing the snakes 0, 15,
or 60 days of attendance. Female’s presence had only a weak impact on
incubation temperature, but female attendance had a dramatic impact on egg
water loss. Clutches of eggs attended by females for 60 days lost only 16% of
their initial mass; eggs partially attended lost 37% of their initial mass, and
eggs artificially incubated without female attendance lost 51% of their mass
and had the lowest hatching success. The hatchlings from each group were then
given performance tests; maternally brooded offspring swam faster over longer distances
and were more active than artificially incubated offspring. The tight coils of
the female apparently reduced water loss in the eggs and produced healthier
offspring.
At
least two Australian elapids have been reported to have females that coil around
their eggs. The Spotted Mulga (Pseudechis butleri) and the common Brown Snake
(Pseudonaja textilis) have been reported to attend eggs in captive situations. But
the elapid best known for attending its eggs is the Hamadryad (Ophiophagus
hannah). In 1892, George Wasey first described female egg attendance in the Hamadryad.
Since that time, several anecdotal reports about female Hamadryads staying with
their eggs have been published. James Oliver described a captive female
building a nest of leaves, depositing her eggs, and staying with them until
hatching. Rom Whitaker and colleagues established a breeding program for the Hamadryad
at the Centre for Herpetology at the Madras Crocodile Bank. They obtained seven
Hamadryads in 1996 and built a series of brick cages. The cages were air
conditioned so a temperature gradient between 6–30ºC was present in each cage.
Females made a nest of leaves and sticks scraped together using their bodies.
The eggs were laid on the pile, and the female then added a second layer of
leaves; she then coiled on top. They obtained clutches of 16 to 37 eggs. Whitaker
and colleagues artificially incubated the eggs that hatched 57 to 63 days later.
The
female Rhombic Night Adder (Causus rhombeatus), a viper, is also known to coil
around eggs and stay with them during incubation. But there are conflicting
reports concerning the maternal attendance of other viperine snakes, and those
have yet to be verified.
Pitvipers
are a different story. While most New World pitvipers are live-bearing, many
Old World pitvipers lay eggs and about a dozen species are known to attend them.
Jacques Hill and colleagues had an opportunity to follow a free-living,
nest-attending female Malayan Pitviper (Calloselasma rhodostoma) in a deciduous
dipterocarp forest in northeast Thailand. Hill had captured a female at the
Sakaeret Environmental Research Station and implanted a temperature sensitive
radio transmitter on May 22. The female snake was released a few days after
surgery and her movements, as well as those of six other Malayan Pitvipers,
were followed through on the same field site. She was found using a rock
crevice in a north-facing slope, and the presence of eggs was confirmed on the
August 24 with the female coiled around them. The eggs were in contact with dry
soil and the female was visually confirmed on the nest 61 times over 56 days
[Figure 7–4].
INSERT
FIGURE 7-4.
Figure 7–4. A female Malaysian Pit Viper
(Calloselasma rhodostoma) coiled around her eggs. Sakaeret Environmental Research
Station, Thailand. Photo by Jacques G. Hill.
The female’s head was oriented toward the
crevice opening. On October 4 the female had eaten. One egg hatched on October 10
and a neonate was seen coiled with the mother; two more hatched two days later
but the young disappeared and could not be located. The female shed on or just
before the October 12, and on this date she was located 58 m from the nesting
site. She ate again on or before November 1. During nest attendance, her
average body temperature was 27.1ºC, while the average air temperature during
this time was 28ºC. The minimum possible incubation time was 48 days; the
maximum incubation time was 62 days, and the minimum time is the maximum time
reported for this species. A clutch size of three is the smallest reported for
the species and undoubtedly related to the small body size of the female (478
mm). Hill and colleagues suggested coiling around the eggs probably regulates
moisture, reduces desiccation and produces larger hatchlings. The female’s
temperature was 1.5ºC higher than an operative temperature model in a nearby
microhabitat and the authors noted that, while the temperature difference is
not as great as that created by pythons; thermogenesis cannot be ruled out for
this species. An unexpected observation of the study was that the female
actually grew during incubation, gaining 3.8 g, and 5 cm in length. However, the
growth was less than expected during a similar time interval for a
non-reproductive snake.
Live-bearing
female pitvipers attend to their young after birth, a behavior that may be best
understood as guarding. Harry Greene
and Dave Hardy studied Blacktailed Rattlesnakes (Crotalus molossus) in
Arizona’s Chiricahua Mountains and radio tracked six females and observed nine
reproductive episodes over six years. They observed mating four times and
observed females accompanied by one or more males on different occasions. From
the time females came out of hibernation until they gave birth, an interval of
about four months, they lived in a relatively small area, traveling less than
150 m from their winter location. The refuge was often an area excavated by a
rodent under a boulder. Females were observed with their offspring on 25 of 70
visits to the birth site, and sometimes the young were piled on top of the
female’s body. Females left the birth sites 1–5 days after the young had shed
their first skin, about 11–12 days after birth.
Terry
Farrell and co-workers found free-living female Pygmy Rattlesnakes (Sistrurus
millarius) would stay with their young until the neonates had completed their
first shed. Additionally, they found captive females were more aggressive
toward a potential predator while they were with their offspring.
Experimentally separating 16 females from their offspring with plywood barriers
resulted in 12 of the females crossing the barrier to associate with their young.
Eight of these females did not leave their offspring for the remainder of the
experiment. When a predatory Black Racer (Coluber constrictor) was introduced
to a female and her litter, the female rattlesnake was very defensive. She
struck at the racer and, in some cases advanced towards it and chased the racer
out of the enclosure. This behavior was not exhibited by non-pregnant females.
Joseph
Butler and colleagues reported on maternal attendance by the Eastern
Diamondback Rattlesnake (Crotalus adamanteus) and hypothesized that attendance
was due to short-term exhaustion after giving birth. This simple explanation
may have been a step in the evolution of maternal attendance but it does not
account for the experimental evidence from Terry Farrell’s work with pygmy
rattlesnakes, or the observation that the female usually stays with the young
until the first shed, or that females with young will drive away predators.
Since maternal attendance is present in Sistrurus rattlesnakes, the most basal
living species, it seems likely that maternal attendance is ancestral in
rattlesnakes.
Additional
evidence on rattlesnake maternal attendance has recently been reported by
Randall Reiserer and colleagues. They observed aggregations of sibling newborn
Sidewinders (Crotalus cerastes) at the entrances to the burrows where they were
born. Reiserer described these aggregations as tight balls of snakes that
sometimes blocked the entrances to the burrows, with snakes frequently
shuttling in and out of the aggregations. This behavior occurred within the
first 10 days of birth, before the young snakes first shed their skins. The
discovery was made while radio tracking two gravid females, a process during
which a third gravid female was found. The female snakes gave birth in mammal
burrows that were about 5 cm in diameter and were probably constructed by
Merriam's Kangaroo Rat (Dipodomys merriami). The three litters contained 8–12
young. Aggregations formed about 30 minutes before sunrise and before their
mother emerged from the burrow. The female stayed outside the burrow until the
ground temperature reached about 35ºC, which was usually five or six hours
after sunrise. Reiserer and co-workers were able to collect temperature data on
the environment in and around the burrows, as well as the core temperature of
the snake balls, and what they found was remarkable. Despite the fluctuating
temperatures of the air, ground, and burrow, the core temperature of the mass
of baby snakes was quite stable and often warmer than the air. Substrate
temperatures went above 42ºC, which is lethal to sidewinders, but the snakes
were able to maintain a mean temperature of 31.94ºC. The balling behavior
appears to stabilize body temperatures, reduce predation, reduce water loss,
and it may well be involved in developmental and social roles in the natural history
of this snake. Similar behavior has not yet been reported in other snake
species, but it seems likely it will be with time.
Social Snakes
Recognition of kin is unexpected and
poorly documented in snakes, but at least two species are able to recognize
their relatives and it seems likely this will be found to be widespread in
snakes. Rulon Clark demonstrated kin recognition with captive-born Timber Rattlesnakes
(Crotalus horridus) by measuring the distances between paired siblings and paired
non-siblings. Clark found females from the same litter associated with each
other more closely than females from different litters, even after they had
been raised in isolation from each other for more than two years. The females
would often lay next to each other and either touch each other or entwine their
bodies; this behavior was less often seen in females that were not siblings.
Males, whether they were siblings or non-siblings, were never seen entwined. Angelo
Pernetta and co-workers studied neonate Smooth Snakes (Coronella austriaca),
and found that after the neonates had shed their first skin, they responded
strongly with tongue flicking to non-sibling neonate odors.
Much of snake behavior is subtle. The absence
of limbs has applied constraints to snakes that make them unable to perform the
behaviors seen in many other tetrapods. The missing appendages have made snake
behavior difficult to interpret. Snakes hunting in cooperative groups is poorly
known, but there is evidence that some do. Richard Shine and family studied the
Turtle-headed Sea Snake (Emydocephalus annulatus) in New Caledonia in January
2004 and January 2005. Snakes were marked so that tagged individuals could be
seen in clear water and capture was unnecessary to identify the snake. An
analysis of the data found that the same snakes were captured on the same dates
one year later and that the snakes were in small social groups. The authors
hypothesized that snakes traveled from deeper water sites in small groups,
dispersed to feed, and then rejoined the group to travel.
Observations made by Tony Phelps on the Black
Mamba (Dendroaspis polylepis) suggest it is social as well. Phelps had 12 burrow-refuges
used by black mambas under observation. He found the snakes showed strong site
fidelity during the two year study, and he reported evidence of social
behavior. All of the snakes were adults, and a male and two females at one site
used the same refuge. At another site, two females shared a refuge, and the
snakes stayed together through the breeding season and beyond. The mambas were
seen basking together, lying entwined, and were overall very tolerant of each
other. Oddly, at some of the refuges, the mostly diurnal mambas shared their
space with Mozambique Spitting Cobras (Naja mossambica), a mostly nocturnal
snake, yet these snakes basked together. The mambas were also tolerant of a
python (Python sebae) that shared a refuge at one of the locations under study.
Combat behavior was first described as
courtship, but it was eventually realized two males were involved in these
bouts, not a male and a female. The behavior consisted of two snakes raising
their bodies off the ground in an attempt to gain a greater height than the
other in order to “top” their rival. These bouts frequently occur in the
presence of a female and have been described from snakes in many different lineages.
Mónica Feriche and co-workers examined the reproductive ecology of the
Montpellier Snake (Malpolon monspessulanus), a large European rear-fanged
species with a generalized diet. Males average 93.4 cm and females average 75.0
cm in body length. The authors described males as territorial, frequently
engaging in combat, and guarding mates. Males are larger than females and
engage in combat bouts and, therefore, males are putting more energy into body
size than into testical size and sperm production. Species with small males,
garter snakes for example, put more energy into sperm production than body size.
Southern Manitoba is well known for its
Red-sided Garter Snake (Thamnophis sirtalis parietalis) dens that may contain
10,000’s of snakes. When the snakes emerge from the dens in May, mating is a
high priority and there is strong competition between males to find females. These
dens have been heavily studied to reveal the reproductive strategies used by
both sexes of the Red-sided Garter Snake. Males come out of hibernation before
the females, bask, and move around the area but stay close to the hibernaculum.
Then, in a weakened state, female snakes exit the den after eight month
hibernation. Males immediately cover the females. Males choose females based
upon pheromones, skin lipids that signal the female’s reproductive fitness.
Females that have not yet recovered from hibernation are frequently targeted by
the males. Courting males rub the female’s back with their chin and, while
laying besides or on top of her send a caudocephalic wave of muscle contractions
along their body. This behavior disrupts the female’s ability to breathe and
induces hypoxia, causing her cloacal opening to gape. This provides males with
an opportunity to mate.
In large mating aggregations, some males have
been observed courting other males. The males being courted are referred to as
‘she-males’ and they are producing skin lipids that mimic the female’s
pheromones. These transvestite garter snakes tend to be larger than other males
and they are often covered in more mud than other males when they emerge from
hibernation. They also tend to crawl more slowly. When Richard Shine and
co-workers tested these snakes, they found the condition to be temporary and
suggest that many, if not all, males may exhibit the she-male condition when
they first emerge from the den. Males in this condition are also reluctant to
court females. The purpose of this may be to enhance the male’s reproductive
success in several ways. The she-males may confuse other males and trick them
into wasting energy. Or, the she-males may conserve energy by not courting when
they exit the den. Likewise, the
she-males may distract competing males from receptive, unmated females that
will be still be available in a day or two when the she-male has converted into
a normal male.
After a day or two, the females have
recovered from hibernation and they disperse away from the dens. At this point the
females are more capable of refusing unwanted males. Because larger females are
courted by males near the den, smaller females can escape the onslaught of
suitors by dispersing.
Communal Nesting
Female snakes sometimes deposit their eggs
in the same location year after year. These communal nests are apparently
beneficial to the offspring and they have been documented for many different
species in many different lineages. In Chapter 2, the Radder and Shine paper
demonstrated that communal nesting in lizards can reduce water loss in their
eggs, but there are other reasons for communal nesting. One hypothesis suggests
that females manipulate the phenotypes of their offspring by selecting a
favorable environment for embryonic development. The communal nesting sites,
for whatever reason, are viewed as more favorable than other sites.
Communal nests may be used by dozens of
individual snakes. Arlington James and Robert Henderson reported a communal
nest used by the Dominican snake Liophis juliae. Liophis is a widespread genus
in the Neotropics and data suggested they usually lay clutches of 2–10 eggs.
James and Henderson found more than 100 eggs in a hole under a tree. Some of
the eggs had hatched while others were in the process of hatching in mid
February. They estimated that the eggs represented the reproductive efforts of
25 to 30 females. Communal nesting for another species, a snail-eating snake in
the Neotropics, has been reported by Cristina Albuquerque and Herbert
Ferrarezzi. They described a nest containing 66 eggs in a hillside cavity under
overlapping slabs of concrete. Sibynmorphus mikanii is known to have an average
clutch size of about six eggs, and the authors estimated that 8 to 11 females had
deposited eggs at this site.
Female Black Ratsnakes (Pantherophis
obsoletus) often use communal nest sites that have a more constant temperature,
but some females chose individual sites. Lucy Patterson and Gabriel Blouin-Demers
tested Black Ratsnake eggs to see if the thermal mean and variance affected the
fitness of the offspring. Clutches of eggs were split into four treatment
groups: two groups with constant temperatures of 26 and 29ºC and two groups
with variable temperatures that had means of 26 and 29ºC, but varied by ±3ºC.
The embryos kept at warmer temperatures (29ºC) hatched earlier, had longer
bodies, and were faster and less defensive than offspring that developed at cooler
temperatures (26ºC). The authors also detected a difference in muscular
strength, noting that individuals incubated at constant temperatures were
stronger but they righted themselves more slowly than the offspring incubated
at warm temperatures. Suggesting that communal nesting, may in fact, produce
healthier offspring.
An earlier study done on the Australian Keelback
(Tropidonophis mairii) suggested that females located communal nests by the
presence of egg shells from other females, and captive experiments supported
this view. In fact, if the scent of an egg-eating snake predator, the
Slatey-Grey Snake (Stegonotus cucullatus) was added, the odor did not deter
female Keelbacks from using the communal nesting site.
Females of several species are known to
return to the location where they were born or hatched to deposit their own
offspring. Gregory Brown and Richard Shine found that Australian Keelback
females ready to lay their eggs returned to the location where their mothers
were collected before they nested. It appears the hatchlings imprint on their
nest site before they disperse. Brown and Shine noted that fidelity to natal
nesting locations confuses simple interpretations about inheritance. Offspring
may resemble their parents because of the similar environments encountered
during development both before and after they are out of the egg. Using a
communal nest over generations is probably producing similar phenotypes because
the nest probably has the same environmental conditions generation after generation.
Snakes are not known to have their sex environmentally determined, but a
generational, communal nest would likely favor females over males and produce
more females, if the environment was influencing sex determination as discussed
in Chapter 2.
The downside of using communal nest sites
is they are likely to attract predators and parasites. On one hand, an abundance
of eggs at one location may be more food than a single predator can eat. But if
it is a generational nest, predation may also become generational. Predator
satiation may, in fact, protect many of the eggs from being eaten, but should
multiple predators locate communal nest the local population could suffer
severe losses.
A recently discovered threat to snake eggs
is the burying beetle, Nicrophorus pustulatus. Gabriel Blouin-Demers and
Patrick Weatherhead found burying beetles inside hollowed-out Black Ratsnake
eggs. Beetles in the family Silphidae are usually carrion-eating species, and beetles
of the genus Nicrophorus usually work in mated pairs. They find a corpse of an
animal, bury it, protect it from decomposition with antibiotic chemicals they
secrete, and lay their eggs around the corpse. The eggs hatch and the beetle parents
stay with larvae and feed them with material from the corpse. Garrison Smith
and colleagues presented three species of the burying beetles of genus
Nicrophorus with snake eggs. Only Nicrophorus pustulatus was successful at
reproducing using snake eggs to feed its grubs. Given snake eggs, N. pustulatus
showed typical breeding behavior. The female beetle deposited her eggs around
the snake eggs; when the beetles hatched, the larva crawled into the snake eggs
through holes their parents had made for them. The parent beetles stayed with
the larva until they dispersed. While captive beetles also ate turtle eggs,
they had greater reproductive success with offspring fed on snake eggs.
In a review of communal egg-laying
patterns in amphibians and reptiles, J. Sean Doody and co-workers found
communal nesting behavior to be far more common than previously believed. Among
the squamates, they found 255 lizards (7% of egg-laying species) used communal
nests, and 52 species of snakes (3% of all egg-laying species) to nest
communally. Hypotheses as to why species use communal nests fall into two
categories. First, there are by-product hypotheses that included the scarcity
of nesting sites, or aggregation for a reason that is not necessarily
egg-laying. The second group of hypotheses is adaptive; communal nesting offers
protection from predators or increases reproductive success because of the
physical environment. Science has arrived at no single answer, but presents a
model for testing communal egg-laying with “choosers” who search for egg-laying
sites and excavate nests, and “freeloaders” who deposit their eggs in a nest
constructed by another. The costs involved with communal nesting have been
discussed above, and it is very likely that communal nests are used for
multiple reasons.
The phenotype-manipulation hypothesis
suggests that female selection of a nest site has long-term evolutionary
consequences. Producing offspring with variable phenotypes is not left to
genetics alone. The environment plays an important role that is only now beginning
to be understood. Snakes are far more social than was previously believed, and
research will undoubtedly find many more interesting relationships between
snakes and their environments.
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