Environmentally cued parturition in a desert rattlesnake, Crotalus atrox

For Peer Review

Environmentally Cued Parturition in a Desert Rattlesnake,

Crotalus atrox

Journal: Biological Journal of the Linnean Society

Manuscript ID: Draft

Manuscript Type: Research Article

Date Submitted by the Author: n/a

Complete List of Authors: Schuett, Gordon; Georgia State University, Biology; Repp, Roger; National Optical Astronomy Observatory, Instrument Hoss, Shannon; San Diego State University, Biology Herrmann, Hans-Werner; University of Arizona, School of Natural Resources and the Environment

Keywords: Climate change , Drought, Ecdysis, Hormones, Life History, North American

Monsoon, Phenotypic Plasticity , Reptile, Snake, Sonoran Desert

Biological Journal of the Linnean Society


For Peer Review

Environmentally Cued Parturition in a Desert Rattlesnake, Crotalus

atrox

Gordon W. Schuett

1*, Roger A. Repp

2, Shannon K. Hoss

3, and Hans-Werner

Herrmann4

1 Department of Biology and Center for Behavioral Neuroscience, Georgia State

University, 33 Gilmer Street, SE, Unit 8, Atlanta, Georgia 30303-3088 USA

2 National Optical Astronomy Observatory, 950 North Cherry Avenue, Tucson, Arizona

85719, USA

3 Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego,

California 92182-4614, USA

4 School of Natural Resources and the Environment, University of Arizona,

Tucson, Arizona 85721 USA

*Correspondent: [email protected] or [email protected]

Word Count: 7, 144 (including references)

Tables: 2

Figures: 1

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ABSTRACT

Embryonic development and birth in animals is under physiological control and

regulation, yet a variety of environmental factors (temperature, precipitation, and

humidity) can influence timing of hatching or birth. Here, we provide evidence that

timing of birth in a large-bodied North American pitviper, the western diamond-backed

rattlesnake (Crotalus atrox), is environmentally cued. Specifically, we show that

parturition coincides with rainfall events during the second-half of the monsoon season

(late July to mid September). Our hypothesis was tested using randomization modeling.

Using radio-telemetry, we radio-tracked 21 individual adult females for extended periods

from 2001-2010. Sufficient data to test our hypothesis were generated from 2003 to 2007,

and during this period 21 females gave birth to 38 litters. In all years, births were

restricted to a 4-week period from 5 August to 7 September, and the mean range of birth

dates across all years was 15 days (± 5.2) (min-max: 6 - 19 days). Most births (92.1%)

occurred in August. The only year in which births were significantly associated with

rainfall events was 2007, although births in 2003 and 2005 occurred closer to rain events

than randomly generated births for respective years. However, when births across all 5

years were combined, the model indicated a significance difference in mean rain-days vs.

random rain-days. Hence, births occurred more closely to rain events than random days.

Increases in cloud cover, relative humidity, and declines in barometric pressure were

concomitant with monsoon rainfall events, though we did not test these variables.

ADDITIONAL KEYWORDS: Climate change – Deserts – Drought – Ecdysis –

Hormones – Life-history – Monsoon rainfall – Phenotypic plasticity – Reptiles – Snake

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INTRODUCTION

Gestation and timing of birth in vertebrates are life history events controlled and

modulated by the physiology (e.g., endocrinology) and behavior of the mother (Stearns,

1992; Rolf, 2002; Adkins-Regan, 2005; Norris, 2006). Notwithstanding their importance,

a wide variety of environmental cues, such as photoperiod, temperature, rainfall, and

even predation, also have important integrative roles on these processes. As a

consequence, births are timed when it is optimal for neonates (Warkentin & Caldwell,

2009). In this perspective, pregnancy and timing of birth can exhibit varying degrees of

phenotypic plasticity (West-Eberhard, 2003; Doody, 2011).

There are numerous individual-based studies on gestation length and birth dates in

mammals, primarily those that are large, relatively easy to observe, and/or aggregate

predictably (Clutton-Brock & Sheldon, 2010). Prominently researched species include

great apes (Goodall, 1968), herding ungulates (Clutton-Brock, 1982; Ogutu et al., 2011),

elephant seals (Le Boeuf & Reiter, 1988), lions (Schaller, 1972; Packer et al., 1988) and

bats (Bumrungsri, Bumrungsri & Racey, 2006). Studies on ungulates and bats, in

particular, show that rainfall cues are strongly associated with parturition dates

(Cumming & Bernard, 1997; Porter & Wilkinson, 2001; Bumrungsri, Bumrungsri &

Racey, 2006; Ryan, Knechtel & Getz, 2007; Ogutu et al., 2011). In these cases, the causal

connection of rainfall to timing of birth is resource-based (e.g., vegetation and insect

abundance) to assure adequate nutrients for lactating mothers.

In other live-bearing vertebrates, such as squamate reptiles (lizards and snakes), small

body size and cryptic lifestyles pose serious challenges to studies of pregnancy and birth

in nature (Morafka, Spangenberg & Lance, 2000). However, the relatively recent use of

implantable radio-telemetry has had pronounced impacts in advancing our knowledge of

these groups (Reinert, 1992; Dorcas & Willson, 2009). In oviparous reptiles, there is a

growing body of evidence that hatching is environmentally cued and can be early,

delayed, or synchronous (reviewed by Doody, 2011).

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Here, we investigated whether timing of parturition in a desert rattlesnake is

environmentally cued. Specifically, we tested the hypothesis that rainfall events during

the monsoon season are cues for timing of births in a population of western diamond-

backed rattlesnakes (Crotalus atrox) inhabiting the Sonoran Desert in southern Arizona.

MATERIALS AND METHODS

STUDY SPECIES

The western diamond-backed rattlesnake (Crotalus atrox) is a large-bodied, viviparous

(live-bearing,) venomous pitviper (Serpentes: Viperidae). In Arizona, C. atrox occupies

the southern half of the state and inhabits most of the biotic regions found there

(Campbell & Lamar, 2004). In some regions C. atrox is extremely abundant, often the

dominant snake species, and sometimes the dominant vertebrate predator (Nowak et al.,

2008).

STUDY SITE

The research site, located in Pinal County, Arizona, is 40 km SSE of the city of Florence,

8 km W of State Route 79. The focal area encompasses ≈ 3 km2 at the western edge of

the Suizo Mountains (32° 40'08'' N, 111° 07'22'' W, Conus 27), a summit that has an

elevation of 947 m. The region is designated as Sonoran Desert, Arizona Upland

Desertscrub subdivision (Brown, 1994; Phillips & Comus, 2000). In addition to

mountainous terrain, the general topography of the Suizo Mountains (SMs) is bajada and

desert flats, intersected by dry washes of varying sizes. Annual rain patterns of the

Sonoran Desert are bimodal (Mock, 1996; Phillips & Comus, 2000). Gentle to moderate

broad frontal storms occur from late fall to early spring (November through March), and

strong to violent, often localized, convective storms occur from mid- to late summer

(early July to mid-September), the period of the North American monsoon. At our site,

availability of free water is highly unpredictable.

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RESEARCH SUBJECTS

Capture and immediate processing

Twenty-one adult female C. atrox were captured from March 2001 through August

2007 (Schuett et al., 2011). Snakes were captured using conventional snake hooks and

plastic grabbers. The capture process involved grabbing a snake and placing it into a

clear plastic tube (1 m length; diameter varied in size). This was done gently and

quickly (typically less than 1 min) to minimize handling stress (Schuett et al., 2004 a).

In many cases, adult subjects were located basking at or near the entrances of dens in

spring (March-April).

Within 24-h of the initial capture, each subject was measured (snout-vent length, tail

length, head dimensions to the nearest 1-mm; body mass to the nearest 1.0 g) and sex

confirmed (via probing) while under anesthesia (isoflurane). Global Positioning System

(GPS) coordinates were collected as Universal Transverse Mercators, UTMs (Kenward,

2001). Each subject had an appropriately sized (< 5% of the total body mass)

temperature-sensitive radio-transmitter (models SI-2T and AI-2T, 11-16 g; Holohil Inc.,

Carp, Ontario, Canada) surgically implanted within the coelom following general

procedures used for snakes (Reinert, 1992; Schuett et al., 2011, 2012). For both short-

and long-term identification, each subject was photographed, implanted with a unique

PIT-tag (AVID, Inc., Norco, California, U.S.A.), and their proximal rattle segments were

colored using Sharpie pens. After processing, all subjects were released at the exact site

of capture.

Radio-tracking and observations

All 21 subjects were fitted with radio-transmitters and tracked by foot minimally 2-4

times per month from 2003 to 2007. Tracking was increased from late July through mid

September, the period of birthing. For each radio-tracked subject located, Universal

Transverse Mercator (UTM) coordinates were recorded using a hand-held Global

Positioning System (GPS) unit. These data were useful in re-locating previously used

sites and birth locations. Some of these spatial data have been presented elsewhere

(Schuett et al., 2013; in preparation).

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Determining reproductive status

The reproductive status of female C. atrox was determined using previous methods

(Schuett et al., 2011, 2013). Briefly, in each year they were radio-tracked, subjects were

assigned a reproductive status of either pregnant (when they produced a litter) or non-

pregnant. Following parturition, the reproductive status of a female changed to post-

partum through the end of that year, and in the following year was re-assigned as either

pregnant or non-pregnant. Like their viper relatives, female C. atrox are noticeably robust

when pregnant (Rosen & Goldberg, 2002; Taylor & DeNardo, 2005; Schuett et al., 2011,

2013). In our study population of C. atrox, vitellogenesis and ovulation occur in late

spring, and duration of pregnancy spans from early June to mid-September (Taylor &

DeNardo, 2005, 2011; Schuett et al., 2011, 2013). Thus, based on their increased mass,

we were able to readily detect reproductive from non-reproductive females by mid- or

late June. Births occur from early August to early September at sheltered sites (e.g.,

Neotoma middens, small mammal burrows, or rock shelves), but not at or near winter

refugia (Repp & Schuett, 2008; Schuett et al., 2011, 2013). Parturition was deemed

imminent when female movements from these sites were greatly reduced or ceased; thus,

radio-tracking episodes were often increased to 1-2 times per day to better pinpoint birth

dates. The number of offspring (or their molts) observed determined litter size. All

mothers remained at birth sites until their progeny underwent their natal ecdysis, which

occurred 5 to 7 days post-birth (Schuett et al., 2011, 2013). Maternal attendance is a

common feature in many temperate rattlesnakes and other North American pitvipers

(Price, 1988; Butler, Hull & Franz, 1995: Greene et al., 2002; Reiserer, Schuett, Earley,

2008).

ASSESSMENT OF RAINFALL

To check for rainfall events and storm systems in the area of our study site, we visited the

Intellicast website (www.intellicast.com) on a daily basis. Furthermore, we checked those

data against the weather reports at Tucson International Airport (TIA) via the National

Oceanic and Atmospheric Administration (www.wrh.noaa.gov/twc/). Importantly, during

the birth season (early August through mid September), we made frequent (sometimes

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daily) visits to the SMs to assess rainfall events (Schuett et al., 2011). For this study, we

used our estimates of rainfall frequency and amount of precipitation at the SMs. Also, we

checked with nearby weather stations for rainfall estimates. Generally, our results closely

matched those generated and reported by the TIA (Table 1).

RANDOMIZATION AND STATISTICAL ANALYSES

We used randomization procedures (Manly, 1991) to assess whether births were

significantly associated with discrete rainfall events during the monsoon season.

ASSIGNMENT OF RAIN DAYS AND BIRTHING DAYS

We first determined the dates of the earliest (5 August) and latest (7 September) recorded

births across all five years (2003 – 2007) of this study to define a general birthing season

for our population. To ensure we included rainfall events that might have influenced the

earliest and latest births in any given year, we extended this range ± 7 days (i.e., 29 July

to 14 September). Rainfall events occurring within this range of dates were included in

all single-year analyses, irrespective of the earliest and latest births recorded during that

particular year.

For each date between 29 July and 14 September, we assigned the smaller of two

absolute values representing the number of days before (negative value) and after

(positive value) a rain event (termed ‘rain-day’).

For example, rain on 10 August and 16 August, with no rain recorded between those two

dates, yields both post- and pre-rain day values for the intervening rainless dates, 11-15

August. Specifically, 10 August and 16 August would be assigned the value 0, because it

rained on those dates. Dates without rain would be assigned the absolute value

representing the minimum number of days post- or pre-rain, e.g. 14 August was 4 days

post-rain (value = 4) and 2 days pre-rain (value = -2), thus assigned the value 2.

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To preserve inter-year variation in rain patterns, we calculated rain-day values for each

year, independently. Each birth date of the study was given the corresponding rain-day

value.

RANDOMIZATION PROCEDURES

PopTools, an Excel add-in, was used to generate 10, 000 random birth dates for each of

the 38 recorded births (2003-2007) used in our analysis.

Each random birth date was assigned a rain-day value (described above) based on the rain

pattern for the year in which the birth occurred. This resulted in a single observed rain-

day value and 10, 000 random rain-day values for each female that produced a litter

during that year. For each year, we calculated the mean observed rain-days (i.e., mean

rain-days for all females who gave birth that year) and 10, 000 mean random rain-days,

We then tested our observed mean to the distribution of 10, 000 random means. Finally,

we conducted a global analysis in which we compared mean observed rain-days for all

births across all years (n = 38) to a distribution of random mean rain-days calculated

across all females. Our a priori hypothesis was that observed mean rain-days would be

less than the random mean rain-days; thus, we used a 1-tailed design for all analyses. The

alpha level for significance was set at α ≤ 0.05.

RESULTS

ANALYSIS OF RAINFALL

Rainfall data at the study site for the calendar dates 29 July to 14 September (J-S period)

from 2003 to 2007 showed variation in both frequency and quantity of rainfall (Table 1).

There were 36 discrete rainfall events in the J-S period for all 5 years (range: 3-9, mean =

7.2 ± 2.8). Total rainfall estimates for the J-S period for all years was 56.6 cm (range:

4.4-17.4 cm, mean = 11.3 cm ± 5.5). For all years, August was the peak month for both

frequency of discrete rainfall events (n = 25) and total rainfall (35.5 cm), followed by

September and July. Total annual rainfall (2003-2007) at the study site (152.1 cm) was

slightly greater (28.3 cm) than the total reported by the TIA (123.8 cm).

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TIMING OF BIRTHS

From 2003 to 2007, 21 females gave births to 38 litters. Parturition was restricted to a 4-

week period from 5 August to 7 September, and most (92.1%) occurred in August (Table

2). The mean range of birth dates across years was 15 days (± 5.2) (min-max: 6 - 19

days).

In 2003, most births (n = 8, 87.5%) occurred over a period of 13 days in August (Table

2). Two births occurred during a rainfall event (0) and five occurred 1 day following

rainfall (1). There was one birth on 2 September, which occurred 2 days following

rainfall (2).

In 2004, most births (n = 8, 87.5%) occurred over a period of 13 days in August (Table 2)

and were not closely aligned to rain-days (Table 1, see analysis below). Only two births

occurred during a rainfall event (0). One birth occurred 2 days following rainfall (2), one

occurred 8 days following rainfall (8), and three occurred on 28 August, 8 days prior to a

rainfall event (-8). There was a single birth on 1 September, which occurred 4 days prior

to rainfall (-4). There were only 3 discrete rainfall events in 2004 (Table 1).

In 2005, most births (n = 7, 85.7%) occurred over a period of 8 days in August (Table 2).

Three births occurred during a rainfall event (0) and two occurred prior to rainfall events

(-4 and -1). There was a single birth on 5 September, which occurred 3 days following

rainfall (3).

In 2006, all births (n = 9, 100%) occurred over a period of 19 days in August (Table 2).

Three births occurred during a rainfall event (0) and one occurred prior to a rainfall event

(-2). Four births occurred following rainfall events), distributed as one (1) three (2), and

one (4). No births occurred in September.

In 2007, all births (n = 6, 100%) occurred over a period of 6 days in August (Table 2).

Four births occurred during a rainfall event (0) and two occurred following rainfall events

(2). No births occurred in September.

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BIRTH AND RAINFALL ANALYSIS

In the five-year period in which we analyzed the association of birth dates and discrete

rainfall events, the only year in which births were significantly associated with rainfall

events (mean rain-days vs. random days) was 2007 (mean rain-days = 0.333, p < 0.001;

Fig. 1 and Table 2). Though not statistically significant, births in 2003 and 2005 occurred

closer to rain events than randomly generated births for respective years. When births

across all 5 years were combined, there was a significant difference in mean rain-days vs.

random rain-days (mean rain-days = 1.84, p = 0.037). Specifically, births occurred more

closely to rain events than random births.

DISCUSSION

Our central hypothesis that timing of births in a desert population of western diamond-

backed rattlesnakes (Crotalus atrox) is cued by rainfall events during the monsoon season

was supported. Specifically, using randomization procedures, we found that females gave

birth on dates that were significantly closer to discrete rainfall events than were randomly

selected dates. Despite the fact that statistical significance was not obtained in some

years, 3 of the 5 years had mean observed rain-days that were smaller (i.e., closer to a

rain event) than mean random rain-days. Furthermore, our combined analysis (2003 to

2007), which benefited from a much larger sample size (n = 38 births), revealed that, on

average, births occurred significantly closer to rain events than expected, based on a

random model. Significance was only attained in 2007 despite the fact that it did not

represent the largest sample size. However, the model performed well (significance was

attained) when we combined all five years for the analysis, which we attribute to a

function of sample size.

We were somewhat surprised to find how close birth dates were clustered in any given

year (min-max: 6-19 days). Although birth “synchrony” has been reported in other

snakes, including rattlesnakes (Graves & Duvall, 1993, 1995), no study provides

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longitudinal information of individual females nor did these studies formally explore

environmental variables as cues (e.g., modeling approaches).

Although we directly observed mothers and neonates (or their natal sheds), the actual

birth process was never directly observed. Nonetheless, the birth dates herein are highly

precise estimates based on frequent use of radio-tracking (Schuett et al., 2011, 2012).

Also, based on several lines of evidence, we are confident that we observed mother-

progeny associations and litter sizes were assessed accurately. First, communal birthing

(e.g., rookeries), which occurs in other rattlesnakes and pitvipers (reviewed by Graves &

Duvall, 1993, 1995) was not observed in this study (see Price, 1988; Schuett et al., 2011,

2013), Second, based on our unpublished DNA-based (microsatellite) parentage analyses

(R.W. Clark et al., in preparation), all progeny or their sheds were matched to identified

mothers. Neonate rattlesnakes associated with adult females may not be progeny or kin-

related (Graves & Duvall, 1993; Parker, Spear & Oyler-McCance, 2012). Last, other

studies show that litter sizes of C. atrox in the region of the study area are small (Rosen

& Goldberg, 2002; Taylor & DeNardo, 2005), thus we do feel our values are

underestimates.

Studies of Timing of Birth in other Snakes

Our inspection of the literature on rattlesnakes and other live-bearing snake species

detected few studies similar to the present one where timing of birth is correlated with an

environmental variable (e.g., rainfall) and explored under a specific model. Estimates of

timing of birth are commonly reported in wild rattlesnakes (e.g., Klauber 1972; Price,

1988; Martin, 1992; Graves & Duvall, 1993; Butler, Hull & Franz, 1995; Ashton &

Patton, 2001; Holycross & Fawcett, 2002; Greene et al., 2002; Reiserer et al., 2008;

Setser et al., 2010) and other live-bearing temperate snake species (Fitch, 1960; Ford &

Seigel, 1989; Seigel, Ford & Mahrt, 2000; Seigel & Ford, 2001). Despite the fact that

several of these studies were longitudinal and individual-based (per Clutton-Brock &

Sheldon, 2011), none provided a formal, hypothesis-based analysis of rainfall or other

environmental cues for timing of birth. Furthermore, several of these accounts were

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anecdotal and based on very small sample sizes (e.g., n = 1) or involved bringing females

into captivity (e.g., Price, 1988; Butler et al., 1995; Setser et al., 2010). Nonetheless,

Price (1988), Greene et al., (2002), and Setser et al. (2010) implicated rainfall as a

potential environmental cue for the timing of birth rattlesnakes.

Gestation Length and Control of Parturition

Although pregnancy in vertebrates, primarily in mammals, has been dominated by studies

emphasizing the role of the endocrine and paracrine systems (Challis et al., 2000; Weiss,

2000; McLean et al., 2007; Smith, 2007; Wada, 2008), both field and laboratory studies

have revealed that gestational length and timing of birth are often controlled and

modulated by hormones (e.g., steroids, oxytocin), prostaglandins (e.g., PGF2α,), and

abiotic factors such as photoperiod, temperature and rainfall (Cumming & Bernard, 1997;

Bumrungsri, Bumrungsri & Racey, 2007). This new perspective is presently extended to

live-bearing reptiles, especially in lizards (Atkins, Jones and Guillette, 2006; Rock, 2006;

While, Jones & Wapstra, 2007; Cadby et al., 2010).

Hormonal profiles of pregnancy have been described for both lizards and snakes,

though the number of studies on lizards far outnumbers those in serpents (Guillette, 1979;

Jones & Guillette, 1982; Guillette, Dubois & Cree, 1991; Schuett et al., 2004; Taylor &

DeNardo, 2011; Smith, Schuett & Hoss, 2012). Nonetheless, all of them demonstrate that

profound hormonal changes occur throughout pregnancy and post-partum periods (Smith

et al., 2012). Similar to studies of mammals, recent research on lizards emphasizes the

importance of an integrative approach to the investigation of gestation length and timing

of birth. One genus in particular, the Old World skink Niveoscincus has been extensively

studied (Girling, Jones & Swain, 2002; Atkins, Jones & Guillette, 2006; Girling & Jones,

2006; Cadby et al., 2010; Wapstra et al., 2010). These studies reveal the complex and

dynamic role of temperature and hormones (e.g., corticosterone, arginine vasotocin,

AVT) on gestation length and timing of birth. Studies of other live-bearing lizard species

show similar relationships (While, Jones &Wapstra, 2007; Cree & Hare, 2011; Rock,

2012). One striking result is that parturition in these lizards can be either accelerated or

delayed, often by weeks, when temperature conditions are not optimal (e.g., low) and

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inhibit the action of hormones associated with parturition, such as AVT (Girling et al.,

2002; Girling & Jones, 2006; While et al., 2007). Accordingly, females show a highly

plastic response to gestational length and timing of birth, which indicates a high level of

dynamic control between physiological systems and environment in the timing of birth.

To the best of our knowledge, studies similar to the present one have not been

conducted on other snakes. Rattlesnakes, including tropical taxa (Almeida-Santos et al.,

2004), and other vipers (Lourdais et al., 2004; Smith, Schuett & Hoss, 2012) are prime

candidates for parallel analyses. The present work provides compelling evidence that

females of C. atrox are capable of controlling timing of parturition to a certain extent,

which seems to be based, in part, on exogenous factors such as rainfall and perhaps other

variables (e.g., relative humidity, barometric pressure) that were not measured in this

study. Among snakes, C. atrox is one of the few species for which steroid hormone

profiles of pregnancy and post-partum periods have been reported (Schuett et al., 2004b;

Taylor & DeNardo, 2011; see Smith et al., 2012), which makes this species conducive to

future work investigating how the interaction between exogenous and endogenous factors

influence timing of parturition.

Timing of Birth and Rainfall Events

Why give birth during or near rainfall events? Based on empirical studies, timing of birth

in wild animals, including reptiles, occurs when it is seemingly optimal for the survival of

neonates. For example, rainfall is often linked to the availability of important resources

such as food (e.g., vegetation, insects, rodents). Furthermore, rainfall can provide

important environmental conditions for newborns, especially during their natal (first)

ecdysis. In many snakes, neonates undergo their first shed (natal ecdysis) shortly after

birth (Tu et al., 2002; Agugliaro & Reinert, 2005). In most temperate rattlesnakes,

including C. atrox (Price, 1988), the natal ecdysis occurs within 5-10 days after birth

(Greene et al., 2002; Agugliaro & Reinert, 2005; Reiserer, Schuett & Earley, 2008;

Schuett et al., 2001, 2013), and maternal attendance and care commonly occur during this

pre-shed period (Greene et al., 2002; Reiserer et al., 2008; Schuett & Repp, unpublished).

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Following shedding, neonates disperse and maternal care is terminated (Greene et al.,

2002; Reiserer et al., 2008).

If ecdysis is not completed successfully, a serious health threat is presented to the

neonate (Harvey-Clark, 1995; Harkewicz, 2002). For example, in newborn rattlesnakes,

retention of the natal shed (dysecdysis), including the eye caps, interferes with

locomotion, feeding, defense, and development of the rattle (G.W. Schuett, unpublished).

Retention of the shed can also lead to secondary bacterial and fungal infections (Harvey-

Clark, 1995; Harkewicz, 2002). Presumably, ecdysis problems in newborn snakes also

would increase vulnerability to predation. Numerous authors have mentioned the

vulnerability of pre-shed neonate snakes to predators (Price, 1988; Butler et al., 1995;

Graves & Duvall, 1995; Greene et al., 2002). A leading cause of dysecdysis in snakes

and lizards is desiccation and insufficient ambient moisture (Harkewicz, 2002).

Birth-sites and Post-birth Maternal Care

Although we have no direct empirical evidence, we suggest that female C. atrox at our

study site selected birth-site locations that were optimal for natal ecdysis, which we

presume would increase offspring survival. In hot and xeric environments, such as the

Sonoran Desert, rainfall produces environmental conditions (e.g., high humidity, ground

moisture, lower temperatures) that are ideal for the neonates to undergo their first ecdysis

(Harkewicz, 2002). Birth sites include small mammal burrows (e.g., Kangaroo rats),

wood rat (Neotoma albigularis) nests (middens), or shallow areas beneath rocky

structures (Schuett et al., 2011, 2013). During rainfall events, these sites exhibit

prolonged, high moisture and humidity, as well as lower temperatures (Schuett & Repp,

unpublished data), which is conducive to ecdysis. In contrast, high temperatures and low

humidity contribute to cutaneous water loss in snakes (Cohen, 1975; Dmi’el, 1985) and

thus are contributing factors in neonates failing to shed properly.

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Climate Change and Drought in Southwestern North America

Most climate-change models project that widespread areas of southwestern North

America will be negatively impacted by elevated temperatures and protracted drought

(Cayan et al., 2010; Woodhouse et al., 2010; Munson et al., 2011). Since 2000, most

areas of Arizona, especially the Sonoran Desert (Weiss & Overpeck, 2005), have had

severe drought and record-breaking high temperatures (National Oceanic and

Atmospheric Administration; www.wrh.noaa.gov/twc/). This has been termed the Early

21st Century Drought (Cayan et al., 2010). Forecasts based on paleoclimate records and

present-day modeling show that plant and animal populations will be affected in ways

both predictable and unpredictable (Munson et al., 2011; Lawing & Polly, 2011; Notaro

Mauss & Wiliams, 2012).

For example, the North American monsoon is a dramatic climatic feature of the

southwest from early July to mid September, especially in generating cloud cover,

elevated relative humidity, and violent thunderstorms centered in the late afternoon and

evening (Mock, 1996; Adams & Comrie, 1997; Sheppard et al., 2002). These storms

produce significant amounts of rainfall. Up to 50% of the annual rainfall occurs during

this period (Sheppard et al., 2002). Recent trends in climate change may disrupt the

North American monsoon, particularly in decreasing the frequency of storms and levels

of precipitation (Sheppard et al., 2002). Subsequently, this may negatively impact

reproductive activities in animals such as timing of birth in desert rattlesnakes. This view

is not unprecedented, as other studies have demonstrated negative impacts of drought on

reproduction in other vertebrates (Ogutu et al., 2011).

CONCLUSIONS

In studies of wild animals, especially in species that are iteroparous and long-lived,

monitoring recognizable individuals over extended periods (successive years, decades)

provides a wealth of ecological and evolutionary information otherwise unobtainable

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(Clutton-Brock & Sheldon, 2010). Examples include life history information such as age-

related changes in reproductive performance, differential fitness, social structure (e.g.,

kinship), selection responses (phenotypic changes), and linkages of reproductive

phenology to climate change (Clutton-Brock & Sheldon, 2010; Visser, et al., 2010).

The phenomena of gestation (incubation) length and timing of birth (hatching) in

vertebrates remain basic and fundamental life history problems to investigate. We thus

contend that robust ecological and evolutionary models will require detained information

on all major lineages. Given that reptiles exploit a wide variety of reproductive strategies

(Shine, 2003, 2005) and the sister group of mammals (Janes et al., 2010), further study of

development and birth in this group is thus justly warranted. Importantly, Doody (2011)

outlines future prospects for the study of environmentally cued hatching in reptiles which

are directly applicable to birth events in live-bearing taxa. Furthermore, owing to the life

history attributes of many vipers (e.g., large body size, tendencies to aggregate),

obtaining information on gestation, birth and post-birth events is possible (Greene et al.,

2002; Lourdais et al., 2004; Reiserer et al., 2008; Schuett et al., 2011, 2012), especially

with the use of radio-telemetry (Dorcas & Willson, 2009). Accordingly, we expect to see

more studies similar to the present one.

ACKNOWLEDGMENTS

We are especially grateful to Douglas Deutschman, San Diego State University, who

provided invaluable statistical and modeling counseling. Many individuals provided

invaluable assistance in the field, especially Martin Feldner, Ryan Sawby, and John

Slone. Dale DeNardo (Arizona State University ) was always helpful with surgeries and

addressing our questions. Arizona State University, Zoo Atlanta, and Georgia State

University (Center for Behavioral Neuroscience) funded this study. Also, we appreciate

the generous financial support of Dr. David L. Hardy Sr. and Kent Jacobs. The

Institutional Animal Care and Use Committee (IACUC) of Arizona State University

approved this study (protocol 98-429R), and appropriate scientific permits were obtained

from the Arizona Game and Fish Department.

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REFERENCES

Adams DK, Comrie AC. 1997. The North American monsoon. Bulletin of the

American Meteorological Society 78: 2197–2213.

Adkins-Regan E. 2005. Hormones and animal social behavior. Princeton, NJ: Princeton

University Press.

Agugliaro J, Reinert HK. 2005. Comparative skin permeability of neonatal and adult

timber rattlesnakes (Crotalus horridus). Comparative Biochemistry and

Physiology Part A 141: 70–75

Almeida-Santos SM, Abdalla FMF, Silveira PF, Yamanouye N, Breno Salomao MG. 2004. Reproductive cycle of the Neotropical Crotalus durissus terrificus: I.

Seasonal levels and interplay between steroid hormones and vasotocinase.

General and Comparative Endocrinology 139: 143–150.

Amarello M, Nowak EM, Taylor EN, Schuett GW, Repp RA, Rosen PC, Hardy DL Sr. 2010. Potential environmental influences on variation in body size and sexual

size dimorphism among Arizona populations of the western diamond-backed

rattlesnake (Crotalus atrox). Journal of Arid Environments 74: 1443–1449.

Ashton KG, Patton TM. 2001. Movement and reproductive biology of female midget

faded rattlesnakes, Crotalus viridis concolor. Copeia 2001: 229–234.

Atkins N, Jones SM, Guillette LJ Jr. 2006. Timing of parturition in two species of

viviparous lizard: influences of β-adrenergic stimulation and temperature on

uterine responses to arginine vasotocin (AVT). Journal of Comparative

Physiology B 176: 783–792.

Atkins N, Swain R, Jones SM. 2007. Are babies better in autumn or spring? The

consequences of extending gestation in a biennially reproducing viviparous lizard.

Journal of Experimental Zoology 307A: 397–405.

Bumrungsri S, Bumrungsri W, Racey PA. 2007. Reproduction in the short-nosed

fruit bat in relation to environmental factors. Journal of Zoology 272: 73–81.

Butler JA, Hull TW, Franz R. 1995. Neonate aggregations and maternal attendance of

young in the eastern diamondback rattlesnake, Crotalus adamanteus. Copeia

1995: 196–198.

Cadby CD, While GM, Hobday AJ, Uller T, Wapstra E. 2010. Multi-scale approach

to understanding climate effects on offspring size at birth and date of birth in a

reptile. Integrative Zoology 5: 164–175.

Page 17 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

18

Cayan DR, Das T, Pierce DW, Barnett TP, Tyree M, Gershunov A. 2010. Future

dryness in the southwest US and the hydrology of the early 21st century drought.

Proceedings of the National Academy of Sciences USA 107: 21271–21276.

Challis JRG, Matthews SG, Gibb W, Lye SJ. 2000. Endocrine and paracrine regulation

of birth at term and preterm. Endocrine Reviews 21: 514–550.

Clutton-Brock T. 1982. Red deer: the behavior and ecology of two sexes. Edinburgh,

Scotland: Edinburgh University Press.

Clutton-Brock T, Sheldon BC. 2011. Individuals and populations: the role of long-term,

individual-based studies of animals in ecology and evolutionary biology. Trends

in Ecology and Evolution 25: 562–573

Cohen AC. 1975. Some factors affecting water economy in snakes. Comparative

Biochemistry and Physiology 51A: 361–368.

Cree A, Hare KM. 2011. Equal thermal opportunity does not result in equal gestation

length in a cool-climate skink and gecko. Herpetological Conservation and

Biology 5: 271–282.

Cumming GS, Bernard RTF. 1997. Rainfall, food abundance and timing of parturition

in African bats. Oecologia 111: 309–317.

Diller LV, Wallace DL. 2002. Growth, reproduction, and survival in a population of

Crotalus viridis oreganus in North Central Idaho. Herpetological Monographs

16: 26–45.

Dmi’el R. 1985. Effect of body size and temperature on skin resistance to water loss in a

desert snake. Journal of Thermal Biology 10: 145–149.

Doody JS. 2011. Environmentally cued hatching in reptiles. Integrative and Comparative

Biology 51: 49–61.

Dorcas ME, Willson JD. 2009. Innovative methods for studies of snake ecology and

conservation. In: Snakes: ecology and conservation. SJ Mullin, RA Seigel (Eds.),

pp. 5- 37. Ithaca, NY: Cornell University Press.

Duvall D, Arnold SJ, Schuett GW. 1992. Pitviper mating systems: ecological potential,

sexual selection, and microevolution. In Biology of the pitvipers, Campbell JA,

Brodie ED Jr. (eds.), pp. 321–336. Selva: Tyler, Texas,

Fitch HS. 1960. Autecology of the copperhead. University of Kansas Museum of Natural

History 13, 85–288.

Page 18 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

19

Ford NB, Seigel RA. 1989. Phenotypic plasticity in reproductive traits: evidence from a

viviparous snake. Ecology 70: 1768–1774.

Girling JE, Jones SM. 2006. In vitro steroid production by adrenals and kidney-gonads

from embryonic southern snow skinks (Niveoscincus microlepidotus):

implications for the control of timing of parturition? General and Comparative

Endocrinology 145: 169–176.

Girling JE, Jones SM, Swain R. 2002. Induction of parturition in snow skinks: can low

temperatures inhibit the actions of AVT? Journal of Experimental Zoology 293:

525–531.

Goodall J. 1968. The behavior of free-living chimpanzees in the Gombe Stream Reserve.

Animal Behavior Monographs 1: 165–311.

Graves BM, Duvall D. 1993. Reproduction, rookery use, and thermoregulation in free-

ranging, pregnant Crotalus v. viridis. Journal of Herpetology 27: 33–41.

Graves BM, Duvall D. 1995. Aggregation of squamate reptiles associated with

gestation, oviposition, and parturition. Herpetological Monographs 9: 102–119.

Greene, HW, May PG, Hardy DL Sr, Sciturro JM, Farrell TM. 2002. Parental

behavior by vipers. In: Biology of the vipers: 179–206. Schuett, G.W., Höggren,

M., Douglas, M.E. & Greene, H.W. (Eds.). Eagle Mountain, UT: Eagle

Mountain Publishing, LC.

Guillette LJ Jr. 1979. Stimulation of parturition in a viviparous lizard (Sceloporus

jarrovi) by arginine vasotocin. General and Comparative Endocrinology 38:

457–60.

Guillette LJ Jr, Dubois DH, Cree A 1991. Prostaglandins, oviductal function, and

parturient behavior in nonmammalian vertebrates. American Journal of

Physiology 260: R854–R861.

Harkewicz KA. 2002. Dermatologic problems in reptiles. Seminars in Avian and Exotic

Pet Medicine 11: 151–161.

Harvey-Clark CJ. 1995. Common dermatologic problems in pet reptiles. Seminars in

Avian and Exotic Pet Medicine 4: 205–219.

Holycross AT, Fawcett JD. 2002. Observations on neontal aggregations and associated

behaviors in the prairie rattlesnake, Crotalus viridis viridis. American Midland

Naturalist 148: 181–184.

Page 19 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

20

Janes DE, Organ CL, Kujita MK, Shedlock AM, Edwards SV. 2010. Genome

evolution in Reptilia, the sister group of mammals. Annula Review of Genomics

and Human Genetics 11: 239–264.

Jones RE, Guillette LJ Jr. 1982. Hormonal control of oviposition and parturition in

lizards. Herpetologica 38: 80–93.

Klauber LM. 1972. Rattlesnakes: their habits, life histories, and influence on mankind,

two vols, 2nd

edition. University of California Press, Los Angeles and Berkeley.

Lawing AM, Polly PD. 2011. Pleistocene climate, phylogeny, and climate envelope

models: an integrative approach to better understand species’ response to climate

change. PLoS ONE 6: e28554.

Le Bouef BJ, Reiter J. 1988. Lifetime reproductive success in northern elephant seals.

In: Reproductive Success. Clutton-Brock TH (ed), pp. 344-362. Chicago, Illinois:

The University of Chicago Press.

Lillywhite HB, Navas CA. 2006. Animals, energy, and water in extreme environments.

Physiological and Biochemical Zoology 79: 265–273.

Lourdais O, Bonnet X, Shine R, DeNardo, D, Naulleau G, Guillon M. 2002. Capital

breeding and reproductive effort in a variable environment: a longitudinal study

of a viviparous snake. Journal of Animal Ecology 71, 470–479.

Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G. 2004. Climate affects

embryonic development in a viviparous snake, Vipera aspis. Oikos 104: 551–560.

Macartney JM, Gregory PT. 1988. Reproductive biology of female rattlesnakes

(Crotalus viridis) in British Columbia. Copeia 1988: 47–57.

Manly, BFJ. 1991. Randomization and Monte Carlo methods in biology. London, UK:

Chapman and Hall.

Martin WH. 1992. Phenology of the timber rattlesnake (Crotalus horridus) in an

unglaciated section of the Appalachian Mountains. In Biology of the pitvipers,

Campbell JA, Brodie ED Jr. (eds.), pp. 259–278. Tyler, Texas: Selva.

McLean M, Bisits A, Davies J, Woods R, Lowry P, Smith R. 2007. A placental clock

controlling the length of human pregnancy. Natural Medicine 1: 460–463.

Mock CJ. 1996. Climatic controls and spatial variation of precipitation in the western

United States. Journal of Climate 9: 1111—1125.

Page 20 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

21

Morafka DJ, Spangenberg EK, Lance VA. 2000. Neonatology of reptiles.

Herpetological Monographs 14: 353–370.

Munson SM, Webb RH, Belnap J, Hubbard JA, Swann DE, Rutman S. 2011. Forecasting climate change impacts to plant community composition in the

Sonoran Desert. Global Change Biology 18: 1083–1095.

Mysterud A, RØed KH, Øystein H, Yoccoz NG, Nieminen M. 2009. Age-related

gestation length adjustment in a large iteroparous mammal at northern latitude.

Journal of Animal Ecology 78: 1002–1006.

Norris DO. 2006.Vertebrate endocrinology. 4th

edn. San Diego, CA: Academic Press.

Notaro M, Mauss A, Williams JW. 2012. Protracted vegetation changes for the

American Southwest: combined dynamic modeling and the bioclimatic-envelope

approach. Ecological Applications 22: 1365–1388.

Ogutu JO, Piepho H-P, Dublin HT, Bhola N, Reid RS. 2011. Dynamics of births and

juvenile recruitment in Mara-Serengeti ungulates in relation to climate and land

use changes. Population Ecology 53: 195–213.

Olsson M, Shine R. 1998. Timing of parturition as a maternal care tactic in an alpine

lizard species. Evolution 52: 1861–1864.

Plard F, Gaillard J-M, Bonenfant C, Hewison AJM, Delorme D, Cargnelutti B, Kjellander P, Nilsen EB, Coulson T. 2012. Parturition date for a given female is

highly repeatable within five roe deer populations. Biology Letters (December

2012).

Packer C, Herbst L, Pusey AE, Bygott JD, Hanby JP, Cairns SJ, Mulder MB. 1988. Reproductive success in lions. In Reproductive success. Clutton-Brock TH

(eds.), pp. 363-383. Chicago, IL: The University of Chicago Press.

Parker JM, Spear SF, Oyler-McCance S. 2012. Natural History Notes. Crotalus

oreganus concolor (midget faded rattlesnake). Nursery aggregation.

Herpetological Review 43: 658-659.

Porter RH, Czaplicki JA. 1974. Shedding facilitates exposure learning in the garter

snake (Thamnophis sirtalis). Physiology and Behavior 12: 75–77.

Porter TA, Wilkinson GS. 2001. Birth synchrony in greater spear-nosed bats

(Phyllostomus hastatus). Journal of Zoology 253: 383–390.

Price AH. 1988. Observation on maternal behavior and neonate aggregation in the

western diamondback rattlesnake, Crotalus atrox (Crotalidae). The Southwestern

Naturalist 33: 370–373.

Page 21 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

22

Prival DB. 2008. Morphology, reproduction, and habitat use of a northern population of

banded rock rattlesnakes, Crotalus lepidus klauberi. In The biology

of rattlesnakes. Hayes WK, Beaman KR, Cardwell MD, Bush SP (eds.),

pp. 431–440. Loma Lind University Press, Loma Linda, California.

Reinert HK. 1992. Radiotelemetric field studies of pitvipers: data acquisition and

analysis. In: Biology of the pitvipers. JA Campbell & ED Brodie Jr (Eds.),

pp. 185–197. Tyler, TX: Selva.

Reiserer RS, Schuett GW, Earley RL. 2008. Dynamic aggregations of newborn sibling

rattlesnakes exhibit stable thermoregulatory properties. Journal of Zoology 274:

277-283.

Rock J. 2006. Delayed parturition: constraint or coping mechanism in a viviparous

gekkonid? Journal of Zoology 268: 355–60.

Roff DA. 2002. Life history evolution. Sunderland, MA: Sinauer Associates.

Rosen PC, Goldberg SR. 2002. Female reproduction in the western diamond-backed

rattlesnake, Crotalus atrox (Serpentes: Viperidae), from Arizona. Texas Journal

of Science 54: 347–356.

Ryan SJ, Knechtel CU. Getz WM. 2007. Ecological cues, gestation length, and birth

timing in African buffalo (Syncerus caffer). Behavioral Ecology 18: 635–644.

Schaller GB. 1972. The Serengeti lion. Chicago, IL: University of Chicago Press.

Schuett GW, EN Taylor, EA Van Kirk, and WJ Murdoch. 2004 a. Handling stress

and plasma corticosterone levels in captive male western diamond-backed

rattlesnakes (Crotalus atrox). Herpetological Review 35: 229-233.

Schuett GW, Grober MS, Van Kirk EA, Murdoch WJ. 2004 b. Long-term sperm

storage and plasma steroid profile of pregnancy in a western diamond-backed

rattlesnake (Crotalus atrox). Herpetological Review 35: 328–333.

Schuett GW, Repp RA, Hoss SK. 2011. Frequency of reproduction in female western

diamond-backed rattlesnakes (Crotalus atrox) from the Sonoran Desert of

Arizona is variable in individuals: potential role of rainfall and prey densities.

Journal of Zoology 284: 105–113.

Schuett GW, Repp RA, Amarello M, Smith CF. 2013. Unlike most vipers, female

rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy.

Journal of Zoology 289: 101–110

Page 22 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

23

Seigel RA, Ford NB. 2001. Phenotypic plasticity in reproductive traits: geographical

variation in plasticity in a viviparous snake. Functional Ecology 15: 36–42.

Seigel RA, Ford NB, Mahrt, LA. 2000. Ecology of an aquatic snake (Thamnophis

marcianus) in a desert environment: implications of early timing of birth and

geographic variation in reproduction. American Midland Naturalist 143:

453–462.

Setser, K, Mocino-Deloya E, Pleguezuelos JM, Lazcano D, Kardon A. 2010. Reproductive ecology of female Mexican lance-headed rattlesnakes. Journal of

Zoology 281: 175–182.

Shine R. 2003. Reproductive strategies in snakes. Proceedings of the Royal Society B

270: 995–1004.

Shine R. 2005. Life-history evolution in reptiles. Annual Review of Ecology, Evolution,

and Systematics 36: 23–46.

Shine R, Olsson M. 2003. When to be born? Prolonged pregnancy or incubation

enhances locomotor performance in neonatal lizards (Scincidae). Journal of

Evolutionary Biology 16: 823–832.

Smith CF, Schuett GW, Hoss SK. 2012. Reproduction in female copperhead snakes

(Agkistrodon contortrix): plasma steroid profiles during gestation and post-birth

periods. Zoological Science 29: 273–279.

Smith R. 2007. Parturition. New England Journal of Medicine 356: 271–283.

Stearns SC. 1992. The evolution of life histories. New York, NY: Oxford University

Press.

Taylor EN, DeNardo DF. 2005. Reproductive ecology of western diamond-backed

rattlesnakes (Crotalus atrox) in the Sonoran Desert. Copeia 2005: 152–158.

Taylor EN, DeNardo, DF. 2011. Hormone and reproductive cycles in snakes. In

Hormones and reproduction in vertebrates, vol. 2, reptiles: 355–372. Norris, D.O.

& Lopez, K.H. (Eds.). San Diego, CA: Academic Press.

Tu MC, Lillywhite HB, Menon JG, Menon GK. 2002. Postnatal ecdysis establishes the

permeability barrier in snake skin: new insights into barrier lipid structures.

Journal Experimental Biology 205: 3019–3030.

Visser ME, Caro SP, van Oers K, Schaper SJ, Helm B. 2010. Phenology, seasonal

timing and circannual rhythms: towards a unified framework. Philosophical

Transactions of the Royal Society B: 3113–3127.

Page 23 of 27



123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

For Peer Review

24

Wada H. 2008. Glucocorticoids: mediators of vertebrate ontogenetic transitions. General

and Comparative Endocrinology 156: 441–453.

Wapstra E, Uller T, While GM, Olsson M, Shine R. 2010. Giving offspring a head

start in life: field and experimental evidence for selection on maternal basking

behaviour in lizards. Journal of Evolutionary Biology 23: 651–657.

Warkentin KM, Caldwell MS. 2009. Assessing risk: embryos, information, and escape

hatching. In Cognitive ecology II: the evolutionary ecology of learning, memory,

and information use: 177–200. Dukas R, Ratcliffe J, (Eds.). Chicago, IL:

University of Chicago Press.

Weiss G. 2000. Endocrinology of parturition. Journal of Clinical Endocrinology and

Metabolism 85: 4421–4425.

Weiss JL, Overpeck JT. 2005. Is the Sonoran Desert losing its cool? Global Change

Biology 11: 2065– 2077.

West-Eberhard MJ. 2003. Developmental plasticity and evolution. New York, NY:

Oxford University Press.

While GM, Jones SM, Wapstra E. 2007. Birthing asynchrony is not a consequence of

asynchronous offspring development in a non-avian vertebrate, the Australian

skink Egernia whitii. Functional Ecology 21: 513–519.

Woodhouse CA, Meko DM, MacDonald GM, Stahle DW, Cook ER. 2010. A

1,200-year perspective of 21st century drought in southwestern North America.

Proceedings of the National Academy of Sciences USA 107: 21283–21288.

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Table 1. Rainfall data for Suizo Mountains (29 Jul – 14 Sep, J-S) and Tucson

International Airport (TIA) from 2003 to 2007. All rainfall values are in cm.

Parenthetical values = frequency of discrete rainfall events. See text for further details.

________________________________________________________________________

Rainfall (cm)

______________________

Year Jul Aug Sep Total J-S Rain Suizo (annual) TIA (annual)

________________________________________________________________________

2003 2.5 (1) 9.6 (7) 5.3 (1) 17.4 (9) 29.4 25.5

2004 0.0 (0) 4.1 (2) 2.5 (1) 6.6 (3) 29.7 19.3

2005 0.3 (1) 3.3 (4) 0.8 (1) 4.4 (6) 15.9 24.3

2006 4.6 (2) 5.3 (5) 4.6 (3) 14.5 (10) 28.9 29.9

2007 0.0 (0) 13.2 (7) 0.5 (1) 13.7 (8) 48.2 24.8

All 7.4 (4) 35.5 (25) 13.7 (7) 56.6 (36) 152.1 123.8

Mean 1.5 (0.8) 7.1 (5) 2.7 (1.4) 11.3 (7.2) 30.4 24.8

_______________________________________________________________________

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Table 2. Births and rain-days randomization analysis (see text for details) for the 21 adult female Crotalus

atrox in our study. Births (n = 38 litters) occurred from 2003 to 2007. Parenthetical values = litter size

(number of progeny). Number of litters is denoted in the year column. ID = subject identification. P-values

were generated by comparing mean rain-days to a random distribution of 10 000 mean rain-days.

Significant p-values are bold. See Fig. 1 and Table 1.

Mean Rain-days

___________________________________

Year ID Birth date Rain-days Observed Random p-value

2003 039 8-15 (4) 0 0.875 1.884 0.069

n = 8 014 8-19 (2) 1

044 8-19 (3) 1

002 8-23 (5) 0

016 8-24 (?) 1

030 8-28 (3) 1

046 8-28 (3) 1

042 9-02 (4) 2

2004 001 8-15 (5) 0 4.750 4.405 0.613

n = 8 059 8-15 (4) 0

029 8-18 (?) 2

061 8-24 (?) 8

058 8-28 (4) -8

064 8-28 (?) -8

066 8-28 (?) -8

046 9-01 (3) -4

2005 066 8-21 (?) -1 1.429 2.247 0.095

n = 7 016 8-22 (3) 0

030 8-22 (?) 0

044 8-22 (1) 0

046 8-24 (1) 2

042 8-29 (3) -4

081 9-05 (2) 3

2006 047 8-07 (6) 0 1.444 1.420 0.482

n = 9 094 8-12 (3) -2

093 8-22 (2) 0

001 8-15 (4) 1

058 8-16 (9) 2

102 8-22 (2) 0

030 8-24 (7) 2

061 8-24 (1) 2

095 8-26 (?) 4

2007 016 8-05 (3) 0 0.333 1.953 < 0.001

n = 6 046 8-05 (4) 0

001 8-06 (3) 1

047 8-10 (3) 0

058 8-10 (3) 0

102 8-11 (2) 1

All Years 1.842 2.404 0.037

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Environmentally cued parturition in a desert rattlesnake, Crotalus atrox

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