Natural History of a Northern Population of Twin-Spotted Rattlesnakes, Crotalus pricei

Journal of Herpetology, Vol. 36, No. 4, pp. 598–607, 2002Copyright 2002 Society for the Study of Amphibians and Reptiles

Natural History of a Northern Population of Twin-SpottedRattlesnakes, Crotalus pricei

DAVID B. PRIVAL,1 MATTHEW J. GOODE, DON E. SWANN, CECIL R. SCHWALBE,2 AND

MICHAEL J. SCHROFF

School of Renewable Natural Resources, 104 Biosciences East, University of Arizona, Tucson, Arizona 85721, USA

ABSTRACT.—The twin-spotted rattlesnake (Crotalus pricei) is a small-bodied pitviper that has receivedlittle attention in the literature to date. The species reaches the northern limit of its range in southeasternArizona, where it inhabits higher elevations than any of the state’s 10 other rattlesnake species. During 1997–2000, we captured, measured, and marked 127 C. pricei in Arizona’s Chiricahua Mountains between 2530and 2900 m elevation. We also used radiotelemetry to track the movements of 16 C. pricei in the study areaduring 1997–1998. Mean (6 SE) snout–vent length of C. pricei was 387.8 6 8.3 mm (range 5 168–572), andmean mass was 53.5 6 3.3 g (range 5 3.6–188.5). Based on fecal analyses, lizards constituted the bulk ofprey (74%), but the diet of C. pricei also included mammals, birds, and a conspecific. Mating was concentratedin August and early September and parturition took place during late July and August. Mean number ofembryos was 3.94 6 0.34 (range 5 1–6) and female reproduction appeared biennial or less frequent. Basedon shed and growth rates, female C. pricei develop embryos at 4–5 years of age. Gravid females maintainedwarmer body temperatures relative to substrate temperature than nongravid females or males, presumablyby spending more time basking than other snakes. Radiotelemetry revealed that movement patterns variedfrom year to year, as males moved over six times farther per week during the 1998 monsoon season (Julyto September) than during the 1997 monsoon season. Additionally, use of talus slopes by males decreasedduring 1998. During dry years, such as 1998, males may be forced off talus into cooler microclimates whereresources are less concentrated than on talus.

Although twin-spotted rattlesnakes (Crotaluspricei) were first described over 100 years ago(Van Denburgh, 1895), they have since gonelargely unstudied. Although limited informa-tion about diet (e.g., Klauber, 1972; Gumbartand Sullivan, 1990), reproduction (e.g., Maha-ney, 1997; Goldberg, 2000) and toxicity (Mintonand Weinstein, 1984) can be found in the liter-ature, little effort has been made to obtain eco-logical data beyond that provided by occasionalobservations.

In the U.S., C. pricei is restricted to four dis-junct mountain ranges in southeastern Arizona(Chiricahua, Huachuca, Pinaleno, and SantaRita Mountains). Its range extends souththrough the Sierra Madre Occidental and SierraMadre Oriental in seven Mexican states (Arm-strong and Murphy, 1979; Campbell and Lamar,1989). The Arizona and Sierra Madre Occidentalpopulations in Mexico comprise one of the twosubspecies, Crotalus pricei pricei. These ambushpredators rarely exceed 600 mm in length andare usually associated with rocky slopes (espe-cially talus), ridges, and occasionally canyonbottoms between 1860 and 3050 m (Van Den-

1 Corresponding Author. E-mail: [email protected]

2 Present address: U.S. Geological Survey, SonoranDesert Field Station, 125 Biosciences East, Universityof Arizona, Tucson, Arizona 85721, USA

burgh, 1922; Lowe, 1964). The biotic communi-ties associated with C. pricei are Madrean Mon-tane Conifer Forest and Madrean EvergreenWoodland (Brown, 1994; Pase and Brown, 1994).

Crotalus pricei is interesting from an ecologicaland evolutionary perspective, because it is oneof the smallest rattlesnakes, inhabits higher el-evations than any of Arizona’s 10 other rattle-snake species, and may be morphologically andecologically similar to early rattlesnakes(Greene, 1997). Conservation of populations ofC. pricei in Arizona has been an issue for over30 years (Kauffeld, 1969). Because of the limiteddistribution of the species within the U.S. and athreat posed by collection for the pet trade (Pri-val, 2000), C. pricei is protected by state law inArizona. Although illegal collection for the pettrade may currently be the greatest threat to C.pricei populations in the United States, other po-tential threats include mining, logging, grazing,recreational and other development, and climatechange. Global warming in particular may ul-timately pose a significant threat to Arizona’spopulations because the species is currentlyfound only at the highest elevations of themountain ranges it inhabits. Information aboutthe life history of these snakes will be essentialfor any future conservation efforts (Dodd, 1993).We studied populations of C. pricei in Arizona’sChiricahua Mountains to learn about morphol-ogy, diet, movement patterns, and reproduction.

599TWIN-SPOTTED RATTLESNAKE ECOLOGY

MATERIALS AND METHODS

Study Sites.—The Chiricahua Mountains arelocated near the southeastern corner of Arizonain Cochise County and reach an elevation of2986 m. Typically, slightly more than half (52%)of annual precipitation falls during a summermonsoon season characterized by localized,high-intensity thunderstorms from July to Sep-tember (Adams and Comrie, 1997). Most addi-tional precipitation results from widespread,low-intensity winter storms (National WeatherService, unpubl. data). Rustler Park Ranger Sta-tion, located near the study sites at 2560 m, re-ceives an average of 760 mm of precipitation peryear (Bennett et al., 1996).

We concentrated our efforts on four exposedtalus slides (Sites A, B, C, and D) within theMadrean Montane Conifer Forest vegetation as-sociation (Pase and Brown, 1994). One of thesites (Site A) is a well-known locality for thespecies. We selected other sites by investigatingunvegetated areas marked on topographic maps(1:24,000) and visible in aerial photographs.Vegetation at one of the sites (Site B) was burnedseverely during a wildfire in 1994. Study sitesranged in elevation from 2530–2900 m, and talusarea at each site ranged from 0.7–3.3 ha. SitesA and B faced south, whereas Sites C and Dfaced west.

Capture Methodology.—Searches involved tra-versing talus, primarily during daylight hours.We spent 340 person-hours searching for snakesduring 1997 and 517 person-hours during 1998,primarily during July to September. We alsospent 170 person-hours searching for snakesover five days in late July to early August 1999at Site A and 195 person-hours searching overfour days in late July 2000 at Site A.

We marked 127 C. pricei during the study, in-cluding 83 snakes at Site A, 27 at Site B, 12 atSite C, and 5 at Site D. We recaptured snakes on72 occasions. We captured C. pricei by hand us-ing welding gloves or forceps, and marked themuniquely with Passive Integrated Transponders(PIT tags; Destron-Fearing Corp., South St. Paul,MN). In addition, we painted up to three rattlesegments of each snake with a unique colorcode to facilitate visual identification of individ-uals and to enable us to determine the numberof sheds between captures. We measured tem-peratures at 1.5 m, 0.5 cm, and substrate levelat every capture and observation site.

Morphology and Growth.—We measured snout–vent length (SVL), tail length, mass, and othermorphological characteristics of all snakes cap-tured. After reviewing the data visually, we de-termined that all datasets met the requirementsfor parametric tests except for mass, which wasskewed right. Therefore, we used a natural log

transformation to normalize the mass data forall analyses (Zar, 1996; JMP IN 3.2.1, SAS Insti-tute, Inc., Cary, NC). However, we report non-transformed mean mass in our results. Forsnakes captured more than once, we selectedone capture event at random for most analysesbut only used data from the initial capture forradiotelemetered snakes.

We determined sex by cloacal probing (Lasz-lo, 1975). We were unable to ascertain the sex ofsome snakes based on their small size. The larg-est snake for which we were unable to confi-dently determine sex measured 301 mm SVL.Therefore, we excluded snakes measuring # 301mm SVL from analyses of sex-based differences.We calculated mean growth rates for recapturedsnakes, excluding snakes with fewer than 14days between recapture events. We assessed dif-ferences in growth rate as a function of sex, site,days between recapture events, and initial SVLusing multiple regression. Although sex and siteare categorical variables, we were able to usemultiple regression for this analysis by convert-ing these variables to indicator variables (Ram-sey and Schaefer, 1997). We used a t-test to com-pare growth rates of snakes with and withoutradiotransmitters that had snout–vent lengths ofat least 430 mm, the size of the smallest snakethat carried a radiotransmitter. Using recapturedata from different years, we calculated themean number of sheds per year.

Diet and Reproduction.—We palpated snakesfor food boli on 134 occasions during 1998–2000.We obtained fecal samples when snakes defe-cated while held individually for processing. Weidentified prey by using a dissecting microscopeto compare samples with specimens of animalsknown to occur in the area, based on results oflive trapping, observations, or historical records.

We palpated 44 adult female snakes for em-bryos during 1998–2000. We used logistic re-gression to determine whether number of em-bryos was related to SVL. Although Klauber(1972) reported a gravid female measuring 301mm total length, the smallest gravid C. priceicaptured during this study measured 364 mmSVL. Therefore, snakes smaller than 364 mmSVL were considered to be juveniles. We useddata obtained from snake palpation, radiotelem-etry (movement patterns), and observations ofmating behavior and paired males and femalesto describe the reproductive cycle of C. pricei inthe Chiricahuas. Two snakes involved in the ra-diotelemetry study were not identified by pal-pation as being gravid, possibly because theywere palpated before embryos were largeenough to be detectable, but we believe theywere gravid based on movement patterns andsubstantial weight loss. These two snakes werenot included in the gravid category for statistical

600 D. B. PRIVAL ET AL.

FIG. 1. Size distribution of 127 Crotalus pricei (60male, 43 female, 24 undetermined sex) from the Chir-icahua Mountains, Arizona, 1997–2000.

tests other than those related to movement pat-terns and body temperature.

Movement Patterns and Habitat Use.—We sur-gically implanted temperature-sensitive radi-otransmitters with whip antennas (Holohil Sys-tems, Ltd., Carp, ON, Canada) into 16 snakesduring 1997–1998. Most were 1.8-g transmitterswith an expected battery life of four months (N5 13), but some were 3.3-g transmitters de-signed to last six months (N 5 3). Surgical im-plantation of radiotransmitters followed Reinertand Cundall (1982) with some modifications(see Prival, 2000).

In 1997, we tracked seven males and two fe-males. In 1998, we tracked five males and fivefemales. One male was tracked for 13 months;most other snakes were tracked for less thanfour months each. A TR-4 receiver (Telonics,Inc., Mesa, AZ) and a two-element flexible Yagiantenna were used to locate snakes. We locatedsnakes once per week between July and mid-October and once per month during other timesof the year. We used the radiotransmitter signalto calculate body temperature each time a snakewas located. We also measured temperatures at1.5 m, 0.5 cm, and substrate level with a ther-mometer. Multiple regression was used to assessdifferences in body temperature as a function ofsex, site, month, year, time, and substrate tem-perature (Ts). We converted categorical variablesto indicator variables for this analysis (Ramseyand Schaefer, 1997).

We measured distances and angles betweensnake locations with a tape measure and/orrangefinder and a compass and clinometer. Weused Pitter Plotter 1.2 (Concentrics Company,Santa Fe, NM), a cave-mapping program, to es-timate distances between points. Home-rangesize was estimated with Calhome 1.0 (J. Kie, Pa-cific Southwest Research Station, USFS), usingthe 100% minimum convex polygon model.

The number of snakes with radiotransmittersvaried over time. The largest number of snakeswas tracked between July and September ofeach year. Analyses of home ranges and move-ment patterns, therefore, only involve observa-tions made during those months unless other-wise stated. All means are reported 6 1 SE.

RESULTS

We marked 51 snakes in 1997, 58 in 1998,eight in 1999, and 10 in 2000. Most snakes (93%)were captured between July and September,during which 92% of the total search effort tookplace.

Morphology and Growth.—SVL for all C. priceicaptured averaged 387.8 6 8.3 mm (range 5168–572) (Fig. 1). Mean SVL of males and fe-males did not differ (male 5 423.2 6 8.5 mm,female 5 419.7 6 10.1, t 5 0.26, df 5 101, P 5

0.79). However, only males were longer than 540mm (N 5 3). Mass of all snakes captured aver-aged 53.5 6 3.3 g (range 5 3.6–188.5). Meanmass of males and females did not differ (male5 67.2 6 4.5 g, female 5 58.0 6 5.3, t 5 0.44,df 5 101, P 5 0.66). However, only male snakesexceeded 119 g (N 5 8). Overall, 58.3% (N 5 60)of snakes . 301 mm SVL were males, indicatingthat the population did not differ from a 1:1 sexratio (x2 5 2.8, df 5 1, P 5 0.09). Sixty-threepercent of all snakes captured were adults. Theratio of tail length to total length differed be-tween the sexes (male 95% CI 5 0.0856–0.0888,female 95% CI 5 0.0680–0.0708, t 5 15.9, df 5101, P , 0.0001). However, there was some over-lap (male range 5 0.0656–0.0995, female range5 0.0590–0.0816). The length-mass relationshipfor C. pricei was highly significant (mass 5e(0.2653 1 0.00882 SVL); t 5 44.2, df 5 125, P , 0.0001,r2 5 0.94).

Of the variables tested (sex, site, days betweenrecaptures, and initial SVL), growth rate(DSVL/day) was related only to initial SVL (ini-tial SVL: F3,60 5 11.6, P 5 0.0012, r2 (whole-mod-el) 5 0.19). Juvenile snakes grew faster thanadult snakes in terms of DSVL/day (t 5 2.92, df5 67, P 5 0.0048) and DSVL/shed (t 5 2.65, df5 39, P 5 0.012; Table 1). The presence of ra-diotransmitters did not affect C. pricei growthrate (t 5 0.62, df 5 35, P 5 0.54). On average,C. pricei shed 1.76 6 0.14 times per year (N 528). If the estimated growth and shed rates areaccurate, C. pricei become large enough to de-velop embryos (364 mm SVL) at four or fiveyears of age.

Diet.—Food boli were detected in 36% of C.pricei palpated, including 44% of males (N 5 66palpated) and 25% of females (N 5 56; x2 5 4.8,df 5 1, P 5 0.029). We found food boli in 29%of adults (N 5 97) and 54% of juveniles (N 537; x2 5 7.4, df 5 1, P 5 0.0066). During the


TABLE 1. Crotalus pricei growth rates (mean 6 SE). Snakes , 364 mm SVL were considered to be juveniles.

All snakes N Juveniles N Adults N

D SVL (mm)/dayD SVL (mm)/shedD mass (g)/dayD mass (g)/shed

0.063 6 0.0357.26 6 3.83

20.019 6 0.0272.06 6 1.92

69416841

0.253 6 0.07325.1 6 7.62

0.085 6 0.0585.72 6 4.09

149

149

0.015 6 0.0372.24 6 4.04

20.045 6 0.0301.03 6 2.17

55325432

FIG. 2. Prey distribution in Crotalus pricei fecalsamples (N 5 31).

TABLE 2. Reproductive condition of recapturedCrotalus pricei in the Chiricahua Mountains, Arizona,1998–2000. G 5 Gravid. NG 5 Not gravid. ? 5 Notcaptured.

Snake ID 1998 1999 2000

13750D83683CE42

GGGG

NG

?NGNGNGG

G???

NG

monsoon months, adult males ate most often inJuly (55% with food boli; N 5 20 palpated) andSeptember (50%; N 5 10), and least often in Au-gust (14%; N 5 14; x2 5 6.1, df 5 1, P 5 0.048).

Thirty-three fecal samples were collected andanalyzed, 31 of which contained identifiableprey items (Fig. 2). We found more than onetype of prey in four samples. We found lizardscales in 23 samples (74%). All of the scaleswere Sceloporus, and at least eight samples con-tained scales of Sceloporus jarrovii. Lizard speciescould not be determined with certainty for theother 15 samples.

One fecal sample contained snake scales anda rattle. The rattle size and shape and the col-oration of the scales matched more closely withspecimens of C. pricei than with specimens ofother montane rattlesnakes from southeasternArizona (C. lepidus, C. molossus, and C. willardi).The rattle consisted of one segment and a but-ton. A comparison of the ventral scales in thesample with C. pricei specimens suggests thatthe prey snake measured approximately 225mm SVL. According to the length-mass curve,a snake of this size would weigh about 12.4 g.This sample was obtained on 28 September 1998from a male snake measuring 466 mm SVL andweighing 70 g.

We found hair in nine samples (29%). Bonesin two of these samples were identified as Per-omyscus. Hair from another sample was identi-fied as Neotoma, most likely a Mexican woodrat(Neotoma mexicana). We could not identify othersamples to genus. We found feathers in twosamples (6.5%). The color gradation of the feath-

ers and the rachis color in one of the samplessuggest the prey item was a canyon wren (Cath-erpes mexicanus).

Seventy-five percent of the 24 samples ob-tained from snakes captured on talus containedSceloporus, whereas 25% contained mammals.Off talus, Sceloporus accounted for 57% of theprey of the seven snakes producing samples,with mammals comprising the other 43%. Bothbird samples and the C. pricei prey were ob-tained from snakes found on talus.

Reproduction.— No embryos were detected be-fore 9 June or after 1 September. We found mostgravid snakes in July and August. During thosemonths, 50% of 36 captured adult females weregravid. Mean number of embryos detected pergravid snake was 3.94 6 0.34 (N 5 18, range 51–6).

Gravid snakes averaged 430 6 8.6 mm SVL(range 5 364–500), whereas adult nongravid fe-males captured during July and August aver-aged 442 6 12.0 mm (range 5 400–534), indi-cating that adult body size was unrelated to re-productive activity (t 5 0.79, df 5 28, P 5 0.62).In addition, there was no relationship betweenbody size and number of embryos (x2 5 12.8,df 5 1, P 5 0.17).

Between 1998 and 2000, five females werepalpated for embryos in July or August in morethan one year. None of these females was gravidin consecutive years (Table 2). Both snakes cap-tured in alternate years were in the same repro-ductive condition in both years (one gravid, onenongravid).

Male and female snakes were observed inclose proximity to each other (ø 1 m) on 13 oc-casions between 11 August and 21 September1997, and between 9 August and 13 September


TABLE 3. Distance moved and home-range size for radiotelemetered Crotalus pricei, July–September (mean6 SE). N 5 3 for 1998 female home range.

1997 (N 5 4 males, 1 female)

Distance moved(m/week)

Home range(ha)

1998 (N 5 5 males, 4 females)

Distance moved(m/week)

Home range(ha)

MalesFemales

14.0 6 6.242.5

0.16 6 0.100.83

87.8 6 11.019.7 6 7.1

2.29 6 0.880.20 6 0.011

1998. Courtship was observed on 21 August1997 between a 492-mm SVL male and a 466-mm SVL female. The behavior was character-ized by constantly intertwined tails and cyclesof about 2.5 min of chin-pressing and tongue-flicking by the male, followed by 4 sec of vig-orous tail movement and 20 sec of motionless-ness from 0851–0949 h. We could not determinewhether copulation occurred.

A 441-mm SVL C. pricei gave birth to fourneonates sometime between 2100 h 16 Augustand 1430 h 17 August 1998 while being de-tained temporarily for processing (mean SVL ofneonates 5 168.8 6 2.32 mm, range 5 163–173;mean mass 5 4.4 6 0.04 g, range 5 4.3–4.5). Allfour neonates appeared to be healthy and alert.The female weighed 66.5 g prepartum and 42.5g postpartum.

A 390-mm SVL female gave birth to three ne-onates during and following processing on 28–30 July 2000 (mean SVL of neonates 5 155.0 64.00 mm, range 5 151–163; mean mass 5 4.1 60.19 g, range 5 3.8–4.4). The first neonate wasstillborn; the other two were lethargic and cov-ered by a flaky layer of dead skin. The samefemale also produced an undeveloped ovumand was carrying at least two more embryos orova when released on 30 July. Prepartum massof this female was not obtained; she weighed 57g prior to release.

Based on movement patterns and substantialdecreases in mass, we believe three radiotele-metered snakes gave birth during late August1998, although these neonates were never locat-ed. The four gravid snakes measured before andafter parturition lost 32.4 6 5.4 g (range 5 22.5–44.0 g), representing an average weight loss of39.4 6 3.4% (range 5 31.7–47.3%).

Other neonate snakes (defined here as snakeswith a rattle consisting of only a prebutton orbutton) were captured on 15 September 1997(185 mm SVL, 3.6 g), 22 September 1997 (200mm, 7.1 g), 30 September 1997 (176 mm, 6.1 g),and 29 July 2000 (168 mm, 3.8 g).

Movement Patterns and Habitat Use.—Males (N5 9) moved an average of 55.0 6 14.4 m/weekand females (N 5 5) moved 24.2 6 7.1 m/weekduring the monsoon months (July to September;t 5 1.5, df 5 12, P 5 0.16; Table 3). Variation

was high within each sex (male range 5 2.6–115.4 m/week, female range 5 4.7–42.5 m/week).

On average, males moved 73.8 6 13.7 m/week farther in 1998 than 1997 during the mon-soon months (t 5 5.4, df 5 7, P 5 0.001) (Table3). One male was monitored over most of bothmonsoon seasons. He moved almost four timesfarther per week in 1998 than in 1997.

Movement patterns of gravid females trackedbefore and after parturition in 1998 (N 5 3)were characterized by little movement (# 3.2m/week) between mid-July and the time we be-lieve they gave birth at the end of August, fol-lowed by greatly increased movement in Sep-tember (mean: 73.1 6 30.4 m/week, range 538.5–133.6 m/week). The nongravid femalemoved 53.5 m/week between 24 July and 29August 1997, and 30.0 m/week between 29 Au-gust and 30 September.

During the monsoon months, mean homerange size for males (N 5 9) was 1.37 6 0.60 ha(range 5 0.0038–5.34) and for females (N 5 4)was 0.36 6 0.16 ha (range 5 0.18–0.83; t 5 0.18,df 5 11, P 5 0.86). Home range size of malesdiffered in 1997 (N 5 4) and 1998 (N 5 5; t 53.5, df 5 7, P 5 0.010; Table 3). The nongravidfemale monitored in 1997 had a substantiallylarger home-range size during the monsoonthan the gravid females tracked in 1998.

Home range of the male monitored duringmost of the monsoon season in both years wasover 12 times larger in 1998 than in 1997. Hishome range over the entire 13 months he wastracked was 14.7 ha. He did not revisit any ofhis 1997 locations in 1998, and his home rangesduring the two monsoon seasons did not over-lap.

Radiotelemetered males differed in use of ta-lus during the monsoon months between years(t 5 2.4, df 5 7, P 5 0.044). In 1997, four maleswere found on talus 87.5 6 9.5% of the time(range 5 60–100%), whereas in 1998, five malesspent only 44.5 6 13.6% of their time on talus(range 5 0–76.9%). The male tracked duringboth monsoon seasons was always found on ta-lus slopes in 1997 but never in 1998.

Radiotelemetered females varied in their useof talus while gravid in July and August. Three


FIG. 3. Relationship between body temperatureand substrate temperature for Crotalus pricei. The linerepresents body temperature 5 substrate temperatureand can be used to examine how C. pricei body tem-perature varied from surface temperature.

gravid females were found on talus 33%, 75%,and 100% of the time in 1998, whereas the singlenongravid female tracked during that period in1997 was observed on talus 40% of the time.

Body Temperatures.—A total of 198 body tem-peratures were obtained from 15 male, fivegravid female, and four nongravid femalesnakes. One hundred sixty of these tempera-tures were obtained during the monsoon sea-son. Mean body temperature during this seasonwas 26.1 6 0.468C (range 5 12.0–39.08C). Dur-ing the monsoon season, body temperature wasrelated to substrate temperature (Ts) and sex (Ts:F5,152 5 94.8, P , 0.0001; sex: F5,154 5 9.8, P 50.0022; r2 (whole-model) 5 0.50). Female (gravidand nongravid) body temperatures were 4.49 60.918C higher than male body temperatures (t 54.95, df 5 158, P , 0.0001).

During all months, body temperatures of C.pricei ranged from 5–398C, but only rarelydropped below 108C or exceeded 358C (Fig. 3).On average, body temperature of all snakes dur-ing the monsoon months was 1.59 6 0.428Chigher than Ts (paired t-test: t 5 3.79, df 5 157,P 5 0.0002). Mean body temperature of gravidfemales was 4.64 6 1.158C higher than Ts,whereas mean body temperature of nongravidfemales and males was closer to Ts (1.11 60.948C and 0.97 6 0.508C, respectively F2,151 55.14; P 5 0.0069). However, the difference be-tween Ts and air temperature (T at 1.5 m) wassimilar at gravid female, nongravid female, andmale snake locations (F2,151 5 2.19; P 5 0.12).

DISCUSSION

Growth.—Juvenile C. pricei grew significantlyfaster than adults. This finding is consistentwith studies of other rattlesnake species (e.g.,Macartney et al., 1990; Beaupre et al., 1998).Kauffeld (1943b) reported a mean growth rateof 0.73 mm/day for the first 135 days in the

lives of five C. pricei neonates fed in captivity.These snakes likely grew faster than wild snakesand much faster than we estimated for juveniles(0.25 mm/day). Neonate growth may be partic-ularly rapid. Adults grew little over the courseof the study, and radiotransmitters did not seemto affect growth rate.

In most rattlesnake species, adult males tendto be larger than adult females (Klauber, 1972).This phenomenon is common in snake speciesthat exhibit male combat (Shine, 1993). Al-though male C. pricei attained a larger maxi-mum size than females, the mean body size dif-ference between sexes was not pronounced inour study.

One possible explanation for this apparentlack of large males is the relatively short activeseason at the high elevations inhabited by C. pri-cei. In a well-studied population of Crotalus vir-idis viridis in Wyoming, both sexes were similarin body size, even though males engage in com-bat (Graves and Duvall, 1990). These male C. v.viridis may remain small because they devoteabout half of the short active season to findingfemales instead of finding food (Duvall andBeaupre, 1998). Our data indicate that adultmale C. pricei eat much less often in August thanin July or September, presumably because theyconcentrate on searching for females in August.Therefore, in areas in which the active season isrelatively short because of thermal constraints,male rattlesnakes of some species, such as C. pri-cei and C. v. viridis, may typically remain assmall as females despite selection pressure forlarge size because of combat.

Diet.— On several occasions, we observed C.pricei adjacent to rocks during the day in thesame S-shaped hunting posture as has been de-scribed for C. horridus (Brown and Greenberg,1992) and C. lepidus (Beaupre, 1995a). We did notfind evidence of an ontogenetic shift in preypreference in C. pricei. However, juveniles weremore likely to have eaten recently than adultsnakes during the summer, possibly becauseadults devote time to reproduction during thisperiod.

Lizards were previously identified as the pri-mary food item for C. pricei (Amaral, 1927). Sub-sequent field observations in southeastern Ari-zona reported S. jarrovii as the most frequentprey (Gloyd, 1937; Kauffeld, 1943a; Woodin,1953). An analysis of nine C. pricei specimensalso suggested that their diet was comprisedprimarily of lizards, including S. jarrovii (Klaub-er, 1972). The only other lizard species reportedtaken by C. pricei is a single crevice spiny lizard(Sceloporus poinsettii; Armstrong and Murphy,1979).

Prey other than lizards are rarely mentionedin the literature. An adult C. pricei disgorged a


‘‘field mouse’’ in the Pinaleno Mountains, Ari-zona (Klauber, 1972). The role of invertebratesin the diet of C. pricei is unclear, because it isdifficult to determine whether arthropod exo-skeletons found in feces represent insects eatenby the snakes themselves or by their insectivo-rous lizard prey. However, other prey remainswere always present when arthropod exoskele-tons were found, suggesting that the latter sce-nario is likely. Centipedes (Scolopendra) are animportant prey item for the other two small-bodied montane rattlesnakes found in Arizona,Crotalus willardi and C. lepidus (Rubio, 1998). NoScolopendra parts were found in Crotalus priceifecal samples. However, no Scolopendra were ob-served at the study sites. Crotalus pricei havebeen observed preying on yellow-eyed junconestlings (Junco phaeonotus) in the Chiricahuason three occasions (Gumbart and Sullivan,1990). Yellow-eyed juncos are ground-nestingbirds common at high elevations in the range.

Some have speculated that C. pricei are forcedto live in areas with abundant lizard popula-tions because the neonate snakes are too smallto eat rodents (Klauber, 1972). However, mam-mal hairs found in a very small snake (SVL 5240 mm, mass 5 7.6 g) indicate that even youngC. pricei can take mammalian prey when the op-portunity arises. The ability of small rattle-snakes to use proportionately large mammalianprey has been well documented (e.g., Graves,1991). In fact, small mammals seem to be amore important food source than previouslyrecognized. The canyon wren and unidentifiedbird remains in two of the samples provide fur-ther evidence that C. pricei diet is more diversi-fied than the limited literature suggests.

Cannibalism is a widespread phenomenon,occurring in almost all major vertebrate and in-vertebrate groups (Elgar and Crespi, 1992).Studies indicate that consumption of conspecif-ics is a constant, but small, part of the diet ofmany reptiles (Polis and Myers, 1985). Prior tothis study, cannibalism had been documentedin at least 191 reptile species (Mitchell, 1986).Crotalus pricei is the fourth rattlesnake species inwhich cannibalism has been documented out-side of captivity, joining the prairie rattlesnake(C. v. viridis; Gloyd, 1933; Klauber, 1972; Genter,1984), eastern massasauga (Sistrurus c. catenatus;Ruthven, 1911), and Colorado Desert sidewind-er (Crotalus cerastes laterorepens; Funk, 1965). Per-haps cannibalism is more common in rattle-snakes than previously acknowledged.

Reproduction.—Although female C. pricei be-gin developing embryos at the age of four orfive, they are presumably able to mate in thepreceding year at the age of three or four, a typ-ical age for sexual maturity in rattlesnakes(Keenlyne, 1978; Fitch and Pasani, 1993; Beaupre

et al., 1998). Typically, births are reported in theliterature for captive C. pricei that were impreg-nated while they were still in the wild. Partu-rition dates range from 20 May (Armstrong andMurphy, 1979) to 23 September (Keasey, 1969).However, most births occur in July (N 5 6; VanDevender and Lowe, 1977; Armstrong and Mur-phy, 1979) or August (N 5 3; Kauffeld, 1943b;Mahaney, 1997). Fully formed embryos havebeen found in snakes collected in late June (D.Prival, unpubl. data) and late August (Tanner,1985).

Determining the precise number of embryosin C. pricei by palpation is difficult, because em-bryos are often bunched closely together andmust be handled gently. Based on the 14 recordscited in the preceding paragraph and the‘‘healthy’’ parturition event from this study, themean litter size for C. pricei is 6.00 6 0.44 (range5 3–9). We do not know whether the lowermean estimated litter size reported in this study(3.94) represents a real difference between C.pricei from the Chiricahua Mountains andsnakes from other areas, or whether the lowermean size is because of sampling error.

Compared to most other rattlesnake species,C. pricei have relatively small litter sizes (Klaub-er, 1972). Compared to other small-bodied mon-tane rattlesnakes, however, C. pricei litter sizesare not unusual. Crotalus lepidus from Texas hada mean litter size of 3.6 (Beaupre, 1995a), where-as C. willardi from several ranges had a meanlitter size of 5.4 (Holycross and Goldberg, 2001).

Based on our observations and data from thisstudy, most mating occurred during Augustand early September. Females presumablystored sperm over the winter, a common strat-egy for rattlesnakes (Schuett, 1992; Almeida-Santos and Salomao, 1997). The reproductive cy-cle of C. pricei seems similar to that of C. lepidusin the Chiricahua Mountains (D. Prival, unpubl.data) and C. willardi in nearby ranges (Holycrossand Goldberg, 2001). In 1998, gravid C. priceiwere active until around mid-July, after whichthey remained in a small area for about sixweeks. On average, embryos and associated tis-sues comprised about 39% of the mass of gravidsnakes; thus, limited mobility may be one rea-son these snakes confined themselves to a smallarea during pregnancy.

Gravid snakes seemed to require warmerbody temperatures than other snakes. This phe-nomenon has been observed in studies of othersnake species (Graves and Duvall, 1993; Peter-son et al., 1993). The difference between sub-strate temperature and air temperature was sim-ilar between gravid female, nongravid female,and male snake sites, indicating that gravidsnakes do not inhabit warmer microclimatesthan nongravid snakes. However, gravid fe-


males had body temperatures substantiallyabove the substrate temperatures, whereas bodytemperatures of nongravid females and malesclosely approximated substrate temperatures,suggesting that gravid females spend more timebasking than nongravid snakes.

Half the female snakes palpated for embryoswere gravid, and none of four gravid femalespalpated in consecutive years were gravid bothyears, suggesting that females reproduce bien-nially. A histological study of museum speci-mens provided additional evidence that femaleC. pricei reproduce biennially (Goldberg, 2000).However, longer-term field studies are neededfor certainty (Blem, 1982). This evidence for bi-ennial or less frequent reproduction and smalllitter size suggests that C. pricei may not be ableto repopulate areas after a disturbance as quick-ly as some other rattlesnake species.

Movement Patterns.—Although there have beenfew comparative studies of snake movements,some indicate that gravid females tend to moveless than nongravid females, and that nongravidfemales move about as far as males (Macartneyet al., 1988). Our data are consistent with thesefindings.

Although our sample sizes were small, we ob-served a large difference in male activity be-tween years—males moved over six times far-ther per week in 1998 than 1997. The snake ex-hibiting the least movement in 1998 moved overtwice as far per week as the most mobile 1997snake. The coinciding habitat shift betweenthese two years, from predominantly talus in1997 to predominantly wooded areas in 1998,was also striking.

Reptile activity is often dictated by weatherconditions, and weather may be the proximatecause of yearly differences that we observed insnake movement. Approximately 30% more rainfell during the monsoon season in 1997 than in1998 near the study area at Chiricahua NationalMonument. Also, in 1997, 60% of the rain dur-ing those months fell in August, whereas in1998, over 75% fell in July.

Thus, August and September were much dri-er in 1998 than in 1997. The reduction of intenserains during those months in 1998 likely corre-sponded with a decrease in cloud cover. Thesunnier, drier weather in 1998 may have in-creased the talus surface temperature to a pointwhere snake activity on the talus was limited.This weather may have also affected prey avail-ability, as Sceloporus jarrovii population abun-dance indices at three sites indicated the lizardswere much less active in 1998 than in 1997 (Pri-val, 2000). Perhaps snakes moved off talus totake advantage of the cooler, more favorable mi-croclimates found in the vegetated areas sur-rounding the talus. The talus, with its relatively

high prey density and extensive cover, may at-tract C. pricei. When C. pricei are forced off talus,they become more dispersed; thus, males mayhave to move farther and more often to locatefemales or obtain food. In mottled rock rattle-snakes (C. l. lepidus), warmer environmentaltemperatures were found to reduce the amountof available foraging time, resulting in lowergrowth rates (Beaupre, 1995b). A higher restingmetabolic rate caused by warmer temperaturescould also reduce growth rates (Beaupre,1995b). Therefore, in drier, warmer summers,the advantages of leaving the talus (increasedactivity period, reduced resting metabolic rate)may outweigh the advantages of remaining ontalus (abundant cover, higher concentration ofpotential mates).

Acknowledgments.—We thank R. Steidl, S. Bon-ar, D. Turner, and J. Lovich for providing helpfulcomments on drafts of this manuscript. We alsothank field technician K. Schoenecker and the701 volunteers who assisted us in the field fortheir hard work. A. Holycross and C. Jones pro-vided important logistical support, G. Helbingof Coronado National Forest helped us obtainpermits, and R. Huerta, C. McCleave, B. Car-bajal, and R. Maze provided administrative as-sistance. Primary funding was provided by anInventory, Identification, Protection, and Man-agement (IIPAM) grant (I97040) from the Ari-zona Game and Fish Department (AGFD) Her-itage Fund. We received additional supportfrom T & E, Inc. and the University of ArizonaGraduate School. All animals were handled un-der AGFD Scientific Collecting Permits and anIACUC-approved protocol.

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Accepted: 18 February 2002.

Journal of Herpetology, Vol. 36, No. 4, pp. 607–614, 2002Copyright 2002 Society for the Study of Amphibians and Reptiles

Association between Breeding Cycle and Male Body Condition inHyla labialis

HORST LUDDECKE

Departamento de Ciencias Biologicas, Universidad de los Andes, A.A. 4976, Bogota, Colombia;E-mail: [email protected]

ABSTRACT.—During four consecutive years, I used a mark-recapture method to study the relationshipbetween breeding cycle and changes in male body condition in an Andean population of Hyla labialis. Theannual weather pattern consisted of a long unimodal rainy season from February to November and a shortdry season in December and January. A pronounced unimodal annual pattern in body condition was pos-itively correlated with the amount of local rainfall. The annual reproductive cycle began during the rainyseason in August or September, when males had high body energy reserves. Breeding activity ended inApril or May of the following year, when males were in poor body condition. Reproductive activity wasdivided into two breeding periods by a short reproductive recess during the dry season. The annual cycleended with a recovery period during the wettest months, when males regained their body condition whilebreeding activity ceased. Abundance of males and mated pairs was bimodal, with a high peak in Octoberduring the first breeding period and a lower peak in February during the second breeding period. Abun-dance was low during the driest and wettest months of the year. Individually marked males participatedin up to seven consecutive breeding periods. Males found repeatedly in the same breeding period had thelowest body condition. A male’s body condition declined as his time at the breeding aggregation increasedand improved during recovery periods. Although rainfall pattern seemed to influence the amount of breed-ing activity, body condition seemed to determine the onset and end of the annual breeding cycle.

Prolonged breeding activity occurs in manytropical anurans (Dixon and Heyer, 1968;Crump, 1974; Woolbright, 1983; Donnelly, 1989,1999) and may be sustained by males as long asbody energy reserves are sufficient (Bevier,1997; Moreira and Barreto, 1997). Energy re-serves may be used up by energetically costlycalling activity (Grafe et al., 1992; Wells et al.,1996), perhaps combined with reduced foragingactivity and food intake (Toft, 1980; Rodel,1995). Breeding activity also may be influencedby hormonal cycles (Obert, 1977; Cei et al., 1996)and climate (Beattie, 1985; Telford and Dyson,

1990; Rodel et al., 1995). In the tropics, anuranreproductive activity may be adjusted to localrainfall patterns (Jørgensen et al., 1986), partic-ularly in pond breeders (Dixon and Heyer, 1968;Aichinger, 1991; Gascon, 1991; Donnelly andGuyer, 1994).

Hyla labialis occur at high altitudes in the An-des of Colombia (Ruiz-Carranza et al., 1996;Luddecke, 1997), where sites are characterizedby a cold and wet climate with seasonal rainfall.It is a philopatric pond breeder with two pro-longed annual breeding periods, which are sep-arated by the rainiest months around midyear

608 HORST LUDDECKE

and by the driest months at the turn of the year(Luddecke, 1996). Although males may spendseveral months per year in or near the breedingponds, gravid females arrive unpredictably andenter the water mainly for oviposition (Lud-decke, 1997). Although potentially reproductivefemales may be encountered in any month ofthe year (Hunter and Valdivieso, 1962), most fe-males in the highlands spawn only once peryear (Luddecke, 1997). Adult male H. labialismay survive for at least five years under naturalconditions (Luddecke and Amezquita, 1999). Tocompare the reproductive cycle of male H. la-bialis with that of females, I used the body con-dition index (BCI; Hemmer and Kadel, 1972) ofindividually marked males from the same high-land population. The usefulness of this index asan indicator of reproductive disposition (Kuhn,1994; McCauley et al., 2000) was demonstratedin a long-term study estimating the reproduc-tive potential of female H. labialis (Luddecke,1995). I combined the information on body con-dition with information on animal abundanceand breeding phenology, to answer the follow-ing questions: (1) Are reproductive cycles andBCI-changes of males concurrent with localrainfall pattern? (2) Do males lose and gainbody condition according to their reproductiveactivity pattern?

MATERIALS AND METHODS

Study Area.—The field study was carried outin a highland valley at about 3500 m altitude inthe nature reserve Parque Nacional NaturalChingaza (48429N, 738489W) in the eastern An-des near Bogota, Colombia. The vegetation is ofthe paramo type (Monasterio and Vuilleumier,1986), generally open, low, and herbaceous (vander Hammen and Cleef, 1986) and dominatedby grasses, dwarf bamboo, and woolly plants.Extended over an area of about 300 3 500 mand about 60–200 m apart, six clusters of 4–12mostly permanent ponds each were scatteredalong the bottom of the valley and offered suit-able oviposition sites for H. labialis. The pondswere surrounded by large swampy areas wheremany small puddles formed during the rainyseason and were bordered by steep slopes withrocky outcrops.

Annual weather consists of a long unimodalrainy season from February to November. Rain-fall is highest in June and July, and the short dryseason extends from December to January. Ac-cording to an incomplete record (1952–2000) ofBogota’s water supply company, average annualrainfall is about 1830 mm. During the rainymonths it is usually very cloudy, windy, andcold. Occasional hail storms occur. Mean annualair temperature is about 78C, with about 28C dif-ference between the warmest (March) and the

coldest month (June). Daily air temperature fluc-tuations are generally large (3–188C), and occa-sional frosts may occur during clear nights inthe dry season (Sarmiento, 1986; Sturm andMora-Osejo, 1994; Dıaz et al., 1997).

Field Procedures.—From March 1989 untilApril 1993, at intervals of 1–2 weeks I made 181visits to the valley (1989: 39, 1990: 35, 1991: 45,1992: 53, 1993: 9 visits). Each time, I searchedthe area during daylight hours (about 0800–1400 h) by slowly walking across the terrain andlooking for frogs, usually with the help of oneor two students. All captured frogs weremarked individually by disc-clipping (Lud-decke and Amezquita, 1999). The SVL of eachfrog was measured on each capture to the near-est millimeter with vernier callipers while hold-ing the animal against a flat surface, and bodymass was determined with an OHAUS field bal-ance to the nearest 0.1 g. I used a body condi-tion index (BCI) to quantify and compare thesomatic condition of males. The index is a ratioof body mass and SVL (Hemmer and Kadel,1972), where BCI 5 body mass (mg)/cube ofSVL (cm). I identified males by SVL, body mass,and the presence of a nuptial pad on the firstfinger. Previously I showed that males are small-er than females (Luddecke, 2001). Males attainan average snout–vent length (SVL) of 51.3 62.5 mm (range 43–59 mm), and a body mass of10.4 6 1.7 g (range 5.5–17.1 g). Their averageBCI is 76.6 6 7.9 (range 50–113, N 5 620 indi-viduals). I determined the duration of eachbreeding period according to the occurrence ofamplectant pairs (Luddecke, 2001).

Statistical Analysis.—Data were processed us-ing StatView 512y (Brain Power Inc.) on a Mac-intosh computer. I present mean values 6 thestandard deviation (SD). Because many maleswere captured and measured repeatedly, anddata on body size and frog abundance are notindependent, I performed nonparametric testson untransformed data (Neave and Worthing-ton, 1988). I used Friedman two-way ANOVAsto test whether male body size and abundancechanged across the year. I used Spearman’s rankcorrelations to determine associations betweenthe amount of monthly rainfall, male and pairabundance, and male body size. I also used thistest to correlate recapture intervals with chang-es in BCI-values.

RESULTS

Male Breeding Phenology.—The average month-ly amount of local rainfall during the four-yearstudy period was correlated with the long-termrainfall pattern (rs 5 0.83, P 5 0.028, N 5 8; themonths July, September, November, and Decem-ber were excluded because of incomplete recentofficial records). Therefore, I used the average

609BREEDING CYCLE AND BODY CONDITION

FIG. 1. Top: Average monthly distribution of rain-fall from August to July calculated from an incompleterecord between 1952 and 2000 at a weather stationlocated about 5 km from the study site at Chingaza.Center: Cumulative monthly distribution of 2705 cap-tures (circles) of 788 male Hyla labialis (triangles) and132 mated pairs (squares). Bottom: Annual course ofrelative changes (percentage above and below popu-lational average, marked as zero) in SVL (dashed line),body mass (thin line) and BCI (thick line) of male H.labialis in the study population. Horizontal bars alongthe x-axis indicate location of breeding peaks (black)and maximum duration of breeding activity (stripes).

FIG. 2. Four-year record showing cyclic annualfluctuations in average male BCI (thick line) and maleabundance (thin line) in a highland population of Hylalabialis. The position of each year marks its beginning.Periods of reproductive activity are characterized byhigh male abundance and low BCI-values.

monthly values of the long-term rainfall recordfor subsequent statistical analyses. Overall, Junewas the wettest and December was the driestmonth in the unimodal rainfall distributionacross the year (Fig. 1 top). I marked 788 males,which were captured 2705 times. A total of 462(58.6%) males were recaptured on average 3.66 3.5 times (range 5 1–24 times). Males expe-rienced cyclic annual fluctuations in abundance

and body condition (Fig. 2). Overall, BCI tendedto be high when male abundance was low (rs 520.287, P 5 0.045, N 5 50 months).

The overall annual abundance of males fol-lowed a bimodal seasonal course with signifi-cant differences between highest and lowestmonthly values (Fig. 1 center; Friedman ANO-VA, df 5 11, x2 5 24.45, P 5 0.011). Monthlyabundance of mated pairs also had a bimodalannual distribution and was significantly cor-related with male abundance (rs 5 0.91, P 50.0025, N 5 12). Both were lowest during thewettest months of the year and negatively cor-related with the average monthly amount ofrainfall (cumulative count of mated pairs: rs 520.61, P 5 0.0425; cumulative count of unmatedmales: rs 5 20.64, P 5 0.0348; number ofmarked males: rs 5 20.59, P 5 0.0514; N 5 12in each case). The first mated pairs appeared inAugust to September, and male abundance in-creased quickly from August to October, at thesame time that rainfall diminished. This markedthe onset of the annual breeding cycle. A firstpeak of breeding activity occurred in October.As rainfall diminished further, fewer matedpairs, and fewer males were found. During thedriest months, male abundance as well as mat-ing activity declined. Once the rainy seasonstarted in February, male abundance and matingactivity increased again and reached a secondpeak. But as rainfall continued to increase, maleabundance dropped and mating activity de-clined in April and ceased entirely in May. Maleabundance was lowest during the months ofheaviest rainfall.

Although the pooled four-year record showsmated pairs in December and January, breedingactivity actually ceased for 4.5 6 3.7 weeks(range 5 2–10 weeks, N 5 4) during the driest

610 HORST LUDDECKE

FIG. 3. Duration of nine breeding periods of Hylalabialis at Chingaza, based on a four-year record ofmated pairs. Breeding periods are arranged accordingto the annual breeding cycles, which begin in Augustand September. Plus signs in front of the first and fol-lowing the last bar indicate unknown extension ofthese breeding periods.

FIG. 4. Distribution of 1682 recapture intervals ofmale Hyla labialis at Chingaza.

months of each year. This gap divided the an-nual reproductive activity into two breeding pe-riods (Fig. 3). For practical reasons, I call firstbreeding period the time interval from Augustor September to December, and I call secondbreeding period the interval from January toApril or May, which is followed by the wet-sea-son recovery period until August or September.Apart from the overall absence of mated pairsin June and July (Fig. 1 center), in any given yearthe actual cessation of breeding activity duringthe rainy season was longer than two months(mean 5 13.0 6 1.8 weeks, range 5 11–15weeks, N 5 4). Correspondingly, actual breed-ing periods in any given year were shorter thanthe pooled record indicates (mean 5 17.4 6 2.6weeks, range 5 14–21 weeks, N 5 7).

The average recapture interval for unmatedmales was 20.1 6 24.5 weeks (range 5 1–161weeks, N 5 1682). Most recapture intervals (N5 1223, 72.7%, corresponding to 316 males)were shorter than 26 weeks (Fig. 4). On the oth-er hand, the time intervals between first and lastcapture of 121 (26.3%) males exceeded one year,those of 95 (20.6%) males exceeded two years,and those of 43 (9.3%) males three years (max-imum 5 195 weeks). This, and multiple recap-tures of many males (126 males five times ormore) are evidence that many males participat-ed in successsive breeding periods of the pop-ulation: 121 individuals were encountered intwo successive breeding periods, 50 in three, 19in four, 11 in five, two each in six and sevensuccessive breeding periods. The number oftimes I found marked males first in the firstbreeding period and again in the second period(N 5 140) was not different from the number oftimes I found marked males first in the secondbreeding period and again in the first period (N5 144). This also confirms that repeated partic-ipation in breeding activity was the rule. I founda significant correlation between the number oftimes a male was recaptured and the time in-terval between first and last capture (rs 5 0.66,

P 5 0.0001). This indicates that males may re-main reproductively active over several years.

Body Condition.—Based on all male captures,fluctuations in SVL, body mass, and BCI fol-lowed a unimodal pattern across the year, withsignificant differences between highest and low-est monthly values, except for SVL (Fig. 1 bot-tom; Friedman ANOVAs, df 5 11 in all cases;SVL: x2 5 19.18, P 5 0.0579; body mass: x2 536.58, P 5 0.0001; BCI: x2 5 29.96, P 5 0.0016).These fluctuations were positively correlatedwith rainfall (SVL: rs 5 0.87, P 5 0.004; bodymass: rs 5 0.93, P 5 0.0021; BCI: rs 5 0.82, P 50.0068; N 5 12 in all cases). Because SVLshowed only small deviations from the mean,the changes in BCI depended mainly on thelarge seasonal fluctuations in body mass. Bodymass and BCI follow a similar annual course,but because the latter is independent of SVL, Iuse it in the following description of the cycle.In June, July, and August, coinciding with themidyear annual period of reproductive inactiv-ity and the onset of the annual reproductive cy-cle, males had a very high BCI. They rapidly lostBCI while the first peak of breeding activity oc-curred in October. The BCI continued to de-crease across the remainder of the first breedingperiod, the dry season reproductive recess, andinto the second breeding period. Males beganto recover BCI in March after the second repro-ductive peak, once the new rainy season wasunderway. They experienced a fast recovery ofBCI toward the end of the second breeding pe-


FIG. 5. Average monthly fluctuation of BCI-valuesin three male categories in a population of Hyla labialisat Chingaza, based on temporal encounter pattern ofmarked individuals. Dashed line: males found onlyonce per year or at longer intervals; thin line: malesfound only once per breeding period; thick line: malesfound repeatedly during the same breeding period.

riod and during the following reproductive re-cess.

The number of successive breeding periods amale attended did not affect its BCI (rs 5 0.06,P 5 0.38, N 5 204). However, I found an effectof the duration of the recapture intervals onBCI-changes within three phases of the annualbreeding cycle (all except the dry-season recess,which was too short and recaptures were toofew to obtain enough data). The longer a maleattended the breeding aggregation during thefirst breeding period, the greater was his BCI-loss (rs 5 20.16, P 5 0.0057, N 5 283). Thistrend also appeared in the second breeding sea-son, but it was not significant (rs 5 20.026, P 50.659, N 5 282). On the other hand, the longera male’s recovery period during the rainiestmonths, the higher was his BCI-gain (rs 5 0.24,P 5 0.001, N 5 188).

The general pattern of BCI-fluctuation acrossthe year was modulated depending on a male’sbreeding phenology. To show this, I establishedthree categories. Males in the first one (N 5 302,1639 captures) were found at least twice in thesame breeding period. These had comparativelythe lowest BCI (Fig. 5). The second category in-cluded 113 males (398 captures) that were foundin successive breeding periods but only onceper breeding period, that is, twice per year.These experienced relatively lesser BCI-lossesduring the first breeding period and entered thesecond breeding period with a relatively highBCI. The third category consisted of 398 males(456 captures) seen at intervals of at least oneyear but mostly only once during the entire

study period. These had a significantly higherBCI (77.2 6 8.2) than males in the first category(75.3 6 8.9; Wilcoxon signed-rank test, Z 522.82, P 5 0.0047) but a BCI indistinguishablefrom that of the second category (75.9 6 8.2;Wilcoxon signed-rank test, Z 5 0.97, P 5 0.33).They had a longer recovery period and achieveda higher BCI than all other males before enter-ing the annual breeding cycle.

DISCUSSION

Males from this population of H. labialis ex-hibited annual reproductive activity that beganhaltingly in August or September, when theyhad high body energy reserves, and peaked inOctober. After a short recess during the dry sea-son and a second peak in February, reproduc-tive activity declined in April or May of the fol-lowing year, after energy reserves had beengradually depleted. The annual cycle was com-pleted by a recovery period that lasted until Au-gust or September, during which males rapidlyregained body condition. The strong positivecorrelation between recapture interval and BCI-gain during this period suggests that it is ad-vantageous to recover from reproductive activ-ities during the wettest months of the year. Thismay be a time of high biomass productivity inprey species of H. labialis, allowing fast and ef-ficient energy acquisition.

The recapture results reveal that many maleH. labialis sustained reproductive activity formany months each year. Extended reproductivedisposition also occurs in other tropical anurans(Wells, 1977; Woolbright, 1983; Donnelly, 1989,1999; Kuhn et al., 1990), and in anurans livingin mild and rainy temperate climates (Vences,1994). Further, across several consecutive years,male H. labialis tended to participate in everybreeding cycle and even in every breeding pe-riod of their population. Although potentiallyreproductive female H. labialis may be encoun-tered in any month of the year (Hunter and Val-divieso, 1962), most highland females spawnedonly once per year or at even longer intervals(Luddecke, 1997), as may also happen in geo-graphically marginal populations of temperatezone anurans (Andren and Nilson, 1985;Jørgensen, 1992; Kuhn, 1994). Across 4–5 yr ofliving in my laboratory under monotonous hy-dric conditions, each of 18 female H. labialiswent through several reproductive cycles ofvarying duration. Although most of them hadspawned in March of 1989 shortly after capture,they never spawned synchronously again (Lud-decke, 1995). This, and lack of synchronizationunder natural conditions (Luddecke, 1997), sug-gest endogenously determined individualbreeding cycles, which may become evidentwhen living under virtually constant climatic

612 HORST LUDDECKE

conditions, for instance as a pronounced repro-ductive quiescence in males of the giant swampfrog (Dicroglossus occipitalis) on the Africanequator (Kuhn et al., 1990). Hyla labialis live ina seasonal climate and reproductive quiescenceis clearly associated with the rainiest months.Presently, it is unknown whether the onset ofreproduction in September is associated with in-creasing androgen plasma levels or testes sizesat some moment during the recovery period.The terrestrial habits of adult H. labialis duringthese months suggest a physiological-based re-productive recess. Concerning biomass produc-tion, the basic reproductive cycle of male H. la-bialis was annual and hence did not differ fromthat of females (Luddecke, 1997). Across the an-nual cycle, males gain biomass (body tissue)within a short time and spend it slowly, where-as females accumulate biomass (eggs) slowlyand lose it in a single night while spawning.

The seasonal fluctuations in body condition ofmale H. labialis were directly correlated with lo-cal rainfall pattern. Because rainfall pattern inthe study area is pronounced and predictable, itmight be used by the frogs as an external cue,as has been shown to occur in several other an-uran species with annual reproductive cyclicity(Bea et al., 1986; Jørgensen et al., 1986). Al-though H. labialis did not reproduce during therainiest months of the year, it cannot be consid-ered a dry-season breeder for two reasons. First,Chingaza is a wet paramo (Sarmiento, 1986;Dıaz et al., 1997), and except for December toFebruary, rainfall was plentiful and maintainedbreeding ponds’ near capacity (ponds used forspawning did not dry in 1992, an El Nino-year).Second, reproductive activity actually ceasedduring part of the dry season. Lack of rainfallduring the dry season seemed to restrain H. la-bialis from breeding (perhaps owing to less lo-comotor activity to avoid excessive loss of bodywater), and the first showers at the beginning ofa new rainy season in February seemed to trig-ger breeding activity. A burst of sporadic breed-ing activity immediately after an exceptionalrainstorm in mid-January 1992 (pers. obs.) alsosuggests that rain modulates reproductive be-havior. But males and females maintained theirreproductive disposition during the dry season:when taken to the laboratory they spawned inaquaria (Luddecke, 1995).

Body energy reserves rather than rainfall mayhave determined the start and end of the annualreproductive cycle. Onset of breeding activity inAugust or September occurred despite dimin-ishing rainfalls after males had gained a highBCI during the rainiest months. Corresponding-ly, despite increasing rainfalls, mating activityceased entirely in May after males had arrivedat a low BCI. Thus, body condition may func-

tion as a physiological threshold for the startand end of the annual reproductive cycle. Cer-tainly, rainfall pattern does not function as aspecieswide synchronizer of reproductive activ-ity. Adjacent mountain ranges in the same An-dean chain have dissimilar rainfall patterns(Sarmiento, 1986; Dıaz et al., 1997). Therefore, ifrainfall were a determinant of breeding activity,then local adjustments would be expected.However, in a population of H. labialis some 30km distant from the study site, breeding activityalso peaked in October, but it coincided withthe months of heaviest local rainfall (Amezquitaand Luddecke, 1999). This trend is more in ac-cordance with other hylids, which even in ex-tremely wet tropical areas increased reproduc-tive activity in response to increased rainfall(Donnelly and Guyer, 1994). Seasonal tempera-ture fluctuations are almost nonexistent near theequator and probably have little or no effect onthe timing of reproductive activity of any pop-ulation of H. labialis.

It seems that males captured once or recap-tured at very long intervals actually interruptedbreeding activity for extended periods, and theyhad a higher BCI than other males when theyfinally returned to the pond for breeding. Con-cerning males recaptured at shorter intervals,the initial decline in BCI in July and August,even before mated pairs had been found, wasprobably caused by early calling activity, sincecalling occurs more frequently than actual re-production, as in other frog species (Blair, 1961;Donnelly and Guyer, 1994) and is energeticallycostly (Taigen and Wells, 1985). During the firstbreeding season I found a significant correlationbetween recapture interval and BCI-loss of maleH. labialis, the rather low correlation coefficientsuggests that each male may have its particularpattern to join or drop out of the breeding ag-gregation, as observed in males of several an-urans (MacNally, 1981; Given, 1988; Grafe et al.,1992; Lance and Wells, 1993; Bevier, 1997), andsuggested by dynamic modeling of breedingphenology (McCauley et al., 2000). In fact, at theindividual level, BCI-changes of male H. labialissometimes occurred contrary to expectations,for instance, males assumed to be reproductive-ly active gained body mass. It is known thatmales of some tropical anuran species can gainbody mass during an absence of a few daysfrom the breeding aggregation (Bevier, 1997).Therefore, particularly for longer recapture in-tervals, caution is recommended when assum-ing that males actually spent all these weeks un-interruptedly at the breeding aggregation. Butdespite my coarse-grained field-day schedule,this assumption seems reasonable, given thatmales found repeatedly during the same breed-ing period had overall the lowest BCI. Because


factors like the social environment at the pondand competitivity for females may also play arole in a male’s decision to stay or leave, therules for changes in individual behavior may bemore complex and more plastic than those thatguide the start and end of the annual reproduc-tive cycle.

Acknowledgments.—I am grateful to M. L. Bo-horquez and A. Amezquita for assistance in thefield. I thank K. R. Lips, B. K. Sullivan, an anon-ymous reviewer, and particularly M. A. Don-nelly for providing many suggestions thathelped to improve the manuscript. The Colom-bian Ministry of the Environment granted per-mission to study frogs in the nature reserve.Universidad de los Andes, Bogota, gave finan-cial support.

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Accepted: 20 February 2002.

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