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Feeding Ecology of the Endemic Rattleless Rattlesnake, Crotalus Catalinensis, of Santa Catalina Island, Gulf of California, Mexico

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Feeding Ecology of the Endemic Rattleless Rattlesnake, Crotalus Catalinensis, of Santa Catalina Island, Gulf of California, Mexico Copeia, 2007(1), pp. 80–84 Feeding Ecology of the Endemic Rattleless Rattlesnake, Crotalus catalinensis, of Santa Catalina Island, Gulf of California, Mexico HE´ CTOR AVILA-VILLEGAS,MARCIO MARTINS, AND GUSTAVO ARNAUD Crotalus catalinensis is a rattleless rattlesnake endemic to Santa Catalina Island, in the Gulf of California, Mexico. It has been hypothesized that the lack of a rattle in this species is a stealth adaptation for hunting birds in vegetation. We provide detailed data on the diet of C. catalinensis from samples obtained during nine trips to the island in 2002–2004. Over two-thirds (70%) of the diet of C. catalinensis was composed of the Santa Catalina Deer Mouse (Peromyscus slevini). The remaining prey were lizards (Dipsosaurus catalinensis, Uta squamata, and Sceloporus lineatulus). There was an ontogenetic shift in diet and higher feeding activity during the dry season. The diet of this species is only a small subset of the diet of its supposed closest relative, C. ruber, probably as a result of limited diversity of prey on the island. The lack of birds in the diet of C. catalinensis argues against the supposed importance of birds as an essential feature for the hypothesis relating the lack of a rattle with a stealth hunting technique for birds in vegetation. However, since P. slevini is partially arboreal, there remains the possibility that the lack of a rattle is an adaptation for stealth hunting for mice in vegetation. HE rattleless rattlesnake, Crotalus catalinensis, Catalina Leaf-Toed Gecko, Phyllodactylus bugastrole- T is endemic to Santa Catalina Island, in the pis. Avila-Villegas et al. (2004) found remains of P. Gulf of California, Mexico. It is a slender, slevini in the stomach contents of two snakes and moderate-sized rattlesnake that is dimorphic in Avila-Villegas et al. (2005) reported evidence of coloration, having an ashy gray phase and a brown- predation on Santa Catalina Desert Iguana (Dipso- ish phase (Beaman and Wong, 2001; Grismer, saurus catalinensis). We here provide detailed data 2002). The most remarkable feature of this on the diet of C. catalinensis from samples obtained rattlesnake is the lack of the rattle, which was in the field in 2002–2004 and discuss the implica- hypothesized to be a consequence of the absence tions of our results to the ecology and evolution of of natural predators on the island (Radcliffe and this species. Maslin, 1975; Greene, 1997; Rubio, 1998), a stealth adaptation for hunting birds in vegetation (Ottley MATERIALS AND METHODS and Murphy, 1983; Greene, 1997; Grismer, 2002), or the result of random changes in genes Santa Catalina (25u399N, 110u499W) is a granit- controlling rattle formation (Greene, 1997). ic island with an area of 41 km2 (Murphy et al., Based on its phylogenetic affinity with the Red 2002). Its topography is characterized by rocky Diamond Rattlesnake, C. ruber, it is supposed that hillsides separated by wide and narrow sandy C. catalinensis originated from the isolation of arroyos bearing the typical vegetation of the a population of the former species on Santa Sonoran Desert (Wiggins, 1980). The island is Catalina Island during the Pleistocene (see located within the protected area Parque Nacio- Murphy and Crabtree, 1985; Murphy and nal Bahı´a de Loreto, off the coast of Loreto, in Aguirre-Leo´n, 2002). Besides the lack of a rattle, Baja California Sur. The climate of this region another obvious difference between C. ruber and can be divided into three seasons according to C. catalinensis is body length, up to 1.7 m in the patterns of precipitation: the dry season (March– former and 0.7 m in the latter (Grismer, 2002). June), characterized by the absence of rainfall; Information on the biology and ecology of C. the summer rainy season ( July–October), with catalinensis is limited. Previous work was reviewed a substantial increase in precipitation caused by by Beaman and Wong (2001), and recently the cyclonic activity of the tropical Pacific; and Goldberg and Beaman (2003) presented infor- the winter rainy season (November–February), mation on reproduction. Regarding its diet, with a reduction of rainfall (Salinas-Zavala et al., Grismer (2002) reported remains of Santa 1990). Catalina Deer Mouse (Peromyscus slevini), Black- The vertebrate fauna of Santa Catalina Island Throated Sparrow (Amphispiza bilineata), and Santa is composed of nine reptile species besides the Catalina Spiny Lizard (Sceloporus lineatulus)in Rattleless Rattlesnake: the lizards Dipsosaurus scats. Grismer (2002) also suggested that juveniles catalinensis, Sauromalus klauberi, Sceloporus line- may feed on small lizards, centerly the Santa atulus, Uta squamata, Aspidocelis catalinensis, and # 2007 by the American Society of Ichthyologists and Herpetologists AVILA-VILLEGAS ET AL.—CROTALUS CATALINENSIS FEEDING ECOLOGY 81 TABLE 1. FREQUENCY OF OCCURRENCE OF PREY TYPES IN STOMACH CONTENTS AND FECES OF C. catalinensis COLLECTED DURING THE DRY (D) AND RAINY (R) SEASONS. Numbers in parentheses are values per taxonomic group. Stomach contents Feces D R D R Total % Mammals (70) (70.7) Peromyscus slevini 5 6 18 41 70 70.7 Reptiles (29) (29.3) Dipsosaurus catalinensis 2 1 3 10 16 16.2 Uta squamata 0 2 1 6 9 9.1 Sceloporus lineatulus 0 0 0 4 4 4.0 Total 99 100 Phyllodactylus bugastrolepis, and the snakes Lam- by comparing the proportion of snakes with propeltis catalinensis, Hypsiglena torquata, and Lep- stomach contents between the dry and rainy totyphlops humilis (Grismer, 1999, 2002; Murphy seasons with a Chi-square test. Statistica 7.0 was and Aguirre-Leo´n, 2002). Only one terrestrial used for all statistical procedures. mammal species occurs on the island, the Santa Catalina Deer Mouse, Peromyscus slevini (Hall, RESULTS 1981), together with over 15 bird species (e.g., Amphispiza bilineata, Carpodacus mexicanus, Cardi- We examined 193 live snakes for stomach nalis cardinalis, Auriparus flaviceps, Calypte costae; contents, and 15 (12.8%) of them (seven males, Cody and Velarde, 2002). six females, and two of unknown sex; SVL range We conducted nine visits to Santa Catalina 257–660 mm) had prey detectable by palpation. Island from 2002 to 2004: three during the dry Sixteen prey items were found: 11 (68.8%) Santa season (March–June) and six during the rainy Catalina Deer Mice, Peromyscus slevini (three season (July–October). In each field trip (3– males, two females, and six of unknown sex); 5 days) we looked for snakes on the surface of three (18.8%) Santa Catalina Desert Iguana, arroyos and adjacent hillsides from 1900 to Dipsosaurus catalinensis (sexes unidentified); and 2400 h, sampling a different locality each day. two (12.5%) Santa Catalina Side-Blotched Lizard, Captured snakes were searched for stomach Uta squamata (one male and a lizard of unknown contents and feces, which we obtained by forced sex; Table 1). Only one snake had two prey items regurgitation and gentle palpation of the last third in its stomach (both P. slevini). All prey were of the body, respectively. When possible, we ingested headfirst. recorded direction of ingestion and sex of prey. We searched for feces in 194 live snakes, which We also recorded snout–vent length (SVL), sex (by resulted in 93 samples. Of these, 75 snakes cloacal probing; Schaefer, 1934), color pattern (80.6%, 35 males, 33 females, and seven of (gray phase or brown phase), and area of capture unknown sex; SVL range 279–762 mm) had (arroyo or hillside) of each snake. Snakes were identifiable remains. Eighty-three prey remains released immediately after data gathering. Prey were found out of the 75 samples examined: 59 samples were preserved in alcohol (70%), and prey (71.1%) P. slevini; 13 (15.7%) D. catalinensis; remains (e.g., scales, fur) identified under a dis- seven (8.4%) U. squamata; and four (4.8%) S. secting microscope. Lizard scales were identified lineatulus (Table 1). In eight cases, remains of by comparison with a reference collection of two different prey species were found in the same lizards from Santa Catalina Island or with the use sample: P. slevini and U. squamata (three times); of a scale identification key. Previous reports of our P. slevini and D. catalinensis (twice); P. slevini and findings (Avila-Villegas et al., 2004, 2005) are also S. lineatulus (once); D. catalinensis and S. line- included in the analyses. atulus (once); and D. catalinensis and U. squamata We tested for differences in diet between sexes, (once). We found no bird remains in scats or color patterns, seasons, and areas of capture by stomach contents of C. catalinensis in any year or comparing the frequencies of prey types with season. a Chi-square test. Yates correction was applied There were no significant differences in diet when necessary (Zar, 1984). Ontogenetic shifts in composition between sexes (x2 5 0.18, df 5 1, P diet were tested by comparing the SVL of snakes . 0.05), color patterns (x2 5 2.77, df 5 1, P . that consumed lizards with those of snakes that 0.05), or seasons (x2 5 1.01, df 5 1, P . 0.05). ate mammals using a Mann-Whitney U-test. We However, there was a significant difference in the analyzed seasonal differences in foraging activity proportion of mice and lizards consumed by area 82 COPEIA, 2007, NO. 1 of capture (x2 5 6.41, df 5 1, P , 0.05), with slevini) available to C. catalinensis, the mainte- lizards being preyed at a higher proportion on nance of a viable population of that species is streambeds than on hillsides. Snakes that con- critical for the conservation of C. catalinensis. sumed mammals (n 5 64) were significantly Crotalus catalinensis preyed upon three of six larger (Z 5 3.31, P , 0.001) than those that ate lizard species that inhabit Santa Catalina Island: lizards (n 5 32), showing a marked ontogenetic Dipsosaurus catalinensis, Sceloporus lineatulus, and shift in diet, from ectothermic to endothermic Uta squamata (Grismer, 2002; Avila-Villegas et al., prey.
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