162South American Journal of Herpetology, 3(2), 2008,Microhabitat 162-167 use in catalinensis © 2008 Brazilian Society of Herpetology

Exploring hypotheses about the loss of the rattle in rattlesnakes: How arboreal is the Isla Santa Catalina rattleless rattlesnake, ?

Marcio Martins1,4, Gustavo Arnaud2, and Rosalva Murillo-Quero3

1 Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, 05508‑090 São Paulo SP, Brazil. Email: [email protected] 2 Centro de Investigaciones Biológicas del Noroeste, Mar Bermejo No. 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S. México. C. P. 23090. Email: [email protected] 3 Centro de Investigaciones Biológicas del Noroeste, Mar Bermejo No. 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S. México. C. P. 23090. Email: [email protected] 4 Corresponding autor.

Abstract. Rattle loss in the Isla Santa Catalina ( Sur, México) rattlesnake, Crotalus catalinensis, was hypothesized to be a stealth adaptation for hunting for birds within the vegetation. Recently, however, it was shown that birds are rarely captured by C. catalinensis, while a semi-arboreal mouse is very important in its diet. It was thus suggested that the loss of the rattle could be a stealth adaptation for hunting for mice within the vegetation. But both these hypotheses imply a high degree of arboreality in C. catalinensis, and there is no detailed study on microhabitat use in this . Here we use field data recently obtained (2005 to 2008) to test the hypothesis of a high degree of arboreality in C. catalinensis. During nine visits to Isla Santa Catalina we searched for in suitable habitats. Of 92 observations in which the snakes were exposed, in seven occasions (7.6%) they were on the vegetation. There was no difference between sexes or between young and adult snakes in the frequency of use of vegetation. Thus, C. catalinensis is a primarily terrestrial rattlesnake which uses the vegetation only occasionally, similar to its sister species . Results of a previous phase of our studies at Isla Santa Catalina are similar to those presented herein. These results make the hypothesis of the loss of the rattle as a stealth adaptation for hunting on the vegetation very unlikely, since such a low frequency of use of vegetation may not function as a selective agent that could lead to an adaptive loss of the rattle.

Keywords. Crotalus catalinensis, rattle loss, microhabitat, feeding, México.

Introduction The loss of the rattle in rattlesnakes was suggest- ed to be (1) a consequence of the absence of natural Rattle vestigialization (rattle loss or reduced rattle predators on the habitat (e.g., Radcliffe and dimensions) in rattlesnakes is well known in the pig- Maslin, 1975; Greene, 1997; Rubio, 1998; Rabatsky, my rattlesnake, Sistrurus miliarius (e.g., Rowe et al., 2007), (2) a stealth adaptation for hunting for birds 2002), and in three island species of the Gulf of Cali- on the vegetation (e.g., Ottley and Murphy, 1983; fornia: the Isla Santa Catalina rattlesnake, Crotalus Greene, 1997; Grismer, 2002), or (3) the result of catalinensis (e.g., Beaman and Wong, 2001; Grismer, random changes in genes controlling rattle formation 2002), the Isla San Lorenzo rattlesnake, Crotalus (i.e., by genetic drift; Greene, 1997; Rabatsky, 2007). lorenzoensis (e.g., Radcliffe and Maslin, 1975; Hol- Regarding the first hypothesis, Radcliffe and Maslin lingsworth and Mellink, 1996), and the Isla San Este- (1975) suggested that the absence or relaxation of the ban rattlesnake, Crotalus estebanensis (e.g., Grismer, selection pressure for a warning mechanism exerted 2002). In the former species, almost all individuals by predators in the islands where Crotalus catalin‑ lack a rattle, whereas in the two latter rattle loss is ensis and Crotalus lorenzoensis occur allowed the variable (Grismer, 2002; Rabatsky, 2007). However, fixation of a mutation leading to rattle loss and that recently, Rabatsky (2006, 2007) reported on the find- this mutation may not have occurred in other island ing of five additional populations/species of rattle- populations of rattlesnakes that still possess the rattle snakes in which rattle vestigialization occurs. Thus, (Crotalus atrox in Isla San Pedro Mártir and Crota‑ rattle vestigialization in rattlesnakes is more preva- lus tortuguensis in Isla Tortuga). Regarding the sec- lent than once thought. Rabatsky (2007) also showed ond hypothesis, it was suggested that the loss of the that several degrees of rattle vestigialization occur rattle in C. catalinensis would avoid the potential for in island rattlesnakes, from a virtually complete loss clicks of the rattles against vegetation, which could of the rattle in C. catalinensis to different degrees of startle birds, its potential prey (e.g., Ottley and Mur- rattle reduction in other populations/species. phy, 1983; Greene, 1997; Grismer, 2002). Finally, Martins, M. et al. 163

Greene (1997) suggested that the loss of the rattle in M.Sc. thesis (Avila-Villegas, 2005), which data was C. catalinensis could be due to genetic drift (i.e., ran- gathered in a previous phase (2002‑2004) of our stud- dom changes in the genes that control the formation ies at Isla Santa Catalina. In this current study, we use of the basal segment). field data recently obtained for the Isla Santa Catalina Although the hypotheses regarding the loss of the rattlesnake to test the hypothesis of a high degree of rattle in rattlesnakes remained poorly explored until arboreality in this species. recently, recent reports are beginning to disentangle the multiple factors involved (e.g., Avila-Villegas et al., 2007; Rabatsky, 2007). For instance, Rabatsky Methods (2007) provided good evidence for the hypothesis of relaxation of the selection pressure for a warning Study – Crotalus catalinensis is endemic to mechanism: rattle vestigialization was significantly Isla Santa Catalina in the Gulf of California, México. correlated with lack of potential mammalian enemies It is a slender, moderate-sized rattlesnake that is di- (e.g., ringtails, Bassariscus spp.; foxes, Urocyon spp.; morphic in coloration, having an ashy gray phase and and coyotes, Canis spp.) in the islands. a brownish phase (Beaman and Wong, 2001; Gris- Regarding the second hypothesis, Avila-Villegas mer, 2002). Based on its hypothesized phylogenetic et al. (2007) showed that birds are almost never con- relationship with the Red Diamond Rattlesnake Cro‑ sumed by the Isla Santa Catalina rattlesnake. This re- talus ruber, it is supposed that C. catalinensis origi- sult is against an essential feature for the hypothesis nated from the isolation of a population of the former relating the lack of a rattle with a stealth hunting for species in the Isla Santa Catalina during the Pleisto- birds on the vegetation: the supposed importance of cene (see Murphy and Crabtree, 1985; Murphy and birds in the diet of Crotalus catalinensis (Ottley and Aguirre-León, 2002; Murphy et al., 2002; Castoe and Murphy, 1983; Hollingsworth and Mellink, 1996; Parkinson, 2006). Besides the lack of a rattle, another Greene, 1997; Rubio, 1998; Grismer, 2002). Howev- evident difference between C. ruber and C. catalin‑ er, Avila-Villegas et al. (2007) point out that there re- ensis is the body length, attaining 1.7 m in the former mains the possibility that the lack of a rattle may have and 0.7 m in the latter (e.g., Grismer, 2002). been selected for a stealth hunting for the partially arboreal mouse, Peromyscus slevini, by far the most Study site – Isla Santa Catalina (25°39’N; 110°49’W) important prey of C. catalinensis (over three thirds is a granitic island with an area of 41 km2 (Murphy of all prey found). Nonetheless, the possibility that et al., 2002). Its topography is characterized by rocky the rattle loss may have been selected for to facilitate hillsides separated by sandy arroyos (dry streambeds) stealth when hunting for arboreal prey implies a high bearing the typical vegetation of the Sonoran Desert degree of arboreality in C. catalinensis. Reports on (Fig. 1A; see Wiggins, 1980). The island is located in the use of perches on the vegetation by rattlesnakes the Parque Nacional Bahía de Loreto, off the coast of are common in the literature and in several instances, Loreto, in Baja California Sur. The climate of this re- this behavior is attributed to foraging (e.g., Cunning- gion can be divided into three seasons: the dry season ham, 1955; Klauber, 1956; Rubio, 1998). Klauber (March-June), characterized by the absence of rain- (1956), for instance, provides several descriptions fall; the summer rainy season (July-October), with of the use of perches on the vegetation for over ten a substantial increase in precipitation caused by the species or subspecies of rattlesnakes. For C. catali‑ cyclonic activity of the tropical Pacific; and the win- nensis, Rubio (1998:124) states that “Charles Bogert ter rainy season (November-February), with a reduc- [...] related that the Santa Catalina Island rattlesnake tion of rainfall from previous months (Salinas-Zavala [...] is frequently found in shrubs hunting birds...”. et al., 1990). Grismer (2002:326) reported finding six individuals (five of them gravid females) within the vegetation From 2005 to 2008 we conducted nine visits to in the summer and stated that these snakes “seemed the southern region of Isla Santa Catalina, three dur- to glide as swiftly through the branches as would an ing the dry season (March-June), two during the arboreal or semiarboreal snake.” Grismer (2002) also summer rainy season (July-October), and four dur- suggested that the climbing ability of C. catalinensis ing the winter rainy season (November-February). In would be related to its supposed bird-eating habits. each field trip (4‑7 days) we looked for snakes on the However, there is no detailed report on microhabi- surface of arroyos and adjacent hillsides at different tat use in C. catalinensis, except for an unpublished times of the day, but mainly in late afternoon and at 164 Microhabitat use in Crotalus catalinensis

Figure 1. A. View of the vegetation that covers the arroyos and hillsides of Isla Santa Catalina, Baja California Sur, México. B. An individual of Crotalus catalinensis on a low shrub (Bursera hindsiana) at Isla Santa Catalina. Martins, M. et al. 165

night (1900 to 2400 h), most of the times sampling a Discussion different locality each day. We recorded the snout- vent length (SVL ± 1 mm), sex (by cloacal probing; Our results show that Crotalus catalinensis is a Schaefer, 1934), microhabitat, and area of capture primarily terrestrial rattlesnake which uses the veg- (arroyo or hillside) of each snake found. For most etation only occasionally, similar to its sister species snakes, we also recorded posture and behavior: coiled Crotalus ruber (e.g., Klauber, 1956; Ernst, 1992). in ambush, coiled in a resting posture (see Oliveira They also indicate the lack of an ontogenetic shift and Martins, 2001), stretched out but not moving, or in the use of vegetation. Results of a previous phase moving. Snakes were released immediately after data (2002‑2004) of our studies at Isla Santa Catalina (see gathering. Avila-Villegas, 2005) are similar to those presented We tested for an ontogenetic shift in microhabitat herein: of 193 C. catalinensis observed during visual use (i.e., for a difference in the size of snakes found searches, only 20 (10.4%) were on the vegetation (12 on the ground and on the vegetation) with a Mann- males, eight females; 18 adults, two juveniles), with a Whitney U‑test and for a difference in the frequency higher proportion of snakes on the vegetation in July of use of vegetation between sexes with a Chi-square (20% against a mean of 7.7% in the other months: test. April, May, June, August, September, and Octo- ber). The absence of a high degree of arboreality in C. catalinensis weakens the hypothesis of the lack of Results the rattle as a stealth adaptation for hunting on the vegetation (Ottley and Murphy, 1983; Greene, 1997; A total of 112 observations of snakes were made. Grismer, 2002), since such a low frequency of use of Snakes were exposed (i.e., not hidden) in 92 observa- vegetation may not function as a selective agent that tions, and under dead plants (N = 17, always under could lead to an adaptive loss of the rattle. cardón) and rocks (N = 3) in 20 obervations. Of the However, the large number of assertions of a high 92 observations in which the snakes were exposed, in degree of arboreality in Crotalus catalinensis in the seven occasions (7.6%) the snakes were on the veg- literature remains unexplained. Perhaps the state- etation, always with their bodies stretched as in fig- ments regarding C. catalinensis as using the veg- ure 1B. These snakes were found in January (two of etation frequently stems from a wrong impression ten snakes found), June (one of six), September (one caused by the fact that both by day and at night it is of 21), November (one of nine), and December (two much easier to see a C. catalinensis on the vegetation of five). For snakes found within vegetation, mean than under the low trees and bushes that characterize height of the perch above ground was 44.7 ± 26.2 cm the vegetation of Isla Santa Catalina. Indeed, during a (range 20‑100 cm). Five of the plants used by snakes study underway on C. catalinensis movements using were identified: Lycium sp., Bursera microphylla, thread bobbins (see Avila-Villegas, 2006), the re-lo- Bursera hindsiana, Pachycereus pringlei, and Eu‑ cation of snakes by day on the shaded ground under phorbia magdalenae. plants is almost always difficult. Snakes found on the vegetation had a mean to- Alternatively, there may be some periods of the tal length of 607 ± 72 mm (range 480‑669 mm) year in which Crotalus catalinensis uses the veg- and snakes that were exposed and on the ground etation more frequently than in other periods, and had a mean total length of 636 ± 123 mm (range samples restricted to the periods in which it uses the 212‑828 mm). The size of the exposed snakes found vegetation more frequently would produce a biased on the vegetation (N = 7) was not significantly dif- view of microhabitat use. Grismer (2002) found six ferent from the size of the snakes that were exposed snakes (five of which gravid females) on the vegeta- and on the ground (N = 82 snakes measured; z = 1.15, tion in a few days in July and we (in the 2002‑2004 p = 0.250). phase of the study; see Avila-Villegas, 2005) found Of the 92 snakes found exposed on the ground, a larger number of snakes on the vegetation also in 78 had their sex determined: 41 were females and 37 July, including a snake with two mice (Peromyscus were males. Of the snakes found on the vegetation, slevini) in the stomach. But why should the snakes be five were females and two were males. The propor- more arboreal in July? Perhaps during the extreme- tion of males and females found on the vegetation ly hot days of summer (air temperatures may attain was not significantly different from that of exposed 34.5°C by day and 28.9°C at night), perches on the snakes found elsewhere (χ2 = 0.92, p = 0.337). vegetation are good sites for thermoregulation, with 166 Microhabitat use in Crotalus catalinensis a mosaic of sunlight and shadow and away from the a la isla, buscamos serpientes en habitats apropiados. extremely high temperatures of the exposed rock and De 92 observaciones en las cuales las serpientes es- soil surface (which may be as high as 70.2°C dur- tuvieron expuestas, solo en siete ocasiones (7.6%) ing daytime and 29.3°C at nigth). Indeed, on Shedao ellas estuvieron sobre la vegetación. No hubo dife- Island (China), Shine and Li-Xin (2002) found lower rencia entre sexos ni entre jóvenes ni adultos en la operative temperatures inside copper models in trees frecuencia del uso de la vegetación. En este sentido, than on the ground (because of wind) and that indi- C. catalinensis es una serpiente primordialmente te- viduals of Gloydius shedaoensis were cooler in ar- rrestre que utiliza la vegetación solo ocasionalmente, boreal ambush sites than in terrestrial sites. A long- como su especie hermana Crotalus ruber. Resultados term, multi-seasonal study on thermoregulation in de una fase previa de nuestros estudios en Isla Santa C. catalinensis would probably reveal the advantages Catalina son similares a los presentados aquí. Estos of using the vegetation in this species. resultados hacen de la hipótesis de la pérdida del cas- This study and those by Rabatsky (2007) are the cabel como una adaptación a la cacería sigilosa sobre first to directly explore the hypothesis related to rat- vegetación, poco apropiada, debido a que la baja fre- tle vestigialization in island rattlesnakes. Rabatsky cuencia del uso de la vegetación puede no funcionar (2007) provided strong arguments for the hypothesis como un agente selectivo que pueda llevar a la pérdi- of relaxation of the selection pressure for a warning da adaptativa del cascabel. mechanism in several species/populations of island rattlesnakes and found no evidence for the stealth hunter hypothesis for rattle loss. We showed (here and Acknowledgments in Avila-Villegas et al., 2007) that the hypothesis of rattle loss in Crotalus catalinensis as a stealth adapta- Héctor Avila-Villegas, Miguel Ángel Leal, Luis Burgete, and tion for hunting for birds on the vegetation should be Iván Hernández provided invaluable assistance in the field. Ali abandoned, since C. catalinensis is neither an impor- Rabatsky provided very helpful comments that greatly improved tant bird-eater nor a highly arboreal rattlesnake. Our the manuscript. Otavio A.V. Marques also provided helpful com- ments. We thank Consejo Nacional de Ciencia y Tecnología understanding of the mechanisms involved in rattle (CONACYT) y Fondo Méxicano para la Conservación de la Na- vestigialization in rattlesnakes would greatly benefit turaleza (FMCN) for financial support. Centro de Investigaciones from future detailed studies on the biology of each of Biológicas del Noroeste, S.C. (CIBNOR) provided institutional the eight species/populations identified by Rabatsky support. Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) provided funds for MM to conduct fieldwork in Méxi- (2007) as possessing rattle vestigialization, as well as co. Authorities of the Parque Nacional Bahía de Loreto provided their peninsular or continental sister species. permits for travel to the island (permit number 6252).

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