2009 SOUTHEASTERN NATURALIST 8(1):121–128 Do Abandoned Woodpecker Cavities Provide Secondary Cavity Nesters Protection from Climbing Snakes? David L. Leonard, Jr.* Abstract - The pine forests of the southeastern United States support a number of cavity-nesting birds as well as several species of rat snakes (Pantherophis spp.). Rat snakes are well-documented nest predators, and nest predation of some of the region’s cavity nesters is higher than in other areas. Picoides borealis (Red-cockaded Woodpeckers) and Melanerpes eyrthrocephlus (Red-headed Woodpeckers) invest substantial energy in excavating nest and roost cavities in particular trees, presumably to reduce snake predation. The abandoned cavities of these woodpeckers are important nest sites for many other cavity nesters and may provide protection from snakes. I examined the climbing ability of P. guttata (Red Cornsnake) on abandoned Red-cockaded Woodpecker cavity trees and on barkless snags similar to those used by Red-headed Woodpeckers for nest cavities. Compared to snakes climbing on control trees, snakes (n = 9) either took longer to climb to abandoned Red-cockaded Woodpecker cavities, or where unable to climb past the resin barrier. Snakes were unable to climb barkless pine snags. Despite the fact that populations of both woodpeckers have declined, the concomitant reduction in cavities has not resulted in declines of generalist secondary cavity nesters. Introduction The pine (Pinus spp.) forests of the southeastern United States support a diverse suite of cavity-nesting birds (Engstrom 1993). In Florida and southern Georgia pine forests, nest success of some cavity nesters is lower than that of the same species in other regions. For example, nest success of Sitta carolinensis Latham (White-breasted Nuthatch) in northern Florida and southern Georgia was 39% (Leonard 2005) compared to 52% in Arizona (Li and Martin 1991). Miller (2000) reported that nest success for Poecile carolinensis Audubon (Carolina Chickadee) in northern peninsular Florida was 30–51% lower than that reported from northern populations (see Mostrom et al. 2002). Much of these differences may be due to widespread snake predation (Leonard 2005). Rat snakes (Pantherophis spp.) are common throughout the region and are well-documented nest predators of cavitynesting birds (Jackson 1970, 1976, 1978; Neal et al. 1993; Phillips and Gault 1997). Two characteristics of southern pine forests facilitate nest predation by snakes. First, the forest’s vegetative structure is simple (i.e., open forests with little mid-story vegetation). In captive trials, rat snakes were most successful in locating nests in such habitats (Mullin and Cooper 1998). Second, *Department of Wildlife Ecology and Conservation, PO Box 110430, University of Florida, Gainesville, FL 32601. Current address - Hawaii Department of Land and Natural Resources, Division of Forestry and Wildlife, 1151 Punchbowl Street, Room 325, Honolulu, HI 96813; david.l.leonard@hawaii.gov. 122 Southeastern Naturalist Vol. 8, No. 1 the furrowed bark of the region’s pines provides a surface easily climbed by rat snakes (Saenz et al. 1999). In some parts of their range, Melanerpes erythrocephalus Linnaeus (Redheaded Woodpecker, hereafter RHWO) excavate cavities in barkless snags (Ingold 1989, Venables and Collopy 1989, Withgott 1994), which have few surface irregularities used by snakes to climb vertical surfaces. In Arkansas, the time required for RHWOs to excavate cavities was 3 to 5 times longer than that of individuals in other parts of the species’ range (Withgott 1994). This difference was due to birds selecting hard, barkless snags for nest cavity excavation over softer snags with bark. This increased excavation time often prevented pairs from double brooding, indicating a cost to selecting and excavating nest sites vulnerable to snake predation (Withgott 1994). Picoides borealis Vieillot (Red-cockaded Woodpecker, hereafter RCWO) excavate nest and roost cavities in living pines (Ligon 1970) and modify these trees by excavating small holes (i.e., resin wells) in and scaling bark from the tree above and below the cavity entrance. Resin fl owing from wells is an effective snake deterrent (Jackson 1974, Rudolph et al. 1990), and bark scaling and accumulating resin produce a smooth surface difficult for snakes to climb (Rudolph et al. 1990). Resin wells are most often excavated during the breeding season (D.L. Leonard, Jr., pers. observ.), the time when snakes are most likely to climb cavity trees (Neal et al. 1993). Red-cockaded Woodpeckers rarely nest or roost in dead pines (Ligon 1970), and compared to sympatric cavity nesters, RCWOs have high nest success (see DeLotelle et al. 2004, Miller 2000). Two studies have demonstrated that the climbing ability of rat snakes is infl uenced by tree trunk texture (Mullin and Cooper 2002, Rudolph et al. 1990). Anecdotal observations suggest that abandoned RCWO cavity trees with a smooth but dry resin barrier also may inhibit the climbing ability of rat snakes (Dennis 1971, Jackson 1974); if so, they may be important resources for cavity nesters, especially given the number of species that use their cavities (Everhart et al. 1993, US Fish and Wildlife Service 2003). Here I assess the ability of rat snakes to climb abandoned RCWO and RHWO cavity trees. I predict that snakes will be less able to climb woodpecker trees compared to control trees. Methods Study sites and subjects I conducted snake-climbing trials (hereafter trials) in central Florida and southwestern Georgia pine forests. Both sites were maintained in an open condition by frequent fire and were dominated by Pinus palustris Mill. (Longleaf Pine). Pantherophis gutatta Linnaeus (Red Cornsnake) is common at these sites (D.L. Leonard, Jr., pers. observ.) and were used in the trials. Snakes were obtained from a research project at Tall Timbers Research Station, Leon County, FL. Each snake was sexed, and its mass and snout–vent length measured. None were in the process of ecdysis, 2009 D.L. Leonard, Jr. 123 nor did any female appear gravid. Snakes were housed in aquaria and provided with water. The 9 snakes were in captivity for <5 days and were not provided with food. All snakes were released at their point of capture after the conclusion of the trials. Climbing trials Trials were conducted in the early morning or late afternoon from 20 to 22 May 2003; temperatures ranged between 22.4 and 29.4 °C. At the central Florida site, I selected 2 cavity trees abandoned by RCWOs the previous year (i.e., experimental trees). Both were Longleaf Pines, were used as nest sites for at least 9 years (R. DeLotelle, DeLotelle and Guthrie, Inc., Gainesville, FL, pers. comm.), and had a large build-up of dry resin. I selected 2 Longleaf Pines without RCWO cavities, 1 in central Florida and 1 in southwestern Georgia (i.e., controls) that were similar in size to experimental trees. At the Georgia site, I selected 3 barkless Longleaf Pine snags to test the ability of snakes to climb trees similar to those used by RHWOs for nest trees (hereafter snags). On each RCWO cavity tree, I marked a 1- or 2-m course. The length of the course was dictated by the presence of an adequate resin build-up. A similar length course was marked on the respective control trees. I used Swedish climbing ladders to mark the course, to position snakes at the proper height, and to retrieve snakes after each trial. Ladders were placed such that they could not be used by snakes and I was careful not to damage the resin coating on the experimental trees. To prevent snakes from escaping into cavities, I temporary plugged each cavity. Live mice were used to provide snakes with a stimulus to climb. Prior to each trial I placed the mouse near each snake until the snake appeared to be aware of the mouse. I then placed the mouse in a small (10- x 12-cm) wire cage attached to each tree approximately 0.5 m above the end of each climbing course. To begin a trial, a snake was held against a tree below the beginning of the course. On experimental trees, each snake was positioned on the tree directly beneath the cavity. On control trees and snags, their placement was random with respect to position, although each course was started at 1.5 m. Once the snake had secured a purchase on the tree, it was released. If it immediately began climbing down, I removed the snake and again held it against the tree at the start of the course. Snakes that climbed down on the second attempt were removed and not used in that trial; these were not considered unsuccessful attempts. Once a snake began to climb it was not “coaxed” in any manner to climb the tree (see Rudolph et al. 1990). I recorded whether or not each snake completed the climb, the time that elapsed between each snake’s snout crossing the beginning and ending points of the course (hereafter ascent time), and the behavior of each snake. Snakes that initially climbed upwards, but then began to climb down were classified as unsuccessful attempts only after it became obvious that the snake was not searching for an alternative, upward route, but was moving toward the ground. Methods for the trials on barkless snags were similar to those for trials on living trees, except that a 2-m course was marked on all 124 Southeastern Naturalist Vol. 8, No. 1 snags. Each snake was only used twice in a given day. A significance level of 0.05 was used for all statistical tests. Results The RCWO cavity and control trees were typical for each site (Table 1) as were the snags. The snakes varied in length and mass, females tended to be smaller than males (Table 2), and their length was positively correlated to their mass (Spearman’s rank correlation: rs = 0.97, P < 0.01). All snakes climbed upward immediately after being released, except for 1 female that climbed down on both attempts on control tree 1 and experimental tree 2. On each control tree, 3 snakes climbed down on their first attempt, but climbed upward on their second attempt. All snakes successfully completed the 2-m course on experimental tree 1; only half (4 of 8) of the snakes completed the 1-m course on experimental tree 2. Ascent times for experimental tree 1 were longer than those for control tree 1 (Wilcoxon-Signed ranks test: Z = 2.52, P = 0.01). Parallel results were not found for experimental tree 2 and control tree 2 (Wilcoxon-Signed ranks test: Z = 1.83, P = 0.07; Table 3), although this was likely due to the low Table 1. Characteristics of the trees used in the Red-cockaded Woodpecker (Picoides borealis) portion of the snake climbing experiments in Florida and Georgia during 2003. Experimental trees were those with abandoned woodpecker cavities. DBH (cm) Cavity height (m) ResinA (m) Experimental tree 1 29 6.30 3.50 Experimental tree 2 42 5.30 1.70 Control tree 1 31 - - Control tree 2 43 - - ALength of the dried resin barrier below the cavity entrance. Table 2. Morphometrics of Corn Snakes (Elaphe guttata guttata) used in climbing experiments in Florida and Georgia pine forests during 2003. Snout–vent length (cm) Mass (g) Sex n Mean ± SD Range Mean ± SD Range Males 7 90.0 ± 14.3 71–108 295.0 ± 155.3 101–511 Females 2 67.0 ± 12.7 58–76 105.0 ± 54.5 67–144 Total 9 85.0 ±15.7 58–108 253.0 ± 150.4 67–511 Table 3. Length of the climbing course on experimental (ExpTree) and control trees (ConTree), the number of snakes which climbed the trees, the number that successful climbed the course, and the mean (± SD) time (seconds) required to complete the climb of 4 pine trees in Florida and Georgia during 2003. ExpTree1 ContTree1 ExpTree2 ContTree2 Course length (m) 2 2 1 1 Attempted 9 8 8 9 Successful 9 8 4 9 Ascent time 563 ± 342 250 ± 146 421 ± 178 104 ± 70 2009 D.L. Leonard, Jr. 125 number of snakes that successfully completed the course on experimental tree 2. Ascent times for snakes climbing either the first or second meter of experimental tree 1 were longer than those of snakes climbing control tree 2 (218.2 seconds and 344.9 seconds vs. 104.7 seconds, respectively; Wilcoxon- Signed ranks test: Z = 2.68 and 2.66, P = 0.01 and 0.01, respectively). Despite differences in dbh, ascent times were similar for the 2 control trees (Wilcoxon-Signed ranks test: Z = -0.42, P = 0.68). The mass of the snakes was positively correlated with ascent times for experimental tree 1 (Spearman’s rank correlation: rs = 0.90, P < 0.01), but not with either control tree (Spearman’s rank correlation: rs = -0.024, P = 0.99 and rs = 0.57, P = 0.11, respectively) or that of experimental tree 2 (Spearman’s rank correlation: rs = 0.80, P = 0.20). However, 3 of the 4 snakes successfully climbing the latter tree were the smallest of the 9 snakes. The 4 snakes unable to climb experimental tree 2 were larger (358.8 ± 162.3 g) than those that were successful (193.5 ± 101.7 g); small sample sizes and substantial variation in mass precluded the difference from being statistically significant. Snakes climbing experimental tree 2 spent more time searching for alternative routes than those climbing experimental tree 1. During climbing trials on experimental tree 1, snakes were mobbed by M. carolinus Linnaeus (Red-bellied Woodpecker; n = 2) and Sialia sialis Linnaeus (Eastern Bluebird; n = 2). These events lasted from 5 to 15 seconds, with birds fl ying by or hovering near the snakes and vocalizing. None of the birds landed on the tree or struck the snakes. The 3 snags used to quantify rat snake climbing ability ranged from 35.3–49.7 cm dbh. No snake was able to climb the snags, and fell to the ground when released. In contrast, no snakes placed on live trees selected for the trials related to RCWO cavity trees fell after being released. Based on this finding, I did not place snakes on control trees of a similar size to the snags. Discussion The smooth resin barrier of abandoned RCWO cavity trees and the smooth barkless surface of snags hindered the climbing ability of rat snakes. Climbing times were longer for individuals successfully climbing across the resin barrier of RCWO cavity trees compared to those climbing control trees, and 25% of the snakes failed to climb past the resin barrier. Increased climbing times could carry a substantial cost by increasing the exposure of snakes to mobbing birds and raptors (see Mullin and Cooper 2002, Nilsson 1984, Withgott and Amlaner 1996). Rat snakes were unable to climb barkless snags similar to those used by RHWOs for nest sites. The resin barrier of occupied RCWO cavities is an effective snake deterrent. Rudolph et al. (1990) reported that the climbing rate of snakes on occupied RCWO cavity trees was infl uenced by their size and tree diameter. In this study, dbh did not affect ascent times, but that was likely because of 126 Southeastern Naturalist Vol. 8, No. 1 the small sample of trees. Similar to the findings of Rudolph et al. (1990), smaller snakes were better climbers than larger snakes. Larger snakes spent more time searching for suitable climbing routes, especially on RCWO cavity trees. Rudolph et al. (1990) reported that climbing rates on cavity trees were slower compared to control trees, and only 3 of 18 snakes successfully negotiated the resin barrier. In my study, snakes required more time to climb abandoned RCWO cavity trees than did snakes on control trees. However, compared to occupied RCWO cavity trees (Rudolph et al. 1990), in this study, more snakes successfully crossed the resin barrier of abandoned RCWO cavity trees. The 4 unsuccessful attempts in my study all occurred on the same tree, suggesting that variation in the amount and age of resin affects the likelihood of snakes successfully reaching cavities. Withgott (1994) proposed that RHWOs excavate cavities in barkless snags to deter snake predation. Few studies, however, have quantified RHWO nest success (Smith et al. 2000), and none have compared nest success as it relates to nest-tree characteristics. In other species, however, nest success is related to the surface characteristics of nest trees. In Arkansas, Empidonax virescens Vieillot (Acadian Flycatchers) preferentially nested in Quercus nuttallii Palmer (Nuttall Oak), a tree with smooth bark, and individuals nesting in this tree had higher nest success than those nesting in other trees (Wilson and Cooper 1998). Mullin and Cooper (2002) demonstrated that rat snakes were unable to climb the smooth trunks of mature oaks. In California, where Pituophis melanoleucus Daudin (Gopher Snakes) are the most common nest predator of M. formicivorus Swainson (Acorn Woodpeckers), individuals nesting in smooth-barked Plantanus racemosa Wats. (California Sycamores) had higher nest success than woodpeckers using other tree species (Hooge et al. 1999). Delibes et al. (2001) suggested that anthropogenic changes to landscapes can create sinks where mortality or breeding failure is elevated in what would otherwise be high-quality habitat. If pine forests supporting large populations of RHWOs and RCWOs comprised high-quality habitat for other cavity nesters, much of this habitat has been lost. The results of this study, as well as others (Hooge et al. 1999, Mullin and Cooper 2002, Withgott 1994), illustrate that tree characteristics can inhibit the climbing ability of snakes. These results suggest that nest predation historically may have been lower in southeastern pine forests when abandoned RHWO and RCWO cavity trees were more common. Interestingly, most of the cavity nesters that use RHWO and RCWO cavities are still common (Smith et al. 2000, USFWS 2003). Many of these species, however, are multi-brooded (e.g., Eastern Bluebird) or habitat generalists (e.g., Red-bellied Woodpecker) and may be better able to deal with increased nest predation compared to singlebrooded species or habitat specialists. For example, the White-breasted Nuthatch is single brooded, and nest predation by snakes is common for that species (Leonard 2005). Historically, the White-breasted Nuthatch was found throughout the southeastern pine forests, where it frequently nested in abandoned RCWO cavities; now it is extirpated from much of the lower 2009 D.L. Leonard, Jr. 127 coastal plain and peninsular Florida (Engstrom 1996, Leonard 2005). Studies comparing nest success of different cavity-nesting species using different nest trees across geographic regions are necessary to fully understand the importance of and variation in the effects of snake predation on bird communities (see Weatherhead and Blouin-Demers 2004). Acknowledgments I thank S. Stapleton for providing the snakes used in this study and R. DeLotelle for his assistance with the climbing trials. Suggestions by C. Buddenhagen, H. Freifeld, K. Miller, D. Richardson, and two anonymous reviewers improved this article. Literature Cited Delibes, M., P. 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