2006 NORTHEASTERN NATURALIST 13(1):39–42 Red-cockaded Woodpecker (Picoides borealis) Response to Nest Depredation by an Eastern Rat Snake (Elaphe alleghaniensis) David K. Delaney1,*, Larry L. Pater1, Lawrence D. Carlile2, Dirk J. Stevenson2,4, and Andrew D. Walde3,5 Abstract - We report the depredation of a Picoides borealis (Red-cockaded Woodpecker) nest by an Elaphe alleghaniensis (Eastern Rat Snake). Of 38 banded woodpecker groups monitored by video surveillance during 1998–2000, we documented one nest depredation by an Eastern Rat Snake. Woodpecker visitation to the nest area during the depredation event increased substantially compared with pre-depredation nesting behavior. Woodpecker visitation to the nest cavity was minimal during the first six hours after the snake was discovered by the adult woodpeckers. Visitation levels by woodpeckers remained higher than pre-depredation levels while the snake remained in the nest cavity. After the snake’s departure from the nest, visitation rates dropped below pre-depredation levels. Woodpeckers continued to visit the cavity during the day and roost in the cavity at night for the remaining seven days of surveillance post-depredation. This same banded woodpecker pair nested in the same cavity in 1999 and fl edged 1 female. Overall, we observed a low rate of nest depredation by rat snakes during this study; only one instance was recorded during more than 15,000 hours of video surveillance. Based on the proclivity of Red-cockaded Woodpeckers to re-nest in previous nest cavities, and the potential for snakes to re-climb trees based on past successes, resource managers may want to prioritize placement of snake excluder devices or use of bark-shaving at active cavity trees where snake depredation has occurred, especially if funding is limited. We urge ornithologists to continue to incorporate snake research into their avian research to achieve a greater understanding of predator-prey relationships that impact cavity-nesting birds, especially threatened and endangered species such as Red-cockaded Woodpeckers. Elaphe alleghaniensis Holbrook (Eastern Rat Snake; Burbrink et al. 2000) are proficient tree climbers that are known to depredate nests of many bird species (Fitch 1963, Jackson 1970). These constrictors are thought to regularly climb Picoides borealis Linnaeus (Red-cockaded Woodpecker) nest trees (Neal et al. 1993), though rarely have depredation events by rat snakes been documented directly (Jackson 1978, Summerour 1988). Rat snakes may seek out woodpecker nests during the breeding season, and are reported to climb active cavity trees more often than inactive cavity trees, especially during the nestling phase (Neal et al. 1993). Rat snakes use visual and chemosensory stimuli to facilitate foraging (Mullin and Cooper 1998). Arboreal foraging behavior by rat snakes may be stimulated by repeated use of the same nest cavities over multiple years by birds (Durner and Gates 1993). Increased bird activity at nests (e.g., provisioning of young) after the incubation phase (Conner et al. 1999) provides greater visual cues for foraging snakes (Mullin and Cooper 1998). We are not aware of any studies that have used video surveillance to document Eastern Rat Snake depredation of active Red-cockaded Woodpecker nests. As part of a larger project studying the nesting behavior of Red-cockaded Woodpeckers, we documented a single nest depredation event by an Eastern Rat Snake. This paper describes the depredation event and characterizes the behavioral responses by banded Red-cockaded Woodpeckers before, during, and after the nest depredation. We monitored Red-cockaded Woodpecker nesting behavior between 1998–2000 at Fort Stewart (31.88ºN, 81.57ºW), which is a large Army installation located in southeastern Georgia 30 km west of Savannah. Video cameras and time-lapse recorders were used to monitor the nesting behavior of 38 banded Red-cockaded Woodpecker groups (see Delaney et al. 2002 for more detailed description of study site and camera surveillance equipment). The size of the video image at cluster 37, Notes of the Southeastern Nat u ral ist, Issue 7/4, 2008 753 754 Southeastern Naturalist Notes Vol. 7, No. 4 where we documented the nest depredation by the Eastern Rat Snake, was approximately 90 x 120 cm (height x length), and covered about 90 x 45 cm (height x length) of the tree bole centered on the natural nest cavity, which was about 4 m high with an orientation of 218 degrees. Snake excluder devices (SNEDs; Saenz et al. 1999, Withgott et al. 1995) were not used at any of the active Red-cockaded Woodpecker cavity trees at Fort Stewart. The use of SNEDs are suggested for use on small fragmented woodpecker populations, not larger healthy populations (USFWS 2003) like the one at Fort Stewart. The nest was videotaped between 04:30:00–20:30:00 (EST) each day, and adult woodpecker attendance was assumed to occur overnight based on confirmed arrivals at the nest before dark and departures in the morning. Pre-depredation woodpecker behavior. Adult woodpecker’s regularly entered and exited the active nest cavity at cluster 37 prior to the depredation event. The pair also regularly worked resin wells above and below the nest cavity which appeared to be well maintained. We recorded 186.7 hours of nesting behavior at cluster 37 between the 5th day of incubation (29 May 1998) and the 6th day of the nestling phase when the snake entered and depredated the nest (10 June 1998). The mean number of nesting bouts (period of time that an adult attends the nest between entrances and exits from the cavity) per hour increased from incubation (2.13 ± 0.12; range = 1–4 nesting bouts) through the brooding phase (5.12 ± 0.28; range = 1–14 nesting bouts) until the rat snake arrived. Depredation event. We used a Tree Top Peeper TM (Sandpiper Technologies, Inc., Manteca, CA) to ascertain the reproductive status of the woodpecker’s nest at cluster 37 the morning of 10 June 1998. The attending adult fl ushed off the nest in response to the peeper pole, but returned within 8 minutes. The nest contained 2 eggs and 2 nestlings approximately 6 days old. The adult Red-cockaded Woodpeckers made repeated prey deliveries to the nestlings after the nest status inspection and before the rat snake arrived about 3 hours later. At 11:18:02, an Eastern Rat Snake entered the video field of view approximately 1 m above the nest cavity. The snake climbed down the tree and lunged its body into the nest cavity at 11:19:16. The nest only contained the eggs and nestlings when the snake entered; the attending adult had exited the nest at 11:17:37. The rat snake stayed in the nest cavity for nearly 32 hours, though the snake was observed extending its head outside the cavity a number of times over the course of its stay. The rat snake exited the cavity and climbed down the tree on 11 June between 18:51:37–19:15:57. Due to the late departure of the snake from the nest, no woodpeckers were observed near the nest cavity that evening. We did not observe any direct aggressive interactions between the adult Red-cockaded Woodpeckers and the Eastern Rat Snake. Woodpecker behavior during the depredation event. We identified six behaviors in association with the nest cavity and tree during depredation (i.e., snake present; behaviors 1–5 observed) and post-depredation periods (i.e., snake absent; behaviors 1–6 observed). Woodpeckers were observed to either: (1) perch on the lip of the nest cavity, (2) perch on the nest tree in proximity to the nest, (3) fl utter in front of the nest cavity, (4) fl y-by the nest, (5) maintain resin wells while the rat snake was in the nest cavity, or (6) enter the nest cavity. An adult Red-cockaded Woodpecker first arrived at the depredated nest cavity at 11:20:56 on 10 June about 2 minutes after the snake had entered the cavity, landing on the cavity lip for 1 second before fl ying off, apparently in response to the snake’s presence. After the rat snake had arrived, the mean number of woodpecker visitations to the cavity per hour increased substantially (11.38 ± 2.16, range = 1–27 visitations; Fig. 1) compared to pre-depredation visitation rates. Woodpeckers initially responded to the snake’s presence by fl uttering in front of or fl ying by the nest cavity 2008 Southeastern Naturalist Notes 755 (Fig. 1). After about 6 hours, woodpeckers perched at the cavity lip. Woodpecker visitations to the nest stayed relatively high compared to pre-depredation conditions during the remainder of the snake’s stay in the nest (Fig. 1). There was a decrease in the mean number of visitations (4.95 ± 0.85, range = 1–12 visitations) and an increase in the diversity of woodpecker behaviors observed after the snake departed from the nest cavity (Fig. 2). We did not observe adult Red-cockaded Woodpeckers interact directly with the rat snake before, during, or after the depredation event. Woodpecker behaviors associated with the cavity tree (i.e., resin well maintenance, perching on the lip and tree) occurred over a longer duration (range = 1 sec to ≥1 min) than activity not directly occurring on the nest tree, such as fl uttering or fl y-by behavior which occurred over ≤5 sec. durations. Woodpeckers did not enter the nest cavity while the rat snake was present (Figs. 1 and 2). Post-depredation woodpecker behavior. We recorded 78.5 hours of post-depredation woodpecker behavior at cluster 37 from 10–13 June and 14–17 June 1998. Woodpeckers returned to the proximity of the cavity tree at 05:15:46 on June 12 the morning after the snake departed. Woodpeckers entered the nest cavity for the first time at 07:49:53 on June 12. Woodpeckers then began to occasionally perch on the lip of the cavity for a few seconds at a time or enter the cavity for periods of <3 minutes. On the evening of June 12, an adult Red-cockaded Woodpecker was observed night roosting in the cavity. Adult woodpecker activity levels in proximity to the cavity were still relatively high even up to 68 hours after the nest failed (Fig. 2). Activity levels decreased substantially after 99 hours post-depredation (mean = 1.94 ± 0.31 visitations per hr, range = 1–6). Activity may have dropped off sooner than that; we Figure 1. Number and type of nest-area visits by Red-cockaded Woodpeckers per hour (hours: 0–32) while the rat snake was present in the nest cavity at cluster 37 on Fort Stewart, GA, 1998. The asterisk signifies that only 13 minutes of video data were recorded directly after the snake entered the cavity at 11:18:02 on 10 June 1998 before the tape ended at 11:33:58, and the next tape started at 13:47:04. The rat snake left the cavity during the 32nd hour block between 18:51:37–19:15:57 on 11 June 1998. 756 Southeastern Naturalist Notes Vol. 7, No. 4 did not have video coverage between hours 76–98 post-depredation. Woodpeckers continued to visit the cavity during the day and roost there at night for the remaining seven days of surveillance post-disturbance. We do not know exactly when the rat snake ate the eggs and young while in the nest cavity due to the depth and orientation of the cavity opening relative to the camera angle, but found the nest empty when we checked nest status on 19 June. This same banded woodpecker pair nested in the same cavity in 1999 and fl edged 1 female. A variety of species, such as rat snakes (Jackson 1978), Glaucomys volans L. (Southern Flying Squirrel; Laves and Loeb 1999), and Melanerpes carolinus L. (Redbellied Woodpecker; D. Delaney et al., unpubl. data; Hazler et al. 2004; Kappes 1997) are known to depredate or kleptoparasitize the nests of Red-cockaded Woodpecker. Researchers have commented on the importance of incorporating snake behavioral research into avian work (Weatherhead and Blouin-Demers 2004) and describing snake depredation of bird nests and associated response behaviors (Stickel 1962). The persistent use of specific cavities by birds may promote repeated visitations by snakes (Durner and Gates 1993). Snakes may re-climb trees due to past successes and may investigate multiple cavities during arboreal trips to improve foraging success (Jackson 1977). Evidence suggests that Red-cockaded Woodpeckers evolved the behavior of opening and maintaining resin wells at active cavities (Jackson and Thompson 1971) as a way to deter predators, such as snakes (Rudolph et al. 1990, Steirly 1957). However, few researchers have experimentally tested the effectiveness of this behavior (Jackson 1974, Mullin and Cooper 2002). Rat snakes avoid exposure to tree resin by climbing around active resin wells or avoiding sap-laden trees (Jackson 1976). Successful climbs by rat snakes are thought to be infrequent due to the impact of resin barriers (Jackson 1974, Rudolph et al. 1990), and documented cases of snake depredation are often associated with compromised resin barriers (Jackson 1978, Rudolph et al. 1990). The exact manner of cavity entrance by the snake during our observation could not be Figure 2. Number and type of nest-area visits by Red-cockaded Woodpeckers per hour (hours: 33–75) post nest depredation at cluster 37 on Fort Stewart, GA, 1998. 2008 Southeastern Naturalist Notes 757 positively ascertained due to the field of view of the video, which was about 65% of the tree’s circumference. Therefore, the snake may have gained access to the cavity on the backside of the tree or on the tree trunk above the cavity. The snake may have climbed up vegetation adjacent to the cavity tree, and gained access to the nest from behind or above the nest cavity, as has been documented previously for rat snakes (Dennis 1971). We documented that a rat snake inhabited a tree cavity for an extended period after depredating a nest, which has been documented once by Jackson (1977) who reported continuous use of a Colaptes auratus L. (Northern Flicker) nest by a rat snake over a nine-day period. Snakes appear to reduce their movements after feeding and may actually seek out secluded, safe, and thermally favorable microhabitats to rest and digest meals (Bontrager et al. 2006). Thermal stability of tree cavities may produce favorable conditions for snakes to increase their body temperature following ingestion of prey. This behavior, postprandial thermophily, has been reported in snakes (Blouin-Demers and Weatherhead 2001), and is thought to optimize physiological performance, such as increased digestive efficiency, in some reptiles (Espinoza and Tracy 1997, Tattersall et al. 2004, Toledo et al. 2003). Depredation by rat snakes appears to occur primarily during diurnal and crepuscular hours (Weatherhead and Charland 1985), though Hensley and Smith (1986) documented rat snake depredation of bluebird nests at night. The ability of rat snakes to forage at different times of day, and their willingness to stay in cavities for extended periods of time, may reduce exposure to diurnal predators and lessen their interactions with the previous cavity occupants. During our observed depredation event, the rat snake departed from the cavity during crepuscular hours when diurnal predators and adult woodpeckers were inactive. This behavior potentially reduced the snake’s exposure to attack during its descent from the cavity tree. Presence of adult birds at the nest may deter depredation by rat snakes, but nests may still be vulnerable during periods when adults are not attending the nest. We did not observe any aggressive behavior by Red-cockaded Woodpeckers toward the rat snake during the depredation event. Larger woodpecker species such as Red-bellied and Dryocopus pileatus L. (Pileated Woodpeckers) are known to defend their nests against predators and cavity kleptoparasites (Boone 1963, Kappes 1997, Nolan 1959). A week after the nest failed due to snake depredation, woodpeckers still used the cavity as a roost and continued to maintain resin wells above and below the cavity. Continued visitation by birds to failed nests has been documented to a limited degree (Hensley and Smith 1986). This behavior is not surprising when we consider the high degree of interspecific competition that Red-cockaded Woodpeckers experience for roosting and nesting cavities (Carrie et al. 1998), and how the availability of suitable cavities for nesting may limit reproductive success and lead to the decline of cavitynesting birds (USFWS 2003). Overall, we observed a low rate of nest depredation by rat snakes (and by other predators) during this study. We believe that resin-well maintenance by Red-cockaded Woodpeckers at their nest cavities reduces the risk of predation of their nests by snakes compared to the predation of nests of other cavity-nestng birds that do no deploy such protective measures. Based on the proclivity of Red-cockaded Woodpeckers to re-nest in previous nest cavities, and the potential for snakes to re-climb trees based on past successes, resource managers may want to prioritize placement of SNEDs or use of bark-shaving at active cavity trees where snake depredation has occurred, especially if funding is not available for placement of SNEDs on all cavity trees. Our understanding of predator-prey relationships between cavity nesting birds and arboreal predators such as rat snakes is limited. We urge ornithologists to continue to incorporate snake research into their avian work to achieve a greater 758 Southeastern Naturalist Notes Vol. 7, No. 4 understanding of factors that impact cavity-nesting birds (Weatherhead and Blouin- Demers 2004), especially threatened and endangered birds like the Red-cockaded Woodpecker (Saenz et al. 1999). Acknowledgments. This study was supported by US Army Forces Command and the Fort Stewart Army Installation with funding from the Strategic Environmental Research and Development Program, under Conservation Project No. CS-1083, and the Construction Engineering Research Laboratory, which is part of the Engineer Research and Development Center for the US Army Corps of Engineers. The Environmental Division at Fort Stewart provided logistical support and conducted woodpecker nest surveys. We thank T. Brewton, H. Erickson, M. Fay, M. Huffman, M. Klich, S. Kovac, B. Platt, and A. Rinker for assisting with data collection; A. Cone, B. MacAllister, L. Nguyen, and C. Smith for reviewing videotapes; and T. Grubb and T. Brewton for their assistance in placing video cameras. We also thank D. Richardson and one anonymous reviewer for comments that improved the paper. Literature Cited Blouin-Demers, G., and P.J. Weatherhead. 2001. An experimental test of the link between foraging, habitat selection and thermoregulation in Black Rat Snakes, Elaphe obsoleta obsoleta. Journal of Animal Ecology 70:1006–1013. Bontrager, L.R., D.M. Jones, and L.M. Sievert. 2006. Infl uence of meal size on postprandial thermophily in Cornsnakes (Elaphe guttata). Transactions of the Kansas Academy of Science 109:184–190. Boone, G.C. 1963. Ecology of the Red-bellied Woodpecker in Kansas. M.Sc. Thesis. University of Kansas, Lawrence, KS. 56 pp. Burbrink, F.T., R. Lawson, and J.B. Slowinski. 2000. MtDNA phylogeography of the North American Rat Snake (Elaphe obsoleta): A critique of the subspecies concept. Evolution 54:2107–2118. Carrie, N.R., K.R. Moore, S.A. Stephens, and E.L. Keith. 1998. Infl uences of cavity availability on Red-cockaded Woodpecker group size. Wilson Bulletin 110:93–99. Conner, R.N., D.C. Rudolph, R.R. Schaefer, D. Saenz, and C.E. Shackelford. 1999. Relationships among Red-cockaded Woodpecker group density, nestling provisioning rates, and habitat. Wilson Bulletin 111:494–498. Delaney, D.K., L.L. Pater, R.J. Dooling, B. Lohr, B.F. Brittan-Powell, L.L. Swindell, T.A. Beaty, L.D. Carlile, E.W. Spadgenske, B.A. MacAllister, and R. Melton. 2002. Assessment of training noise impacts on the Red-cockaded Woodpecker: 1998–2000. Engineer Research and Development Center, Construction Engineering Research Laboratory, Champaign, IL. ERDC/CERL TR-02-32. Dennis, J.V. 1971. Utilization of pine resin by the Red-cockaded Woodpecker and its effectiveness in protecting roosting and nest sites. Pp. 78–86, In R.L. Thompson (Ed.). Proceedings of the symposium on the ecology and management of the Red-cockaded Woodpecker. Bureau of Sport Fisheries and Wildlife and Tall Timbers Research Station, Tallahassee, FL. Durner, G.M., and J.E. Gates. 1993. Spatial ecology of Black Rat Snakes on Remington Farms, Maryland. Journal of Wildlife Management 57:812–826. Espinoza, R.E., and C.R. Tracy. 1997. Thermal biology, metabolism, and hibernation. Pp. 149–184, In L.J. Ackerman (Ed.). The Biology, Husbandry, and Health Care of Reptiles. Volume 1, Biology of Reptiles. T.F.H. Publications, Neptune City, NJ. Fitch, H.S. 1963. Natural history of the Black Rat Snake (Elaphe o. obsoleta) in Kansas. Copeia 1963:649–658. Hazler, K.R., D.E.W. Drumtra, M.R. Marshall, R.J. Cooper, and P.B. Hamel. 2004. Common, but commonly overlooked: Red-bellied Woodpeckers as songbird nest predators. Southeastern Naturalist 3:467–474. Hensley, R.C., and K.G. Smith. 1986. Eastern Bluebird responses to nocturnal Black Rat Snake nest predation. Wilson Bulletin 98:602–603. Jackson, J.A. 1970. Predation of a Black Rat Snake on Yellow-shafted Flicker nestlings. Wilson Bulletin 82:329–330. Jackson, J.A. 1974. Gray Rat Snakes versus Red-cockaded Woodpeckers: Predator-prey adaptations. Auk 91:342–347. 2008 Southeastern Naturalist Notes 759 Jackson, J.A. 1976. Relative climbing tendencies of Gray (Elaphe obsoleta spiloides) and Black Rat Snakes (E. O. obsoleta). Herpetologica 32:359–361. Jackson, J.A. 1977. Notes on the behavior of the Gray Rat Snake (Elaphe obsolete spiloides). Journal of the Mississippi Academy of Sciences 22:94–96. Jackson, J.A. 1978. Predation by a Gray Rat Snake on Red-cockaded Woodpecker nestlings. Bird-Banding 49:187–188. Jackson, J.A., and R.L. Thompson. 1971. A glossary of terms used in association with the Red-cockaded Woodpecker. Pp. 187–188, In R.L. Thompson (Ed.). The Ecology and Management of the Red-cockaded Woodpecker. Bureau of Sport Fisheries and Wildlife, US Department of Interior, and Tall Timbers Research Station, Tallahassee, FL. Kappes, J.J., Jr. 1997. Defining cavity-associated interactions between Red-cockaded Woodpeckers and other cavity-dependant species: Interspecific competition or cavity kleptoparasitism? Auk 114:778–780. Laves, K.S., and S.C. Loeb. 1999. Effects of Southern Flying Squirrels Glaucomys volans on Red-cockaded Woodpecker Picoides borealis reproductive success. Animal Conservation 2:295–303. Mullin, S.J., and R.J. Cooper. 1998. The foraging ecology of the Gray Rat Snake (Elaphe obsoleta spiloides): Visual stimuli facilitate location of arboreal prey. American Midland Naturalist 140:397–401. Mullin, S.J., and R.J. Cooper. 2002. Barking up the wrong tree: Climbing performance of rat snakes and its implications for depredation of avian nests. Canadian Journal of Zoology 80:591–595. Neal, J.C., W.G. Montague, and D.A. James. 1993. Climbing by Black Rat Snakes on cavity trees of Red-cockaded Woodpeckers. Wildlife Society Bulletin 21:160–165. Nolan, V., Jr. 1959. Pileated Woodpecker attacks Pilot Black Snake at tree cavity. Wilson Bulletin 71:381–382. Rudolph, D.C., H. Kyle, and R.N. Conner. 1990. Red-cockaded Woodpeckers vs rat snakes: The effectiveness of the resin barrier. Wilson Bulletin 102:14–22. Saenz, D., C.S. Collins, and R.N. Conner. 1999. A bark-shaving technique to deter rat snakes from climbing Red-cockaded Woodpecker cavity trees. Wildlife Society Bulletin 27:1069– 1073. Steirly, C.C. 1957. Nesting ecology of the Red-cockaded Woodpecker in Virginia. Atlantic Naturalist 12:180–192. Stickel, D.W. 1962. Predation on Red-bellied Woodpecker nestlings by a Black Rat Snake. Auk 79:118–119. Summerour, B. 1988. Gray Rat Snakes observed climbing Red-cockaded Woodpecker nesting trees. Alabama Birdlife 35:13. Tattersall, G.J., W.K. Milson, A.S. Abe, S.P. Brito, and D.V. Andrade. 2004. The thermogenesis of digestion in rattlesnakes. Journal of Experimental Biology 207:579–585. Toledo, L.F., A.S. Abe, and D.V. Andrade. 2003. Temperature and meal-size effects on the postprandial metabolism and energetics in a boid snake. Physiological and Biochemical Zoology 76:240–246. Weatherhead, P.J., and G. Blouin-Demers. 2004. Understanding avian nest predation: Why ornithologists should study snakes. Journal of Avian Biology 35:185–190 Weatherhead, P.J., and M.B. Charland. 1985. Habitat selection in an Ontario population of the snake, Elaphe obsoleta. Journal of Herpetology 19:12–19. Withgott, J.H., J.C. Neal, and W.G. Montague. 1995. A technique to deter rat snakes from climbing Red-cockaded Woodpecker cavity trees. Pp. 394–400, In D.L. Kulhavy, R.G. Hooper, and R. Costa (Eds). Red-cockaded Woodpecker: Recovery, Ecology, and Management. Center for Applied Studies in Forestry, College of Forestry, Stephen F. Austin State University, Nacogdoches, TX. US Fish and Wildlife Service (USFWS). 2003. Recovery plan for the Red-cockaded Woodpecker (Picoides borealis): Second revision. US Fish and Wildlife Service, Atlanta, GA. 1US Army Construction Engineering Research Laboratory, PO Box 9005, Champaign, IL 61826. 2Environmental Division, 1177 Frank Cochran Drive, Fort Stewart, GA 31314. 37686 SVL Box, 13233 Sea Gull Drive, Victorville, CA 92395. 4Current address - Project Orianne, Indigo Snake Initiative, 414 Club Drive, Hinesville, GA 31313. 5Current address - 8000 San Gregorio Road, Atascadero, CA 93422. *Corresponding author - David.Delaney@erdc.usace.army.mil.