2010 SOUTHEASTERN NATURALIST 9(2):395–402 Partial Predation at Cavity Nests in Southern Pine Forests Karl E. Miller1,2,* and David L. Leonard, Jr.1,3 Abstract - Although open-cup nesting birds regularly experience partial predation events, little is known about partial predation for cavity-nesting birds. Here we report on 12 partial predation events for 5 species of cavity-nesting birds inhabiting southern pine forests. Snakes, small mammals, and woodpeckers were the primary predators; many were documented by direct visual observation or video photography. We documented two types of outcomes from partial predation events: partial failure, i.e., a single partial predation event followed by successful fledging of >1 young; and complete failure, i.e., multiple, sequential partial predation events that result in total nest failure. We propose the “plate too full” and “eat and run” hypotheses to explain partial nest predation in birds and discuss the characteristics of cavities that may facilitate this phenomenon. Introduction Despite the importance of nest predation as a research topic in recent decades, relatively little is known about the causes or circumstances associated with partial, or incomplete, nest predation. Nest predation traditionally has been interpreted to be an all-or-nothing phenomenon, where the entire contents of a nest are taken during a predation event (Nice 1957, Ricklefs 1969). Consequently, empty nests are typically attributed to a single predation event caused by a single predator species. In addition, most nest-monitoring studies may not detect partial losses of clutches or broods because of infrequent nest inspections. Standard references recommend that nests be checked at 3–4 day intervals (Martin and Geupel 1993, Ralph et al. 1993), and many studies check nest status weekly or even less frequently (e.g., White and Seginak 2000). As the interval between nest checks increases, so does the likelihood for >1 predator to visit the nest in that interval and consume part, or all, of its contents. In addition, even if they are observed, partial clutch and brood loss may not be reported because nest success is often the demographic metric of greatest interest (but see Roy Nielson et al. 2008). Moreover, many nests cannot easily be inspected because of their height or their location in cavities. Thus, observers frequently make inferences about nest status without actually inspecting the contents. Recent use of video photography at songbird nests in various habitats has revealed that open-cup nesting species may regularly experience partial or 1Department of Wildlife Ecology and Conservation, University of Florida, PO Box 110430, Gainesville, fl32611. 2Current address - Florida Fish and Wildlife Conservation Commission Fish and Wildlife Research Institute, 1105 SW Williston Road, Gainesville, fl32601. 3Current address - Hawaii Department of Land and Natural Resources, Division of Forestry and Wildlife, 1151 Punchbowl Street, Room 325, Honolulu, HI 96813. *Corresponding author - Karl.Miller@MyFWC.com. 396 Southeastern Naturalist Vol. 9, No. 2 incomplete predation (Antworth 2005, Carter et al. 2007, Pietz and Granfors 2000, Robinson and Robinson 2001, Small 2005, Stake and Cimprich 2003, Stake et al. 2004, Thompson et al. 1999). In contrast, there is little available evidence of partial predation in cavity-nesting species. This phenomenon may be more difficult to detect in cavity-nesting species because tree cavities are often difficult to inspect and monitor. Here, we report observations of partial predation at 12 nests of 5 cavitynesting bird species in the pine forests of northern Florida and southwestern Georgia. We document two types of outcomes from partial predation events: partial nest failure and complete nest failure. Finally, we propose hypotheses that may explain partial nest predation in birds and discuss the characteristics of cavities that may facilitate this phenomenon. Study Areas Observations were collected at 4 study areas in southwestern Georgia and northern Florida: a mosaic of Pinus elliottii Engelm. (Slash Pine) plantations (even-aged, 30–35 years old) and P. palustris Mill. (Longleaf Pine) sandhill forests (uneven-aged, with scattered ≥100 year-old trees) at Camp Blanding Training Site in Clay County, fl; a remnant old-growth Longleaf Pine clayhill forest (Wade Tract; uneven-aged, with scattered 300–500 year old trees) in Thomas County, GA; second-growth Longleaf Pine clayhill forest (uneven-aged, with scattered trees ≥150 years old) at Pebble Hill Plantation in Grady County, GA; and old field pine (P. echinata Mill. [Short-leaf Pine] and P. taeda L. [Loblolly Pine]) clayhill forest (uneven-aged, with scattered trees ≥100 years old) at Tall Timbers Research Station in Leon County, fl. Some of the study sites at Camp Blanding were provisioned with nest boxes designed to attract Myiarchus crinitus L. (Great Crested Flycatchers) and other passerines (Miller 2000, 2002). The Wade Tract and Tall Timbers sites were provisioned with nest boxes designed to attract Sitta carolinensis Latham (White-breasted Nuthatches; Leonard 2005). Methods Partial predation events were documented incidentally during the course of other studies on the nesting ecology of cavity-nesting birds (Leonard 2005, 2009; Miller 2000, 2002). We used standard methods (Martin and Geupel 1993) to search for nests. When a nest was located, it was monitored at 2–4 d intervals. Nests located <4 m above ground were accessed with a stepladder, and the contents checked with a light and mirror. Nests in cavities >4 m high were monitored with a camera probe mounted on a telescoping fiberglass pole (TreeTop II, Sandpiper Technologies, Inc., Manteca, CA), or by climbing with Swedish sectional climbing or extension ladders. Activity at a portion of nuthatch nests (162 hours) was monitored with a Canon XL-1 digital video camcorder with a 300-mm zoom lens. We visited all nest territories within 1 d after the expected date of fledging to confirm the presence of fledglings and rechecked territories 1–3 times if fledglings were not located on the initial visit. 2010 K.E. Miller and D.L. Leonard, Jr. 397 We defined partial predation as any event in which a partial clutch or brood is taken by a predator. We distinguished between two types of outcomes from partial predation events: partial failure, i.e., a single partial predation event followed by successful fledging of ≥1 young; and complete failure, i.e., multiple, sequential partial predation events resulting in total nest failure. Results We documented partial predation events on 12 nests of 5 species (Melanerpes carolinensis L. [Red-bellied Woodpecker], Great Crested Flycatcher, Poecile carolinensis Sennett [Carolina Chickadee], Baeolophus bicolor L. [Tufted Titmouse], and White-breasted Nuthatch) during 1997–2003 (Table 1). Five of these nesting attempts were partial failures (i.e., fledging of ≥1 young), and 7 were complete failures. Details relevant to interpretation of these events are presented below. Direct observations and video recordings, combined with evidence left at the nest, were used to determine that snakes, small mammals, and woodpeckers were responsible for predation events. Partial failure We documented one case of partial predation on eggs (2 of 4 eggs were removed from a Great Crested Flycatcher nest), where the adults continued to attend the nest and successfully fledge 2 young. We documented one case of partial predation on nestlings (1 of 4 nestlings was removed from a White-breasted Nuthatch nest), where the adults continued to attend the nest and successfully fledge 3 young. In this instance, a M. erythrocephalus L. (Red-headed Woodpecker) was filmed pulling nest Table 1. Cavity nests at which partial predation events were documented in northern Florida and southwestern Georgia. Stage = stage depredated. # = number of fledglings. Nesting species Cavity location StageA Nest predator # Partial failures Great Crested Flycatcher Nest box E Unknown 2 White-breasted Nuthatch Nest box N Woodpecker 3 Red-bellied Woodpecker Dead pine N Snake 1B White-breasted Nuthatch Dead pine N Snake 1B White-breasted Nuthatch Live pineD N Snake 1C Complete failures Red-bellied Woodpecker Dead oak E Unknown - Great Crested Flycatcher Nest box E Flying squirrel - Great Crested Flycatcher Nest box E Unknown - Carolina Chickadee Dead pine E Unknown - Tufted Titmouse Nest box E Flying squirrel - Great Crested Flycatcher Nest box N Snake - White-breasted Nuthatch Live pine4 N Snake - AE = egg, N = nestling. BFledged prematurely, survived <1 d. CFledged prematurely, survived throughout subsequent monitoring. DNest in an abandoned Picoides borealis Vieillot (Red-cockaded Woodpecker) cavity. 398 Southeastern Naturalist Vol. 9, No. 2 material and a nestling from a nest box that contained four 20-day-old nestlings. The woodpecker could fit only its head inside the narrow entrance hole; it tried unsuccessfully to remove additional nestlings for 3 minutes, and then flew off when the adult nuthatch returned with food. Three days later, the remaining nuthatch nestlings were observed out of the nest being fed by their parents. We documented three cases of partial predation on nestlings where the remainder of each brood fledged prematurely (Table 1). In the first case, a ca. 1-m Pantherophis alleghaniensis Say (Eastern Ratsnake) was observed in a Red-bellied Woodpecker cavity in a pine snag and a freshly dead nestling was found on the ground below. The adult woodpeckers brought food to the cavity several times, but each time entered only partially and then flew off with the food. Four days earlier, the cavity contained two 19-day-old nestlings. Fledging occurs at 28 days in this population (K.E. Miller, unpubl. data). In the second case, a ca. 1.5-m P. spiloides Duméril, Bibron, & Duméril (Gray Ratsnake) was filmed entering a White-breasted Nuthatch nest cavity containing four 21-day-old nestlings. When we returned to retrieve the camera, the snake was climbing out of the cavity; 3 lumps were clearly visible in its body, and 1 nestling was found on the ground below the cavity. Subsequent searches of the area failed to locate the prematurely fledged nuthatch. We could not determine if the bird had been attacked by the snake before it fledged, because the camera had run out of film prior to the nestling’s escape. Fledging occurs at 22 d in this population (D.L. Leonard, unpubl. data). In the third case, a White-breasted Nuthatch nest cavity contained a ca. 1 m P. gutatta L. (Red Cornsnake), and no nestlings, and a 21-day-old nuthatch was observed on a nearby tree. The parents were provisioning the prematurely fledged nuthatch and also bringing food to the nest cavity but not entering it. Two days earlier, the cavity had contained at least 3 nestlings. This fledgling was subsequently observed with its parents. Complete failure Repeated partial predation events resulted in eventual loss of the entire clutch at 5 nests (Table 1). At 1 Red-bellied Woodpecker nest, 2 Great Crested Flycatcher nests, and 1 Tufted Titmouse nest, clutches were gradually removed or destroyed over periods of 3–9 d. Two of these nests contained Glaucomys volans L. (Southern Flying Squirrels) and their nest material (Tillandsia usneoides L. [Spanish Moss]) on the day the last egg was found destroyed. In addition, the titmouse nest showed signs of physical disturbance (i.e., nest lining pulled out of the nest cup and the entire structure tilted at a 45° angle from the nest box walls) on repeated occasions that indicated ≥2 sequential predation events. Similarly, repeated partial predation events resulted in eventual loss of an entire clutch at a Carolina Chickadee nest in a pine stump. Consecutive nest inspections at 3–4 day intervals revealed 1, 1, 2, 2, 0, and 0 eggs. On the penultimate visit, the cavity entrance had been enlarged and the cavity was empty. On the last visit, the cavity contained egg shells, indicating that at 2010 K.E. Miller and D.L. Leonard, Jr. 399 least 1 additional egg had been laid and subsequently depredated. It is likely that additional eggs were laid and depredated (i.e., >2 sequential predation events) because 7 days elapsed between the first observation of 1 egg and the first observation of 2 eggs and the typical clutch size is 4–6 for this species (Miller 2000, Mostrom et al. 2002). We also documented repeated partial predation events on nestlings that resulted in eventual loss of the entire brood at 2 nests (Table 1). In the first case, a small (ca. 30 cm in length) Eastern Cornsnake was observed under a Great Crested Flycatcher nest in the corner of the nest box during the egglaying period. We monitored the nest during the next several weeks, but no predation was documented until 4 of the 5 nestlings disappeared just before they were 11 d old. The remaining nestling was gone the following morning, and no fledglings were observed in subsequent searches. Fledging occurs at 15 d in this population (K.E. Miller, unpubl. data). In the other case, we observed a White-breasted Nuthatch nest with two 14-day-old nestlings and a Gray Ratsnake (ca. 1.5 m in length). Four days earlier, the cavity had contained 4 nestlings. We monitored the nest throughout the day and found that adult nuthatches continued to feed the nestlings despite the presence of the snake in the cavity. The following day, the cavity contained the snake and only 1 nestling. Two days later, the snake was gone and the cavity was empty. No fledglings were observed in subsequent searches. Discussion We documented partial predation events throughout the nesting cycle. We attributed observations of partial clutch loss to predation because of the gradual and incremental losses over time coincident with physical damage to the nest site and observations of predators and their nesting material. We attributed partial brood losses to predation because of direct observations and video recordings. Partial brood loss can sometimes result from starvation (i.e., brood reduction; Mock 1994), but brood reduction was rare in the species that we studied. For example, only a single case of brood reduction was documented in White-breasted Nuthatches during 3 breeding seasons (Leonard 2005). Our study was not designed to measure the frequency of partial predation because we were not able to employ cameras at all nests. It is probable that we missed some partial predation events because many cavity nests, especially those of woodpeckers, titmice, and chickadees, were difficult or impossible to inspect because they were located high off the ground in unstable dead wood or inside cavities with narrow openings that would not accommodate a camera probe. Complete inspection of all nest contents was uniformly possible only for Great Crested Flycatcher nests in nest boxes, and they experienced partial predation fairly frequently (4 of 32 nests; 12.5%; K.E. Miller, unpubl. data). We suggest that the lack of information on partial predation in cavitynesting birds is an artifact of the difficulty of monitoring cavity nests. Partial predation is often reported in open-cup nesting species studied with cameras 400 Southeastern Naturalist Vol. 9, No. 2 (Antworth 2005, Pietz and Granfors 2005, Stake et al. 2004) and accounted for 60% of all predation events in one study (Carter et al. 2007). Why does partial predation occur? One likely explanation, which we term the “plate too full” hypothesis, is that predators either cannot handle or cannot consume all the contents at once because of the relative size of predator and prey. For example, Mephitis mephitis Schreber (Striped Skunk) predation on waterfowl nests was influenced by clutch size: small clutches were more likely to be consumed entirely than large clutches (Lariviere and Messier 1997). Video recordings of grassland nests found that predators responsible for partial, repeated predations over >1 d period were primarily small rodents or Molothrus ater Boddaert (Brown-headed Cowbirds) and not larger mammalian predators (Pietz and Granfors 2000). In Florida, a small (56 cm in length) Eastern Ratsnake removed Great Crested Flycatcher nestlings from a nest box one at a time over a >2 d period (Taylor and Kershner 1991). In Panama, a snake 80 cm in length was observed consuming only 1 egg from a Tinamus major Gmelin (Great Tinamou) nest (Robinson and Robinson 2001); after spending >3 h to engulf the first egg, it tried to swallow a second egg but eventually gave up and left the nest. Another explanation, which we term the “eat and run” hypothesis, is that parental defense, or the anticipation of it, interrupts or hurries the predator, causing it to leave before consuming all nest contents. This scenario likely represents a tradeoff between the predator’s hunger and its perception of risk. Carter et al. (2007) describe a Coluber constrictor L. (Southern Black Racer) being chased by Aphelocoma coerulescens Bosc (Florida Scrub-jay) from a nest before it finished swallowing the first nestling. Robinson and Robinson (2001) observed 2 vireos chasing away a toucan after it took 2 of 3 nestlings; the toucan came back 3 d later and took the third. These hypotheses are overlapping, and it is likely that interactions among predator size and aggressiveness, prey size, parental vigilance, and parental defense determine whether the entire contents of a nest are consumed. We also note that the “eat and run” hypothesis may not adequately explain the behavior of snakes at cavity nests. Snakes may benefit by remaining inside a cavity and consuming nestlings gradually over several days, as we observed, when they would otherwise likely be mobbed or attacked when leaving the cavity. Climbing ratsnakes are mobbed by a variety of cavity nesting birds in Florida (Leonard 2009, Miller 2000), and woodpeckers are capable of injuring or dislodging ratsnakes from trees (Casey et al. 2005). Even if some mobbing species do not strike a snake directly, their mobbing can alert raptors to the presence of a snake (Withgott and Amlaner 1996). Cavities provide snakes safety from the attacks of birds (Withgott and Amlaner 1996) and also provide them with an environment conducive to digestion (Bontrager et al. 2006). Partial predation can lead to an underestimate of the frequency of nest predation, particularly if investigators consider partial nest failures as successful nests. Moreover, some partial predation events stimulate premature fledging, 2010 K.E. Miller and D.L. Leonard, Jr. 401 which may put fledglings at greater risk; in our study, 2 of 3 prematurely fledged nestlings failed to survive the first day outside the nest. We agree with Small (2005) that nests should only be considered successful by investigators when fledglings are observed near the nest after the presumed fledgling date. Disparate results for partial predation in birds may be an artifact of different monitoring intensities (Weidinger 2007) or could reflect local (Roy Nielsen and Gates 2007) or geographic (Leonard 2005, Miller 2000) differences in the composition of predator communities. Partial predation in cavity nesting birds warrants further study, particularly in light of the high rates of nest predation on cavity nesting-birds in the pine forests of the southeastern coastal plain of the United States (Leonard 2005, Miller 2000). Acknowledgments K.E. Miller’s research was supported by funding from the Florida Fish and Wildlife Conservation Commission (FWC), the Florida Army National Guard, the University of Florida (UF), the North American Bluebird Society, a Sigma Xi Grantin- Aid of Research, and a Student Research Grant from Sandpiper Technologies, Inc. G. Jones, M. Williams, and A. van Doorn assisted with data collection, and FWC and UF provided administrative support. D.L. Leonard’s research was supported by the staff at Tall Timbers Research Station and UF. Mr. and Mrs. Jeptha Wade graciously provided access to the Wade Tract, and P. Doherty, K. Maute, and R. Ripley assisted with data collection. We thank M. Reetz, E. Stolen, and three anonymous reviewers for their comments on earlier drafts of the manuscript. Literature Cited Antworth, R.L. 2005. Florida Scrub-jay egg and nestlings predation: Snakes, conspecifics, and breeding parents. Florida Field Naturalist 33:115–122. Bontrager, L.R., D.M. Jones, L.M. Sievert. 2006. 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