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A number of strategies have been attempted to reduce predation on sea turtle nests, including lethal removal of the predator (Ratnaswamy et al. 1997; O’Connor et al. 2017), taste aversion conditioning (Ratnaswamy et al. 1997), placement of chili powder or habanero pepper around a nest (Lamarre-DeJesus & Griffin 2015; Lei & Booth 2017), and a cage or nest cover to prevent animals from accessing the nest (Broderick & Godley 1996; Ratnaswamy et al. 1997; Ali & Ibrahim 2002; Kurz et al. 2012; Lei & Booth 2017; O’Connor et al. 2017). Out of all these methods, the use of a nest cover is frequently cited as the most effective predation prevention strategy (Ratnaswamy et al. 1997; Kurz et al. 2012; Lei & Booth 2017; O’Connor et al. 2017). For example, O’Connor et al. (2017) found that controlling hunting foxes via lethal removal resulted in a 27% predation rate on sea turtle eggs, while the use of nest covers reduced the predation rate to 3%. However, nest covers that are not properly implemented can be ineffective, or in the worst-case scenario can actually attract predators that learn to associate a nest cover with incubating eggs (Niehaus et al. 2004; Isaksson et al. 2007). The use and design of nest covers therefore requires thoughtful and deliberate planning and should be tailored to the specific predators in a region (Isaksson et al. 2007; O’Connor et al. 2017). Additionally, nest covers designed in previous studies have been described as having certain disadvantages, including being expensive, heavy, challenging or time consuming to place on nests, and being fully enclosed such that hatchlings cannot crawl freely to sea without human intervention (Lei & Booth 2017; O’Connor et al. 2017). It is therefore important to understand the practicality of a nest cover design when determining its overall effectiveness as a conservation tool.

Our study has two central aims: 1) to determine the rate of predation, seasonal predation patterns, and identify the predator species of sea turtle nests on Playa Carate, Costa Rica, and 2) to test the effectiveness and practicality of bamboo nest covers as a method of preventing predation on sea turtle eggs.

Playa Carate is a 2.6 km long sea turtle nesting beach situated on the Osa Peninsula on the South Pacific coast of Costa Rica (between 8.436333 °N, -83.440139 °W and 8.442367 °N, 83.462083 °W). The most common sea turtle nesting on this beach is the olive ridley turtle (Lepidochelys olivacea), followed by the Pacific green turtle (Chelonia mydas). Hawksbill (Eretmochelys imbricata) and leatherback (Dermochelys coriacea) turtles also nest on this beach, though rarely. In the past few decades, this region has undergone considerable development due to a rise in the tourism and gold mining industries (Minca & Linda 2000). Carate has attracted a sizeable resident population despite the remoteness of the area, resulting in a relatively large population of both domestic and stray dogs. Being situated adjacent to Corcovado National Park, this region is also highly biodiverse and inhabited by a number of predatory animals that extend their hunting range beyond park boundaries and onto beach habitats (Kappelle 2016).

Surveys were conducted every morning from 1 May 2017 until 30 April 2018 by a trained employee of one of three sea turtle research and conservation organizations in this region: Frontier, Planet Conservation, and COTORCO. From May to December 2017, when the number of nesting turtles was highest, patrols were also conducted every night at mid-tide between 19:00 and 23:00. To minimize the disturbance of night patrols on nesting females, survey teams were limited to six people and only red lights were used. Both morning and night patrols consisted of walking the length of the beach looking for the presence of adult turtle tracks and predated nests.

When an adult turtle track was encountered, the following information was recorded: date, time, species, presence or absence of a nest, whether a bamboo cover was placed on the nest, and nest location. The presence of a nest was determined by carefully inserting a stick into the sand to locate the egg chamber, indicated by a marked change in resistance. If no egg chamber was detected, the track was marked as a “false crawl.” The species of turtle was verified either visually if encountered during night patrol or by the size and symmetry of the tracks of the nesting crawl.

The beach was divided into numbered sectors, marked by a painted wooden post every 25 m. Nest location was assigned by the sector in which the nest was found. Bamboo covers were distributed at sector posts along the beach and used opportunistically whenever a cover was available. Every new nest was assigned a nest number and given a marked wooden block tied to a stick placed one meter behind the nest or in the top right corner of a bamboo nest cover.

Figure 1. Left photo: a bamboo nest cover with pieces woven together and tied with hessian twine. Right photo: a bamboo nest cover secured in the sand by anchoring sticks into each corner and burying the edges of the cage in sand.

Bamboo nest covers were constructed by placing strips of bamboo approximately 1 m in length in a 7x7 grid formation (Fig. 1). Each strip was placed approximately 10 cm apart, a gap that was wide enough for hatchlings to emerge through the cover but narrow enough to inhibit digging by predators. If softer, more recently cut bamboo was used, the strips could be secured in place by weaving them together. If older, less malleable bamboo was used, the pieces were tied together using plastic or hessian twine. Nest covers were placed directly on top of turtle nests and secured in place by digging a sturdy stick into each corner and burying the cover in sand.

New nest covers were made at the beginning of each week, requiring between 10 - 20 minutes each to construct. Covers that were broken or washed by the tide to another area of the beach were collected for repair. Intact covers could be reused on subsequently laid nests. Nest covers were stored in piles along the beach so that a nest in any given sector could be protected when a cover was available.

Predated nests were identified based on the presence of animal prints, signs of digging (soft, recently disturbed sand), and the presence of broken or shredded egg shells on the surface of the sand in close proximity to the nest. Only freshly predated nests were recorded, as animals would often dig up previously predated or hatched nests for which data had already been recorded. A nest was identified as freshly predated based on the color and texture of the egg shells; newly predated eggs were soft and white, while old eggs were dried out and had a yellow tint.

When a newly predated nest was found, we recorded the date, time, nest location (sector), nest number, predator species, and presence/absence of a bamboo cover. Predator species was determined based on visual confirmation of the animal or animal footprints near the nest. The one exception was predation by crabs, which was recorded when an egg shell was empty with one small slit in the shell where the crab claw struck. The egg shells were counted to estimate the number of eggs that were predated. Broken shells were counted as a whole egg if more than 50% of the shell was intact. If the nest was only partially predated, the remaining surviving eggs were reburied in the chamber and the predated fragments were buried elsewhere. If a bamboo cover had not already been over the nest but was placed on after predation, this was noted in the data.

All statistical analyses were conducted using Microsoft Excel Version 1806 and RStudio Version 1.1.463. A generalized linear model (GLM) with a binomial error structure was calculated to test whether there was a significant relationship between a nest having a bamboo cover and the likelihood of it being predated. A result was considered statistically significant if p≤0.05. The risk ratio with 95% confidence intervals was also calculated to determine the relative probability of a nest being predated with versus without a nest cover. A risk ratio of 1 would indicate no difference in probability of predation across the two conditions, so a result was considered statistically significant if the confidence interval did not straddle 1.

During the study period 1,032 new nests were found on Playa Carate. Nineteen of the nests were identified as laid by Pacific green sea turtles, one was identified as laid by a hawksbill sea turtle, and the remaining 1,012 nests were identified as laid by olive ridley sea turtles. Another 277 false crawls were recorded, which included one leatherback turtle, 12 Pacific green turtles, and 264 olive ridley turtles.

Of the 1,032 nests found, 79 were relocated to a hatchery, 56 were poached the same night they were laid, and 6 were washed away by the sea immediately after being laid, leaving a total of 891 nests that could be subject to predation during the nesting season (including 39 nests that were relocated from one section of the beach to another). Out of these 891 nests, 133 experienced some level of predation over the course of the study, resulting in a predation rate of 14.9%. An additional 74 unmarked nests were also found to be predated throughout the season. A nest could have been unmarked either because the number label fell off or because surveyors had not seen the tracks after a nest was laid. The unmarked nests were not included in predation rate calculations, although these data contributed to our understanding of the active predators on Playa Carate. The average number of eggs predated per nest was 46.7. The average clutch size of olive ridley turtles at Playa Carate was 88.9 eggs per nest, based on 115 relocated nests that did not experience predation before relocation.

Table 1. Number of sea turtle nests laid, and number of nests predated each month of the study period. Predation rate = the number of nests predated in a given month divided by the number of nests laid that month x 100.

Three predated nests were green turtle nests and the rest were olive ridley nests. Two of the predated green turtle nests, as well as 46 olive ridley nests, were predated the same night they were laid. The remaining nests were predated on average 40 days after being laid. Olive ridley hatchlings tend to emerge 45-55 days after the eggs are laid (Maulany et al. 2012; Honarvar et al. 2016), meaning that nests were often predated close to the time of expected hatchling emergence. Peak nesting season occurred from July to August 2017 and from November 2017 to January 2018 (Table 1). The highest number of predations also occurred within these months, as well as in September 2017. Predation rate for the month was defined as nests predated divided by total nests laid that month and was highest in September 2017 by a large margin - nearly double that of the second highest predation rate. While relatively few nests were laid in September, there were many nests laid in the months leading up to it. We suspect that predators became habituated to finding food on the beach and continued to hunt frequently in September, thus increasing the predation rate. The predation rate was also relatively high in some of the quieter nesting months, such as May and June 2017. Bamboo nest covers should therefore be used all year round when possible, rather than just in the peak nesting season.

Out of the 207 recorded predated nests (both marked and unmarked), 123 (59.4%) predators were identified. Multiple predators were identified for 29 nests, with birds of prey and dogs having the most overlap (28 nests). When multiple predators were identified, it was not possible to distinguish how many eggs were predated by each type of predator. This may explain partially why birds and dogs appeared to predate a similar number of eggs per nest, as dogs and birds were commonly found predating the same nests. In cases where the specific bird of prey could be identified (the bird itself was seen rather than just footprints), the majority of bird predators were black vultures (Coragyps atratus) and turkey vultures (Cathartes aura). Less commonly, crested caracaras (Caracara cheriway) and black hawks (Buteogallus subtilis) were also found predating nests.

The data suggest that dogs and birds of prey caused the most overall damage to turtle nests (Table 2). This is consistent with several previous studies based in Costa Rica, which also reported dogs and vultures were the most prominent predators of both green and olive ridley nests (Fowler 1979; Burger & Gochfeld 2014). While crabs predated a significant number of nests, they tended to only predate a few eggs at a time and therefore the damage they caused to turtle populations was relatively low. Raccoons (Procyon cancrivorus or Procyon lotor) were identified as predators of turtle nests, though relatively infrequently compared to dogs and birds. White-nosed coatis (Nasua narica) were not identified as a predator on any occasion in our study. This was unexpected, as coatis are reported to be the primary predator of olive ridley nests in some regions of Costa Rica (Wainwright 2007) and have been observed predating nests on beaches adjacent to Playa Carate (Korein, E. unpubl. data). We hypothesize that the high number of dogs on Carate scare the coatis and racoons from this beach.

Table 2. Quantity and percentage (out of all 207 predated nests) of nests predated by each identified predator, as well as the average, minimum, and maximum number of eggs predated per nest by each identified predator.

Previous studies reported that vultures scavenged turtle nests that had been dug up by another animal, rather than digging up a nest themselves (Burger & Gochfeld 2014). In our study, most nests predated by vultures also had dog prints present, suggesting that a dog could have dug up the nest first. However, there were other nests for which only bird prints were found. Anecdotally, surveyors reported seeing crested caracaras actively digging up nests, while vultures were most often seen eating eggs already on or near to the surface. Black hawks were only seen consuming hatchlings as they were walking to sea, rather than predating eggs from a nest.

Dogs were the most frequently reported predator of turtle nests. We suggest managing predation by dogs to be the highest conservation priority because dogs have been anthropogenically introduced to this area and therefore do not play a natural role in the local food chain. Interestingly, the presence of dogs may scare away more natural predators to turtle eggs, such as coatis and racoons. Therefore, we sought to protect nests from dogs through the use of bamboo nest covers, rather than control numbers of dogs directly.

Throughout the season 213 bamboo nest covers were placed over newly laid nests. For calculating the effectiveness of bamboo nest covers at preventing predation, we excluded nests predated solely by crabs, because crabs dig into nests under the sand and cannot be stopped by bamboo nest covers. Of the nests with bamboo covers, 14 (6.6%) were predated. The predators of these nests were identified as either dogs, birds, racoons, or a combination of the three. Eight of these nests did not have a nest cover at the time that the surveyor found and collected predation data from the nest. We suspect that the bamboo cover was washed away by the tide or extreme weather (heavy rains and winds), exposing the nest to predators. In the remaining 6 cases, the animal had managed to either push the bamboo cover to the side or dig around and then under the nest cover.

In contrast, out of the remaining 678 nests that did not have bamboo nest covers, 119 (17.6%) were predated. A generalized linear model (GLM) with a binomial error structure revealed that nests without a bamboo cover were significantly more likely to be predated than nests with a bamboo cover (Table 3). A calculation of the risk ratio found that the probability of a nest being predated without a bamboo nest cover was 2.49 (95% CI: 1.50 - 4.15) times greater than the probability of predation with a nest cover. There were 8 cases when an uncovered nest was partially predated, and then surveyors placed a bamboo nest cover on top of the remaining surviving eggs. None of these nests were predated subsequently.

Table 3. Outputs for the estimates, standard errors, confidence intervals, z-values and p-values of the coefficients for the generalized linear model describing the effect of bamboo nest covers on predation. These outputs are reported in the logistic scale, as a binomial error structure was applied for the GLM. “No bamboo” is a categorical variable representing nests that did not have bamboo covers on them, while the intercept represents the variable where nests did have covers on them. The result was considered statistically significant (p<0.001).

Our data show that bamboo nest covers can reduce the rate of predation on incubating sea turtle eggs. Nest cover designs described in previous studies have harbored certain disadvantages, such as being expensive, heavy, difficult to carry long distances, challenging or time consuming to install, or being fully enclosed such that hatching turtles cannot pass the physical barrier of the cover to make their way to sea (Lei & Booth 2017; O’Connor et al. 2017). The bamboo nest covers used in this study were sturdy, lightweight and easy to move, simple to construct, inexpensive, and allow hatchlings to emerge and walk to sea without being blocked by the nest cover, making them an efficient and cost-effective predation prevention system that is well suited to this region of Costa Rica. Our data revealed that nests were often predated just before the typical time of hatching for olive ridley nests. This emphasizes the importance of having a nest cover design that allows hatchlings to leave the nest without being obstructed by the cover, eliminating the need to remove the cover and risk predation prior to hatching.

An additional benefit of bamboo nest covers is that they are more environmentally friendly than cover designs made entirely of plastic; this is especially true when hessian twine is used to tie bamboo pieces together rather than plastic twine. Should a bamboo cover be washed out by tides, only natural and biodegradable materials are at risk of entering the sea, rather than contributing to the burgeoning level of plastic debris in the ocean that can have detrimental effects on sea turtle health (Nelms et al. 2015).

There were some disadvantages to the bamboo nest cover design. Bamboo nest covers are time consuming to construct (approximately 10-20 minutes per cover), and mass production of them requires a team of people. High tides can dislodge bamboo covers and move them to other locations on the beach or drag them into the water, emphasizing the need to anchor covers into the sand with deeply buried sticks. Thin bamboo strips are prone to breaking if treated roughly or exposed to harsh conditions, and poorly tied twine can result in a nest cover falling apart. Freshly cut bamboo was found to be much sturdier and more durable than dry bamboo, and weaving bamboo pieces together was more effective than tying bamboo pieces together. If bamboo nest covers are to be used in other locations, bamboo must be readily available and abundant enough for continual use.

In conclusion, predation is a serious threat to sea turtle eggs in our study region of Carate, Costa Rica. Dogs pose the largest predatory threat, and there is evidence to suggest that dogs may scare away more natural predators. Bamboo nest covers are an effective and inexpensive method of reducing predation and should be used all year round. The most successful bamboo covers use hessian rather than plastic twine, are made from weaving freshly cut bamboo pieces together, and are secured into the sand with anchoring sticks in each corner. Depending on the resources available, nesting beaches in other regions around the world could use bamboo nest covers as a method of reducing predation on turtle eggs.

Acknowledgements. We acknowledge the hard work and commitment of the staff, volunteers and interns of Frontier, Planet Conservation and COTORCO. We give special recognition to the following individuals who significantly contributed to data collection and entry: Nina Cristiano, Jorge Cubillo, Iain Dobson, Tom Everley, Annabell Field, Neil Garry, Bella Jack, Enoc Jimenez Arias, Emma Johnstone, Jordan Leizert, Aoife Luscombe, Loreta Mikulyte, Ewan Quayle, Nicola Scott, Rebecca Sexton, Anjlie Shah, Tamara Spivey, Ella Wilkinson. Permits were distributed by Ministerio de Ambiente y Energía (MINAE) to Katya Barrantes, the lead biologist of COTORCO.

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