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Aggregations of olive ridley sea turtle (Lepidochelys olivacea Eschholtz, 1829) nests is associated with increased human predation during an arribada event
Article in Herpetology Notes · January 2019
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Introduction
Reproductively synchronous organisms breed at the same time as other members of their population (Ims, 1990). Hypotheses surrounding the selective advantages of synchronization include predator satiation, genetic benefits for the offspring, and conflict resolution for females, all of which can increase the probability of success for offspring (Bernardo and Plotkin, 2007).
Arribadas are mass breeding events performed by two species of sea turtles, olive ridley sea turtles (Lepidochelys olivacea Eschscholtz, 1829) and Kemp’s ridley sea turtles (L. kempii Garman, 1880). During arribadas, fertilized females congregate along nesting beaches and lay their eggs over the course of two to three days.
Arribada nesting females synchronize their oviposition with other members of their population leading to several thousand nests being laid on a beach in a single night (Hughes and Richard, 1974; Plotkin et al., 1997).
Despite the potential benefits of synchronous breeding, arribadas are less common among sea turtles than
solitary nesting. Even on beaches where arribadas occur, some females lay their eggs in between arribada events, when the number of nests laid in a night is similar to sea turtle populations that do not have arribadas (Hirth, 1980; Eckrich and Owens, 1995).
A proposed benefit of arribada nesting events relates to predator satiation (Bernardo and Plotkin, 2007).
Predator satiation occurs when the quantity of a specific prey at a given time exceeds the number that can be preyed upon by predators in the same area (Sweeney and Vannote, 1982). Predator satiation leads to inverse density-dependent mortality for many plant and animal species (Karban, 1982; Donaldson, 1993; Kelly, 1994).
Although arribada nesting may reduce the chance for predation due to predator satiation, it could also increase predation by attracting predators, such as coatis (Nasua narica Linnaeus, 1766) and dogs (Canis lupus familiaris Linnaeus, 1758) (Bernardo and Plotkin, 2007). Other negative density dependent factors include the destruction of nests and ejection of eggs from females ovipositing at a later date (Bustard and Tognetti, 1969;
Ocana et al., 2012), or a reduction in hatching success because of reduced O2 and increased CO2 levels in the nests (Honarvar et al., 2008). Beyond the natural threats to sea turtles, Ostional, Costa Rica is one of the few populations in the Neotropics where sea turtle eggs are harvested legally (Valverde et al., 2012). Since 1985, the government of Costa Rica has permitted qualified
Aggregations of olive ridley sea turtle (Lepidochelys olivacea Eschholtz, 1829) nests is associated with increased human
predation during an arribada event
Gregory R. Ruthig1,* and Alexis E. Gramera1
1 Department of Biology, North Central College, Naperville, Illinois 60540, USA
* Corresponding author. E-mail: [email protected]
Abstract. At Playa Ostional, Costa Rica, we related the spatial density of recently laid olive ridley (Lepidochelys olivacea) nests to their likelihood of being depredated by animals or humans. We conducted surveys once following an arribada (mass breeding) event, and once when females were nesting individually (non-arribada). Nests laid during the arribada were spatially aggregated along the beach, whereas nests on the non-arribada night were laid randomly along the beach. There was no association between spatial density and success of nests laid in the non-arribada night, but in the arribada night, nests that were laid in higher densities were more heavily depredated by humans.
Key Words. Arribada; Lepidochelys olivacea; Olive ridley sea turtle; Predator satiation
Gregory R. Ruthig & Alexis E. Gramera
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members of the community of Ostional to harvest olive ridley eggs, but only during arribada events (Campbell et al., 2007).
The social aggregation of olive ridley turtles occurs only during breeding events (Plotkin et al., 1995) suggesting that any adaptive benefit of the behaviour arises in improved mating or breeding. Our objective was to test the benefits of arribadas for olive ridley turtles on nest success in the first night after egg-laying, when nest predation is highest (Gallagher et al., 1972;
Davis and Whiting, 1977; Hopkins et al., 1979; Nellis and Small, 1983). We made our observations during an arribada event and also on a night when turtles displayed solitary nesting (non-arribada). Our hypotheses were that high densities of nests would decrease animal predation because of predator satiation, but human predation would increase due to legal harvesting during the arribada.
Materials and Methods
We tested the effect of spatial density of olive ridley nests on the early survivorship of offspring during both arribada and non-arribada nesting breeding events. We surveyed non-arribada nests on the night spanning 19 and 20 September 2014 and arribada nests on the night spanning 19 and 20 November 2014 at Playa Ostional, National Wildlife Refuge of Ostional in the Nicoya Peninsula, within the Guanacaste Province of Costa Rica on the Pacific Ocean (10.0114°N, 85.7201°W). During the non-arribada event, it was illegal to harvest sea turtle eggs, whereas during the arribada we observed a large number of people excavating fresh nests and collecting eggs (Valverde et al., 2012).
The beach is over 4 km long and 30-40 m wide.
We used pre-existing 50 m markings along the upper boundary of the beach that are maintained by the Minesterio de Ambiente y Energía (MINAE) Ostional Station. We marked off 10 m adjacent belt transects within each 50 m section and surveyed between the high tide line and the vegetation line on the beach. The water line varied between transects so there was some variation in the total area of available nesting beach among the transects. For the solitary nest survey, every nest location was included in the survey. Due to the high number of nests during the arribada event, we randomly selected 100 10 m belt transects.
We identified nesting sites from the previous night by walking along the high tide line, starting at 5:30 in the morning. We counted the number of nests in each transect and assigned a specific fate: successful, depredated by
animals, depredated by humans, destroyed by beach collapse, or aborted (Fig. 1). We did not include aborted nest attempts in our analyses (except for analyses that tested the influence of nest density on aborted nest frequencies) because we could not determine if a female who aborted her nest attempt returned to the beach elsewhere to lay her eggs (Eckert, 1987).
We tested whether solitary-nesting females or arribada-nesting females spatially aggregated (clumped) their nests. We calculated the mean and the variance of the number of nests laid in each 10 m transect to test whether the observed nests had either an even, clumped, or random distribution along the length of the beach.
We used the model
,
where D is the measure of dispersion, δ2 is the variance and μ represents the mean number of nests within each transect. If nests were laid randomly along the beach, the mean number of nests would equal the variance. If nests were evenly dispersed, the mean would be less than the variance, and if the nests were spatially clumped, the variance would be greater than the mean (Cox and Lewis, 1966). We performed a χ2 goodness of fit test to determine if the mean/variance ratio was significantly different than one. The expected values for the number of transects with m nests if D = 1 was calculated by the formula
(Whitlock and Schluter, 2015), where μ is the mean number of nests per transect and X is the number of nests in a transect.
To determine whether nests from arribada or non- arribada nesting events were more likely to be successful, depredated by humans or animals, or be destroyed by beach collapse, we used a χ2 test of association.
For both the arribada and non-arribada nesting events, we tested whether there was a relationship between nest density in a 10 m transect and nest fate (nests with partial animal or human predation were considered depredated). Because of the low number of nests during the solitary breeding event, we performed a χ2 test of association between density of nests and whether they were successful or depredated by humans or animals.
For the arribada event, we used three linear regressions using SPSS (IBM, Armonk, New York, USA) to test whether the number of nests in a transect influenced
,
what proportion of nests in the transect was successful, human depredated, or animal depredated.
We also tested whether the number of nests in a transect influenced whether turtles aborted their attempts to nest.
Aborted attempts were identified by false crawls onto the beach (Fig. 1B). Because of the low number nests during the solitary breeding event, we performed a χ2 test of association between density of nests in a 10 m transect of beach and recorded false crawls. For the arribada event, we used ordinal regression using SPSS (IBM, Armonk, New York, USA) to test whether the number of nests within a 10 m transect of beach affected the number of aborted nest attempts in that transect.
Results
We measured density and the fate of nests among solitary nesting and arribada nesting olive ridley females. During the non-arribada breeding event we observed 34 solitary nests along the 4 km stretch of beach. The mean number of nests within the 400 10 m wide transects was 0.085 ± 0.02 SE. During the arribada event, the mean number of nests within the 100 10 m wide transects was 6.19 ± 0.55 SE. The nests laid during the non-arribada event did not significantly differ from a random distribution (D = 1.135; χ2= 2.66; p-value = 0.26; df = 2; Fig. 2) but arribada nests were laid in an
Figure 1. Images of four nest fates; A: Successful, B: Aborted (false crawl), C: Animal Depredated, and D: Human Depredated.
Human depredated nests were identified by smooth sides formed by shovels. The excavated holes of animal depredated nests were dug on a shallower angle.
aggregated distribution (D = 4.70; χ2 = 1112.77; p-value
< 0.001; df = 19; Fig. 2). Using a test of association, we found that there was not a significant association between nesting strategy (arribada vs. non-arribada) and whether the nests were successful, depredated by animals, depredated by humans, or were destroyed by beach collapse (Fig. 3; χ2 = 0.66; p-value = 0.88; df = 3).
Density (measured as number of nests per 10 m stretch of beach) did not have a statistically significant effect on whether the non-arribada nests were successful or depredated by humans or animals (χ2 = 0.17; p-value = 0.92; df = 2). For the arribada, nest density decreased nest success (R2 = 0.048; p-value = 0.048; Fig. 4A), decreased animal predation, but not significantly so (R2
= 0.023; p-value = 0.176; Fig. 4B), and increased human predation (R2 = 0.131; p-value = 0.001; Fig. 4C).
Gregory R. Ruthig & Alexis E. Gramera
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Figure 2. Distribution of nesting olive ridley sea turtles during a non-arribada nesting night and during an arribada. The map of the beach is aligned to the meter marks on the graphs. The zero mark on the beach was at India Point at the north end of the nesting beach.
In the non-arribada breeding night, only two nest attempts were aborted, one in an otherwise empty transect and one with another nest in the transect. The aborted nest attempt in the transect that contained a nest may have been the same female making two attempts to lay her eggs. For the arribada event, the ordinal regression that tested whether the number of nests in a plot predicted the number of aborted nest attempts in that plot found no significant effect (χ2 = 0.41; p-value
= 0.52; df = 1).
Discussion
Olive ridley sea turtles (Lepidochelys olivacea) display a wide range of nesting behaviour, ranging from temporal and spatial aggregations of nests to solitary nesting. In our study, nests that were laid during a non- arribada night were randomly distributed along a 4 km nesting beach, whereas nests laid during an arribada event were clumped spatially. Our hypothesis that predator satiation would lead to lower rates of predation was not supported; the arribada event had much higher densities of nests along the beach, but animal predation was not reduced. Even within the arribada event, stretches of beach with the highest densities of nests did not have reduced animal predation. Overall there was no difference in human predation between the arribada and non-arribada events (Fig. 3). However within the arribada event, human predation increased along stretches of beach where nest densities were high, supporting our hypothesis and lowering the overall success rate of nests in high density areas (Fig. 4).
Overall, there were no significant differences between the arribada and solitary nesting events in the rates at
which the nests were depredated by humans or animals (Fig. 3), however our results may be diluted by the fact that some of the nests laid during the arribada event were on the periphery of the mass nesting and were laid in densities that were similar to the non-arribada night (Fig. 2). The most visible animal predator on the beach were domestic dogs (Canis lupus familiaris).
We also saw many black vultures (Coragyps atratus Bechstein, 1783) consuming eggs but they did not seem capable of excavating a nest without the assistance of another animal or a beach collapse. In some cases, animals had taken advantage of the holes excavated by Figure 3. Fate of nests during an arribada (n=619) and a non-
arribada (n=34) breeding event. There was not a significant association between breeding strategy and the fate of the nests in their first night.
Figure 4. The proportion of nests that were successful (A), depredated by animals (B), or depredated by humans (C) in their first night after being laid and the number of nests laid within a 10 m belt transect along Playa Ostional. The lines represent least squares linear regression.
humans, making it difficult to determine if a human had depredated the nest. We used the evidence of shovel marks and a vertical hole to identify human predation (Fig. 1).
Our arribada survey occurred during a time when legal harvesting of nests was allowed. During arribadas, people from the town of Ostional work together to collect and package turtle eggs for personal consumption and to sell to other communities in Costa Rica. The reason for allowing human consumption of eggs during arribada events is that nesting females may inadvertently dig up the nests of earlier females during these events. Not surprisingly, nest predation by humans was highest near the town of Ostional near where human population density is highest (Fig. 2). The town was located near the highest density of nests, leading to a positive relationship between nests and their likelihood of being depredated by humans (Fig. 4). The impact of the egg collection on the population of olive ridley turtles is unclear, but can represent a large source of mortality for the eggs in some arribada events (Valverde et al., 2012).
Although the first day after nests are laid is important in terms of predation (Nellis and Small, 1983), breeding synchrony may influence turtles at later stages, especially when the hatchling turtles emerge and swim out to sea, suffering high predation (Witherington and Salmon, 1992). Predator satiation increases hatchling survivorship if many hatchlings emerge synchronously (Peterson et al., 2013; Santos et al., 2016).
An alternative explanation for arribadas is that they are a by-product of mass mating events. Mass mating can increase access to mates and increase genetic diversity in offspring (Bernardo and Plotkin, 2007). Female turtles may be able to choose mates or have their eggs fertilized by multiple mates, ensuring that at least some of their offspring are fertilized by high quality males.
The females of many animal species have a choice of which partner’s sperm will fertilize their eggs after having multiple mating partners (Yasui, 1997). Choice can increase offspring performance and the sexual attractiveness of sons, ultimately elevating offspring fitness (Jennions and Petrie, 2000). Wolf spiders have increased lifetime offspring production from multiple mating, despite the negative effect on female longevity (Arnqvist and Nilsson, 2000). In ridley sea turtles, synchronized breeding potentially increases access to multiple mates for females (Jensen et al., 2006), but the potential fitness effects remain unknown.
Acknowledgments. We thank Marco V. Martinez for advice on experimental design and statistical techniques. Emily Prather- Rodgers, Chandreyee Mitra, and Charles Knapp provided valuable suggestions on the manuscript. Sharon Hsu and Diego Ramirez were instrumental in helping organize and conduct the field work in Ostional. We received a research permit from Sistema Nacional de Áreas de Conservación (SINAC) Costa Rica (Permit ACT-OR- DR0135014). This research was supported by the College Scholars Program, directed by Perry Hamalis at North Central College.
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