Possible Effect of Global Climate Change on Caretta caretta (Testudines, Cheloniidae) Nesting Ecology at Guanahacabibes Peninsula, Cuba

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1 Chelonian Conservation and Biology, 2017, 16(1): doi: /ccb Ó 2017 Chelonian Research Foundation Possible Effect of Global Climate Change on Caretta caretta (Testudines, Cheloniidae) Nesting Ecology at Guanahacabibes Peninsula, Cuba JULIA AZANZA-RICARDO 1,2,*,MARÍA E. IBARRA MARTÍN 2,,GASPAR GONZÁLEZ SANSÓN 2,3, EMMA HARRISON 4,YOSVANI MEDINA CRUZ 5, AND FERNANDO BRETOS 6 1 Instituto Superior de Tecnología y Ciencias Aplicadas, CP 10400, Ciudad Habana, Cuba [julia_dragmarino@yahoo.es]; 2 Centro de Investigaciones Marinas, Universidad de La Habana. Calle 16 No. 114 e/1ra y 3ra, Playa, CP 11300, Ciudad Habana, Cuba; 3 Departamento de Estudios para el Desarrollo Sustentable de Zonas Costeras, Universidad de Guadalajara, Gómez Farías 82, San Patricio- Melaque, Cihuatlán, Jalisco, CP [gaspargonzalez2001@yahoo.es]; 4 Independent contractor [harrison_emma@hotmail.com]; 5 Marina Marlin Azulmar, Club de Pesca Cayo Largo, MINTUR, CP [yosvanimedina@gmail.com]; 6 Cuba Marine Research & Conservation, Patricia and Phillip Frost Museum of Science, 3280 South Miami Avenue, Miami, Florida USA [fbretos@frostscience.org] *Corresponding author ABSTRACT. Changing climate is affecting life all over the world. The loggerhead turtle (Caretta caretta) is one of the most vulnerable turtle species to climate change, particularly with regard to sex determination being affected by high temperatures in most nesting areas, such as the Cuban archipelago. As yet, species information is scarce for the Cuban archipelago as a whole. This study provides information about loggerheads in order to determine the possible effects of climate change on this species, especially in Guanahacabibes. We monitored 10 beaches along the southernmost coast of the Guanahacabibes Peninsula for 18 yrs ( ), from May to September of each year, to determine nesting activity and density. Females were measured and tagged and the remigration interval was determined. Temporal variation was reflected in apparent peaks in reproductive activity on a biennial cycle. We found intraseasonal variation with the highest nesting activity in June, with a 15% increase in nesting activity in the second half of that month. Reduction in clutch size, incubation period, and hatchling size, as well as a potential feminization of hatchling production, indicates a possible effect of climate change in reproductive success. Our results are a first attempt at characterizing Guanahacabibes populations and have great value for establishing conservation priorities such as the protection of the nesting females and control of incubation environment in the face of global climate change within the context of national management plans. KEY WORDS. Cheloniidae; loggerhead turtle; climate change; reproductive success; Cuba Although loggerhead populations are widely distributed in the Atlantic, Fisher et al. (2014) determined that the fate of the Atlantic loggerhead sea turtle is uncertain, mostly due to anthropogenic threats at most beaches in the United States (Antworth et al. 2006) and the increasing impact of climate change. An increase in temperature will not only greatly affect the population of nesting females by altering beach characteristics or reducing the number of suitable ones, but also in hatchling growth and performance on its way from the nest to the sea, which could compromise overall hatchling survival (Fisher et al. 2014). Loggerhead vulnerability to climate change is mainly a result of the increased risk of nest flooding (Reece et al. 2013; Shaw 2013). This finding is stark considering that 32% of the current area of marine turtle nesting beach habitat in the Caribbean will be at risk if a 0.5-m rise in sea level occurs (Fish et al. 2005). This is of special concern in the Caribbean islands, where beaches are narrower than continental ones and because loggerheads frequently lay Deceased. close to the hide-tide line (Azanza et al. 2013). Other possible impacts of climate change are a shift in nesting areas, resulting in increased crowding on narrowing beaches (Reece et al. 2013) and a decrease in food resources (Chaloupka et al. 2008). Moreover, the future of some key nesting areas in the United States, where most loggerhead nesting in the Wider Caribbean region occurs (Dow et al. 2007), may be in the hands of decision makers and politicians that are still reluctant to plan for future sea level rise scenarios (Hernández 2014). At regional levels, relationships between turtle nesting cycles and climate change have already been identified (Van Houtan and Halley 2011). Cuba is the only country in the Caribbean with several loggerhead nesting sites having over 100 nests (Dow et al. 2007), all located in the southwest part of Cuba (Moncada- Gavilán et al. 2014). Cayo Largo, in particular, is the main Cuban nesting site followed by El Guanal in the south of Isla de la Juventud and Cayos de San Felipe (Nodarse et al. 2010), which is also becoming an important nesting site

2 AZANZA-RICARDO ET AL. Loggerhead Nesting Ecology and Climate Change 13 Figure 1. Location and classification of studied beaches in Guanahacabibes Peninsula, Cuba, according to the level of monitoring (index and secondary) and their position on the peninsula (interior and exterior or western and eastern). (Azanza et al. 2013). However, scarce information is available for the Cuban archipelago as a whole (Nodarse et al. 2010; Azanza et al. 2013), and nothing has been published about the species ecology in Guanahacabibes, the westernmost population and the only one with nocturnal monitoring (Azanza-Ricardo et al. 2015). To date research has focused on green turtles because they are the most abundant nesting species in Cuba (Azanza- Ricardo et al. 2013), and hawksbills because they are the most endangered of the 3 species that nest in Cuba (Moncada-Gavilán et al. 2014). Considering the importance of Cuban loggerhead nesting sites in the Antillean context and the threats they might be facing due to climate change, here we present the first ecological characterization of the Guanahacabibes nesting population of loggerhead turtles. The focus of the study was the spatial and temporal variation in nesting behavior and corporal measurements of gravid females during systematic nocturnal monitoring as well as variation in reproductive and hatching success as indicators of possible impacts of climate change on this nesting population. METHODS Study Site. The study was carried out at 10 beaches located on the southern coast of the Guanahacabibes Peninsula (from N, Wto N, W). The selection of beaches followed the same criteria detailed in Azanza-Ricardo et al. (2013) regarding the relative abundance of marine turtles at each location: 5 beaches with more than 50 nests per season were patrolled every day during the night while another 5 beaches with lesser nesting activity (number of nests between 10 and 25) were patrolled during the day every 2 or 3 d). Sampling Design. Data were collected from 1998 to Up to and including the 2010 season, monitoring was performed following the protocol of Azanza et al. (1999); after 2010, data were collected according to the Cuban National Marine Turtle Protocol (Moncada-Gavilán et al. 2013). Basically both protocols include measurements of females, tagging, nest counting, and analysis of hatching success; however, some new measurements were added in the latter one such as nests coordinates, depth, and track direction as well as threats identification. Systematic monitoring (defined as beach patrolling at least every 3 d) was conducted each year from mid-may through the end of August, which corresponds to the nesting season of the loggerhead as reported by Márquez (1996) for the Caribbean region. Rangers from Guanahacabibes National Park determined the date when the first nesting attempt occurred every year. The date when the first track was reported was considered the beginning of the season, and the end of the season was the last date when any nesting activity was recorded. Each season was divided into 15-d intervals to determine more precisely the peak in nesting; the first interval corresponded to the second half of May and the last interval was the second half of August. Since the tagging program began in 2001, patrols have been conducted every night from 9:00 PM to 6:00 AM during the entire monitoring season at 5 index beaches (Antonio, Perjuicio, La Barca, El Holandés, and Caleta de los Piojos) as shown in Figure 1. These beaches were selected due to the high nesting density and their accessibility. As such they are categorized as index beaches. Index beaches are defined as nationally referenced beaches that experience more thorough conservation and monitoring efforts. All females encountered were measured and flippertagged in the right front flipper between the first and second scale using Inconel tags (Style 681, National Band and Tag Company). Turtles were tagged to determine nesting frequency (the number of times tagged females

3 14 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number nested successfully in a single season) and remigration interval (time period between successive nesting seasons). With this information, mean remigration interval per year was determined. Straight carapace length (SCL) notch-totip was measured with a caliper from the anterior point at midline (nuchal scute) to the posterior tip of the supracaudal scutes (distal border of the carapace closer to the tail) of 15 hatchlings per nest. Hatchlings were selected at random and measured within an hour of reaching the surface of the nest after emergence; they were released immediately after measurements were taken. If possible, a direct count of the number of eggs was made during oviposition. Diurnal monitoring was also performed at another 5 beaches (Las Canas, Resguardo, Las Cadenas, Caleta Larga, and Cayuelos). Surveys were conducted at least once a week, sometimes twice, to determine the total number of nests laid. During track surveys all tracks were recorded and categorized as a nest, a false crawl, or a recognition track. A false crawl is defined as an event where a turtle crawled onto a beach and attempted to nest but aborted, whereas a recognition track is a crawl in which no nesting attempt was made. Nests were located by carefully probing the sand using a thin stick until a difference in compaction of the sand was felt, which indicated the location of the egg chamber. Oviposition date was estimated by the percentage of coverage of the egg with an opaque band (less than 100% opacity means that the nest is 7 d old or less; in other words, an egg that is lighter in color and lacking a distinct band is an older one) or by the condition of the track when there was no nest. Overall nesting density was calculated by dividing the total number of nests by total beach length, in kilometers, for all beaches. Expected number of nesting females was determined by dividing the total number of nests by the average nests per females determined for the area, while the number of nesting females detected was determined from the tagging program. Nesting success (i.e., the proportion of successful nesting attempts) was determined by dividing the total number of nests by the total number of tracks. To assist with monitoring, the location of each nest was marked by inserting a thin rope into the nest chamber, which was then attached to a labeled stake placed m from the nest. All the information regarding each nest (i.e., the date, position at the beach, egg number, and female information) was included in a data field sheet. When the estimated hatching date was close, nests were monitored daily until evidence of emergence was observed. HOBOt Onset Pendant sensors were placed in the middle of 4 nests, 2 in 2013 and 2 in 2014 in La Barca Beach, and recorded the temperature synchronously every 2 hrs throughout the incubation period. At the end of the incubation period, the data were downloaded and converted to a format compatible with Excel using the HOBOwaret Onsett Computer Corporation software. Data Analysis. Prior to analysis, data were tested for normality and variance homogeneity using a Kolmogorov-Smirnov and a Levene s test, respectively (Sokal and Rohlf 1995). A comparison between the numbers of nests in high vs. low nesting seasons was made using a Student t-test. Seasons were classified as high if the total of nests increased by at least 10, with respect to the previous season, and low if there was a decrease of at least 10 nests. Regression analysis was used to determine the relationship between season duration and year. Pearson s correlation was used to determine if there was any tendency in nest number during the study period. The number of nests laid within each of the 7, 15-d intervals was transformed into a percentage of the total number of nests; this relative frequency was compared using a Kruskal-Wallis test, at 3 different 6-yr periods, years , , and , to determine if there was any variation in the nest frequency over time within the season. A Student- Newman-Keuls (SNK) test was used for multiple comparisons. The significance of the observed differences was evaluated with the program STATISTICA version 7.0 for Windows. In each analysis, a level of significance of p 0.05 was used. RESULTS Nesting by loggerhead turtles represented only about 3% of the total turtle nesting reported in the Guanahacabibes Peninsula, meaning the number of loggerhead nests per season was very low: between 0 and 48 (Fig. 2). A significant increase in the annual number of loggerhead nests has been observed during the 18 yrs of the study (Pearson, r = 0.48; p = 0.04), with record nesting seasons in the last 3 yrs and the difference in nest number between consecutive low and high nesting seasons increasing significantly over the years (Pearson, r = 0.85; p = 0.03). Very few loggerhead turtles were tagged each season (on average, only 2/yr), except in 2004 when 14 females were tagged, giving a total of 49 individuals tagged in the 15 yrs since Because of the low number of turtles tagged, few returning migrants have been identified (11 in total, equivalent to 22.5% of all turtles tagged). Successful nesting occurred in approximately 67% 6 17% SD of emergences. This value varied between years (37% 95%) and it remained fairly consistent among the beaches studied (67% 6 10% SD). In general nesting was low in May, increased to a peak around mid-june, and then declined through to the end of August; these differences between nest numbers in each 15- d interval were statistically significant (Fig. 3). The mid- June peak is maintained over time in the first 10 yrs, but after 2015, the rate of nesting increased in the first half of June and in 2015 the peak moved to May (Fig. 3). A significant negative relationship was found between the middle and the end of the season and the years (Fig. 4). The end of the season date occurred 36 d earlier in 2015 compared with 1998.

4 AZANZA-RICARDO ET AL. Loggerhead Nesting Ecology and Climate Change 15 Figure 2. Number of loggerhead nests recorded each nesting season in the Guanahacabibes Peninsula, Cuba, Clutch size averaged 93 eggs among all nests during the study period (sample size from 7 to 22 nests per year), but a significant negative correlation was found between the number of eggs laid and year (r = 0.61; p = 0.02), suggesting that the average number of eggs per clutch is decreasing over time. Nevertheless, female size did not vary over time (r =0.18; p = 0.53). A decrease in hatchling size was observed over the study period (Fig. 5, left). Mean SCL diminished by 2 mm between successive analyzed years ( and ) and by 4 mm in total (p, 0.01). The same decreasing trend was observed for incubation period (p = 0.01), with a difference of 9 d between the incubation period in 2002 compared with 2013 (Fig. 5, right). Correlation between mean incubation period and years was strongly negative (r = 0.81; p, 0.01). Incubation temperatures of 4 nests were recorded (Table 1). Average temperature of 3 of the nests was above 318C. The difference in temperature between the middle third of incubation and the overall incubation period was less than 0.88C in all cases (Table 1). Incubation periods are close to the calculated population mean, but emergence success was higher than the population mean of Guanahacabibes in 3 of the nests and considerably lower in the fourth nest. DISCUSSION The Guanahacabibes loggerhead nesting population, although small compared with other populations, exhibits important signs of recovery with a positive trend in nest number per season and high levels of hatching success. Annual nest number corresponds more with the average nesting levels of the majority of the southern Caribbean s rookeries (41%), with fewer than 25 nesting females per year. Inside the Cuban archipelago, Guanahacabibes is confirmed as the fourth nesting population according to the number of nests (and third highest nest density) following Cayo Largo, Isla de la Juventud, and San Felipe Figure 3. Cumulative number of loggerhead nests through the reproductive season at Guanahacabibes Peninsula, Cuba. The analyzed duration was divided in 4 periods of 5 yrs each starting with the first year with the lighter pattern to the fifth year with the darker pattern.

5 16 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number Figure 4. Temporal variation of loggerheads at the middle and end of the nesting season at Guanahacabibes Peninsula, Cuba. The 95% confidence intervals are presented around the regression lines. For 1998 and 1999, the middle of the season could not be determined because data collection started after the beginning of the season. (Moncada-Gavilán et al. 2014). Low nesting rates for the Guanahacabibes loggerhead nesting population could be the result of the high frequency of hurricanes in the area. Dewald and Pike (2013) found that most loggerhead nesting occurs in areas with moderate hurricane frequencies. Nevertheless, the sustained increase in nest number observed in the 4 latest nesting seasons is an encouraging trend that might indicate an increase in the Guanahacabibes loggerhead population. In addition, nesting success (67%) in Guanahacabibes is also higher than other nesting areas such as in Florida, where Antworth et al. (2006) reported a 55% nesting success and in North Carolina where, on average, there were 1.43 false crawls for every nest (Hernández 2014), also indicating good nesting conditions for Guanahacabibes beaches. Biennial nesting patterns of this population have been stable over time. Evidence for a biennial cycle found in our work has also been reported in Guanahacabibes for green turtles (Azanza-Ricardo et al. 2013), but this pattern has not been described for loggerheads in larger nesting populations (Weishampel et al. 2004; Antworth et al. 2006; Reece et al. 2013) in Florida or elsewhere in Cuba, except for the last 4 nesting seasons (Moncada-Gavilán et al. 2014). The timing of the loggerhead nesting season in the Caribbean is very similar among sites and occurs mostly from May to August with a peak in June (Márquez 1996; Aiken et al. 2001; Antworth et al. 2006), which corresponds to our findings. As in Lamont and Houser (2014), nesting ended in August, although in their findings Figure 5. Temporal variation of hatchling size (left) and incubation period (right) for loggerheads at Guanahacabibes Peninsula, Cuba. Letters represent statistical differences among means. Only the years with more than 3 samples are presented.

6 AZANZA-RICARDO ET AL. Loggerhead Nesting Ecology and Climate Change 17 Table 1. Summary of incubation temperatures in loggerhead nests at Guanahacabibes Peninsula, Cuba, and their respective emergence success and incubation period for the years Nest id # Emergence success (%) Incubation period (d) Overall incubation temperature (8C) Middle third incubation temperature (8C) Mean 6 SD Minimum Maximum Mean 6 SD Minimum Maximum no nests were recorded after the first half of the month. In contrast, an interesting pattern is appearing in some loggerhead nesting areas where the peak of the season is occurring earlier in the season (Weishampel et al. 2004; Hawkes et al. 2005; Pike et al. 2006). Although this shift in timing of the peak of the reproductive season was reported for northern Atlantic nesting populations, it was also found for the Guanahacabibes population (Fig. 4). In addition, the end of the season is shifting to an earlier date. This could be the result of temperature rise and requires further evaluation. Mazaris et al. (2008) made an interesting analysis of the relation between sea surface temperature and duration of nesting season and concluded that a complex system of many environmental and demographic factors must be influencing nesting duration, as different results of the relation between these 2 variables were found in different nesting populations (some of them opposites). Pike et al. (2006) also found correspondence of the duration of nesting season with sea surface temperature for loggerhead but not for green turtles (Pike 2009), confirming that loggerheads are highly sensitive to temperature variation. The size of nesting females showed no significant change over time, as also found by Hawkes et al. (2005). However, clutch size did change. In the Antworth et al. (2006) study, clutch size also varied significantly over time, and the mean clutch size ( ) is similar to that found in Guanahacabibes ( nests). Aiken et al. (2001) argued that populations breeding at optimal conditions may experience a decline as temperature increases, which might also be the case in Guanahacabibes. The mean incubation period for Guanahacabibes loggerheads is greater than others north of the Caribbean region, such as Hutchinson Island in Florida, where the average incubation period was less than 50 d with average incubation temperatures greater than 318C (Hanson et al. 1998). On the other hand, the mean incubation time for populations in the Cayman Islands, located closer but to the south of the Cuban archipelago, was longer than Guanahacabibes at 57 d (Aiken et al. 2001). Although few nests could be surveyed to determine incubation temperatures, recorded values are within the interval of average incubation temperatures described for Florida beaches: C (Hanson et al. 1998). Despite this variation in incubation period compared with other areas, the reduction observed over the years in incubation time and hatchling size is significant. Janzen (1993) determined that hatchling size and fitness are affected by high incubation temperatures; as a result, Glen et al. (2005) suggested that hatchlings developed in high-temperature environments are less vigorous. Pike (2014) indicated that changes in nest temperatures might significantly alter hatchling phenotypes. In summary, because temperature in Guanahacabibes is rising and loggerhead hatchlings are becoming smaller, it is quite possible that the fitness of the offspring that have been produced in those beaches has been compromised, and this could increase mortality in the first stages. Because Guanahacabibes loggerhead turtles are nesting within 10 m of the high-tide line corresponding to the bare sand area and no change in nest position has been detected yet, a progressive increase in incubation temperature is anticipated. Glen et al. (2005) determined a negative relation between hatching success and temperature. As a result, not only could hatching success be affected, but sex ratios as well. Estimates indicate skewed proportions toward female production because the incubation period is below the 53-d limit proposed by Mrosovsky et al. (1999), when 100% females are expected, because shorter incubation periods indicate higher incubation temperatures. In correspondence, incubation temperatures of the 3 monitored nests are above the pivotal temperature described for the species (29.38C) when Mrosovsky et al. (2002) confirmed female production greater than 50%. Increasing temperatures are a concern for scientists who are already looking for measures to prevent high temperatures in marine turtle nesting areas (Wood et al. 2014). In summary, the Guanahacabibes loggerhead nesting population shows signs of recovery considering the positive trend in the annual nest number as well as the high hatchling emergence rate. It is vital to maintain the conservation program in the area to ensure that these trends persist in the future. Nevertheless, some results indicate a potential impact of climate change on the health of the population such as shortening of the nesting season and reduction in clutch size, incubation period, and hatchling size as well as potential feminization of hatchlings. Although these results are of great concern for the health of the population, some of the actions that could be taken are not possible in the local context. Active

7 18 CHELONIAN CONSERVATION AND BIOLOGY, Volume 16, Number management of incubation temperature could be performed, but this alteration of natural conditions often can be more harmful than beneficial for embryonic development. Additional analysis and monitoring of these variables are required to apply adequate management policies to guarantee a positive future for the westernmost Cuban loggerhead nesting population. ACKNOWLEDGMENTS This research was supported by the World Wildlife Fund Program in Cuba, The Ocean Foundation, and the Southern Archipelago United Nations Program for Development project. We would also like to acknowledge the joint PhD program of the Universidad Autónoma de México (UNAM) Universidad de La Habana and The Academy of Science for the Developing World (TWAS). We especially want to acknowledge the efforts of the more than 2300 volunteers who helped collect field data during the 18 yrs of the study. 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