Influence of Sandy Coast Vegetation on the Reproductive Success of Green Turtles at Cuban Nesting Beaches
Abstract
Vegetation has been shown to influence nest environment (temperature, humidity), affecting hatchling's development as well as emergence success, and has also been used as a cue during the selection of a nesting site. For green turtles, Chelonia mydas, nest density is typically higher in the vegetated zones. This study evaluated the influence of vegetation presence and percent cover on the nesting success and embryonic development of green turtles in Guanahacabibes Peninsula, Cuba. The vegetation cover had a positive and significant relationship with the number of nests (r = 0.56, p = 0.01, n = 17). Two vegetation patches are identified with different vegetation cover values: 29% for the first (closer to the high tide line) and 37% for the second. We found the highest nesting success (70%) and nest relative frequency (15% of total nesting) around the first patch of vegetation. Median hatchling emergence success was 88% (40%–96%, n = 54) in the first patch and 93% (78%–100%, n = 40) in the second. The incubation period was lower in the first patch (mean = 51 d, range = 48–60 d, n = 44) and higher in the second (mean = 54 d, range = 45–67 d, n = 39). This is the first study that reveals the positive impact of sandy coast vegetation on Guanahacabibes' green turtle nesting and will be useful in conservation actions such as native vegetation restoration plans and temperature control using shade management with vegetation.
The impact of vegetation on sea turtles' reproductive success has been previously evaluated in the scientific literature (Conrad et al. 2011). It has been verified that vegetation affects the selection of their nesting site because different species select where to nest based on the vegetation of the beach (Horrocks and Scott 1991; Hays et al. 1995; Kamel and Mrosovsky 2006) and, as a result, female reproductive success varies. The study conducted by Chen and Cheng (1999) on Wan-An Island, Penghu, Taiwan, found that Chelonia mydas prefers to nest in vegetated areas over areas lacking vegetation. Kelly et al. (2017) state that C. mydas nest density is higher in the vegetated zones, although nesting still occurs on the unvegetated zone of beach, which indicates the variability in nest-site selection of this species.
The early stages of a marine turtle's life cycle are the most vulnerable because of the many threats affecting embryonic development and the survival of offspring, such as nest flooding (Formia 2002; Ditmer and Stapleton 2012), predation (Caut et al. 2006), and moisture below 25% (McGehee 1990) or above 75% (Pike et al. 2015). Hatching and emergence success depends on the interaction of many factors, both natural and anthropogenic, such as the loss of their nesting areas due to urbanization of coastal areas (Sella and Fuentes 2019), erosion (Caut et al. 2010; Spanier 2010, Rivas et al. 2016), increase in incubation temperature (Fisher et al. 2014), and sea-level rise (Fuentes et al. 2010). Vegetation can also affect developing embryos; roots can penetrate incubation chambers and destroy the eggs (Bouchard and Bjorndal 2000) or prevent gas exchange (Ackerman 1997). Also, hatchlings can be entrapped among roots (Staines et al. 2019) or suffer malformations, especially in the presence of plants with thick roots (Cabrera et al. 2019). However, nests with shade from vegetation had longer incubation periods, lower incubation temperature, and an increase in embryo size (García-Grajales et al. 2019; Staines et al. 2019). Kamel (2013) found that vegetation coverage improved hatching success and increased male production in hawksbill turtles (Eretmochelys imbricata). Finally, when hatchlings reach the sand surface, they can be disoriented with vegetation, making it harder to find the sea (Godfrey and Barreto 1995).
Previous studies have evaluated marine turtle reproductive success and nest-site selection concerning beach characteristics such as beach slope, distance from the dune, soil hardness, shrub density, rock percentage, dune height (Ficetola 2007), sand grain size (Mortimer 1990), and the distance of the nest to the high-tide line (Botha 2010). About vegetation, aspects such as its presence or absence (Janzen 1994), vegetation percent cover, and species composition have been studied (Kelly et al. 2017; Hernández et al. 2018; Cabrera et al. 2019; Gerhartz et al. 2019). For instance, Cabrera et al. (2019) found more nesting attempts associated with Suriana maritima but also higher hatchling emergence success. Conrad et al. (2011) evaluated the effect of Ipomoea pes-caprae in leatherback reproductive success. They found nesting site displacement as vegetation spread and lower hatchling emergence success as a result of root invasion of the nest. Also, preferences are highly variable between and within species; therefore, their effect on hatching success and hatchling emergence success needs further evaluation.
In Cuba, the effect of vegetation on marine turtles' reproductive success has been evaluated only in the southwestern region. Calderón et al. (2020) compared two beaches of Guanahacabibes Peninsula, finding differences among nests related to vegetation cover, which is similar to the findings of Gerhartz et al. (2019) in the San Felipe Keys. At 3 beaches at Guanahacabibes Peninsula, Cabrera et al. (2019) studied the importance of shrub species for reproductive success. It is essential to fully understand the potential effect and the importance of the presence of vegetated areas on the reproductive success of C. mydas. To achieve this, the research objectives of this study were to evaluate the effect of the presence, location, and coverage of dune vegetation on nesting success and embryonic development of C. mydas in Guanahacabibes, Cuba.
METHODS
Study Site. — The study location was La Barca Beach, located in the protected area of the Guanahacabibes Peninsula, which is located along the southwestern tip of Cuba (21.85°N, 84.75°W). The authors selected from among 9 beaches to conduct the study based on the beach with the highest annual number of nests (Fig. 1) (Azanza et al. 2019). Data were taken from 2013 to 2019 as part of Cuba's national marine turtle monitoring program (Azanza et al. 2018).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
The beach is 525 m in length and has two patches of vegetation of approximately 10 m in width that are at 10.0 and 20.0 m away from the high-tide line. Between both vegetation patches, there is a sandy strip. The width of the beach oscillates between 10.0 and 60.0 m, and the area contains rocks of different sizes that can even be found under the sand. The rear limit of the beach has a cliff to the west and palm trees to the east (Fig. 2). This beach currently has the largest nesting assemblage of marine turtles on the Guanahacabibes Peninsula (Azanza et al. 2019), most of which are C. mydas (Moncada et al. 2014).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
This beach is made up of a complex of sandy coast vegetation (Ferro et al. 1995), where crawling and herbaceous species predominate (Capote and Berazaín 1984). According to Ferro et al. (2014), among the shrub species, Tournefortia gnaphalodes and S. maritima are the most abundant and most widely distributed species in Guanahacabibes Peninsula; hence, a greater influence on the nesting process of marine turtles. According to Acosta et al. (2010), these species form the first vegetation line of the beach, creating a barrier of succulent leaves, windbreak bushes, and dense foliage. Moreno and Espejel (1986) stated that S. maritima is generally located in the posterior region of the dune, forming a dense and high patch with isolated individuals, while T. gnaphalodes is found in the frontal part of the dune, forming groups (Ferro et al. 2014). According to Ferro et al. (2014), T. gnaphalodes governs the response of disturbed dynamics and causes a negative effect on the number of nests and female emergences on the beach because of their density. However, Cabrera et al. (2019) report more nesting attempts close to S. maritima rather than to T. gnaphalodes, possibly because the root system in the former does not provide sufficient stability to the sand during the digging process.
Characterization of Reproductive Success. — The nests were marked with 1.5-m-long wooden stakes with the nest number recorded in a sketch map for easy geolocation. Nests were visited daily by authorized personnel (2–3 persons) to confirm hatching based on predicted incubation duration. Once the hatchlings emerged, the incubation period, defined as the number of days from the date of egg deposition to the date of the first emergence (Kaska et al. 2006), was calculated. The day after hatchlings were spotted at the surface of the nest, examined, and released, the nest was excavated to count the shells and eggs that did not hatch. Hatchling emergence success was determined by the following formula:
where S is the number of empty shells and L and D are live and dead hatchlings found in the nest, respectively, at excavation time (Santidrián et al. 2012). We used this indicator because it included possible effects of vegetation during embryonic development and those that occur while hatchlings are inside the nest.
Influence of Vegetation on Reproductive Success. — This analysis focused on the relationship between vegetation abundance and nesting success (percentage of nests over total nesting attempts in a defined area). The percentage of vegetation coverage was evaluated on 3 transects perpendicular to the coastline (the first at the beginning, the second in the middle, and the third at the end of the beach). In each, we assessed 2 plots (one per patch) of 100 m2 (Fig. 3) representing 13% of the area covered by vegetation at the beach. The plots were divided into quadrants of 1.0 m2 (100 in total) that were used to determine the vegetation cover (represented by the number of quadrants covered with vegetation). For this, we used the protocol of the sandy coast vegetation monitoring program (Ferro et al. 2013). The measurements were made with a 30-m fiberglass measuring tape with 0.1-m accuracy. These were fixed with stakes to maintain the structure of the grids during the measurement. For each plot, the total aborted nesting attempts and nest number were counted. Nesting was verified during nocturnal monitoring and, in those cases when the nesting process was not observed, the area where potential nesting occurred was excavated until the eggs were spotted. Nesting success was calculated as following: (N/ (A + N)) × 100, where N is the number of nests and A is the number of aborted attempts.
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
Second, we explored the effect of the spatial distribution of vegetation on reproductive success in sections parallel and perpendicular to the sea. In the first case, the beach was divided into 25.0-m sections marked with 2.5-m-high wooden stakes numbered consecutively in an east–west direction from 0. At the beginning of each section, we set a transect 1 m wide from the high-tide line to the end of the second vegetation patch. At intervals of 2.0 m, the evident physical characteristics of the beach were determined and included the presence of sand, rocks, and/or vegetation. Finally, the total number of nests in each section was recorded per year.
Sections perpendicular to the sea were established considering 3.0-m-distance intervals from the high-tide line with a total of 12 intervals (maximum width of nesting area) covering vegetated and nonvegetated areas (Fig. 3). At each interval we determined the number of nests, the nesting success, and hatchling emergence success as well as the incubation period. A finer analysis of the possible consequences of nest-site selection on reproductive success, depending on the position of vegetation at the beach, was made by determining the incubation period and the hatchling emergence success at 2 distinctive vegetation patches: one in the middle section of the beach (F1) and another in the posterior section (F2), as shown in Figure 2.
Data Analysis. — For the representation of the physical characteristics of La Barca Beach, a 22 × 22 quadrant diagram was constructed in which the x axis represented the 21 sections of 25 m in which the beach was divided, while the y axis was the distance intervals from the high-tide line. Each quadrant was assigned a color based on the predominant characteristics: only sand, vegetation, and sand with rocks. To determine the spatial correspondence between the characteristics of the beach and the nesting activity, the number of nests in each of the 25-m sectors was plotted per year of study.
Whisker graphs were used to represent the natural variation of selected reproductive success indicators (relative nest number, number of nesting attempts, hatchling emergence success, and incubation duration). The relationship of the vegetation cover to the number of nests and nesting attempts was determined with a Spearman rank correlation. The Mann-Whitney U-test was performed for emergence success and the incubation period according to the vegetation strips. The Kruskal-Wallis test and its corresponding test of multiple range comparisons were used to verify the relationship between emergence success and the beach intervals. A level of significance of 5% was taken into account for all tests. Tests were carried out in the STATISTICA 7.0 program.
RESULTS
Relationship of Vegetation Cover with Reproductive Success. — The distribution of nesting was related to the presence of vegetation, as the highest nesting success and nest relative frequency were between 6 to 15 m, with a significant difference with the last meters of the beach (H10,75 = 22.75; p = 0.01 and H10,75 = 33.59; p < 0.01), particularly 3 m prior and the first 3 m after the beginning of the first patch. In both patches, median values were higher at the beginning and lower at the end of the patch (Fig. 4).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
The relationship between the presence of vegetation and hatchling emergence success was also significant (H10,71 = 21.07; p = 0.02), although in this case, the highest values (>85%) were associated with the second vegetation patch (between 21 and 36 m), as shown in Fig. 5. The incubation period had no difference across the beach (H10,66 = 16.60; p = 0.08), although higher values were also found farther from the high-tide line.
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
The vegetation cover had a positive and significant relationship with the number of nests (r = 0.56, p = 0.01, n = 17), as shown in Fig. 6. However, there was no relationship between the vegetation cover and the number of nesting attempts.
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
Relation of Geomorphological Characteristics of the Beach with Reproductive Success. — Spatial distribution of vegetation in every section of La Barca Beach is shown in Fig. 7. There was a concentration of sandy areas toward the center of the beach. The extension of the stretch of sand reached up to 10 m from the high-tide line, where the first vegetation patch began, while the second started at approximately 21 m (Fig. 7). Despite this, it cannot be said that the distribution of those 2 patches was maintained throughout the beach.
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
Across the beach, the distribution of the nesting also coincided with that of the vegetation because the highest frequency of nests was concentrated between beach sections 6 and 18, which were those with a wider vegetation distribution. This area was characterized by having clear sand in the vicinity of its entrance.
The 2 vegetation patches that were distinguished in La Barca Beach had different coverage values, with 29% as average for the first and 37% for the second. Significant differences (p < 0.05) were also detected in hatchling emergence success (median values were F1: 88% and F2: 93%; U40 = 891; p = 0.02) and the incubation period (F1: 51 d and F2: 54 d; U38 = 565; p = 0.007) between the 2 patches (Fig. 8). The range of values in the first patch of vegetation was wider because it included lower minimum values (40%–96% hatchling emergence success, n = 54; 45–60-d incubation period, n = 44), while the second had higher values and a narrower range (78%–100% hatchling emergence success, n = 40; 45–67-d incubation period, n = 39). In comparison, values in open areas without vegetation (closer to the high-tide line) were lower, with medians of 74.28% for hatchling emergence success and 51 d of incubation (50%–93%, n = 33 and 47 to 56 d, n = 33, respectively).
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World's Turtle and Tortoise Journal 20, 2; 10.2744/CCB-1460.1
DISCUSSION
Relationship of Vegetation with Reproductive Success. — Sandy coast vegetation plays a decisive role in the reproductive success of marine turtles, despite the discrepancies found in the literature on their positive or negative effect on nesting. In the case of Guanahacabibes, the positive impact of the predominant vegetation on the nesting behavior and the reproductive success of C. mydas are evident.
The preference of females nesting in the area of vegetation or proximity to vegetation may have several explanations. A possible cause, according to Ferrer et al. (2007), is the risk of collapse suffered by the incubation chamber in open beach areas, mainly if the sand is very dry. It can also be a strategy to avoid prolonged flooding in areas near the tide line (Whitmore and Dutton 1985). Besides, the roots of the plants provide a suitable substrate for the construction of the nests because they reduce the compaction of the sand (Horrocks and Scott 1991). Another probable cause of the lower number of nests in the open areas of Guanahacabibes is that turtles have lower nesting success due to the presence of a greater number of buried rocks, which constitute an obstacle to nesting. Other studies have verified the preference for nesting in the interphase zone between vegetation while achieving the greatest nesting success in the vegetation line (Chen and Cheng 1999). In our case, the highest nesting success was achieved within a 6-m fringe before and after the first vegetation line, which might indicate that it is used as a cue to select the nesting place.
The lower emergence success of the offspring in the area near the high-tide line is due to all the risk factors that affect the nests in this area. Kamel and Mrosovsky (2004, 2005) suggest that the proximity to the high-tide line decreases incubation success and emergence success. If the eggs are placed next to the water, they have a high probability of being destroyed by the erosion of the beach (Formia 2002), by the effect of the waves (Botha 2010; Ditmer and Stapleton 2012), or flooded by the water table, which especially impacts deeper nests (Rivas et al. 2018). These last authors state that prolonged precipitation events might increase the risk of nest flooding, affecting the reproductive output of an even higher number of sea turtles. Although they are not destroyed, flooding is a risk because it causes a sudden drop in temperatures, with the consequent effect on various processes such as metabolism (Phillott and Parmenter 2001), sex determination (Wood and Bjorndal 2000), and a reduction in oxygen availability (Ferreira-Júnior 2009; Brenes 2011; Limpus et al. 2020).
In the La Barca Beach diagrams, the presence of cleared sand areas in the beachfront is evident; this characteristic can favor easier entrance of the turtles and their displacement toward the zone with vegetation. This factor is undoubtedly favorable not only to access the beach but also to select a suitable site for nesting (Ficetola 2007) as well as for the presence of vegetation (Coudert 2009; Ditmer and Stapleton 2012; Mathenge et al. 2012). According to Mrosovsky (1983), the presence of obstacles on the beach can make access to it difficult for some species, causing low nesting effectiveness. In this beach, sections in which the rocks predominate at the entrance are concentrated at the ends of the beach. Also, in the final sector that comprises markers 19 to 21, the vegetation line is closer to the high-tide line than in the rest of the beach, thereby encouraging low levels of nesting.
Due to its robustness and thicker roots, the concentration of T. gnaphalodes in the first patch of vegetation could constitute a potential obstacle for the turtles that try to access the interior of the beach. On the other hand, the scarce distribution of I. pes-caprae does not yet represent a danger for the emergence of hatchlings, but it must be further analyzed because they can be trapped in their vines or roots when they leave the nests (Rivas and Marco 2016). In the second patch, S. maritima is the predominant species. Cabrera et al. (2019) established that hatchling emergence success was higher in nests close to this shrub species, probably because their roots are thinner and with slower growth than T. gnaphalodes.
The presence of plant species that can potentially affect the emergence of the offspring, in addition to the lower vegetation cover, seem to suggest lower emergence success recorded in the first vegetation patch. Similar findings were reported by Kamel (2013) for hawksbill turtles. In the same way, this lower coverage can cause higher temperatures in the nest chamber (Kamel 2013) and, as a consequence, the incubation periods are lower in the first strip than in the second, as was observed in the present study.
The increase in cover could represent a limitation for the nesting process because the presence of dense vegetation could hinder the process of digging the nest (Hays and Speakman 1993). Root density can also impact the nesting process and hatching success (Conrad et al. 2011) and has been observed in Guanahacabibes nests, with differences among the shrub species (Cabrera et al. 2019) with higher nesting success close to T. gnaphalodes but higher hatchling emergence success near S. maritima. However, in this area, there is a positive relationship between the number of nests and the vegetation cover, which may be because in most of the sections, coverage did not exceed 45%, allowing C. mydas to nest close to vegetation. This may also be the reason why there is no relationship between the number of aborted nesting attempts and the vegetation coverage. It seems that the levels of coverage are not sufficient to prevent the process of excavation of the nest; however, there are other factors such as the presence of obstacles like rocks, wood, or litter (Hays and Speakman 1993; Azanza et al. 2018), size of the grain of sand (Azanza 2009; Forneiro 2013), disturbances (Azanza et al. 2018), and compaction of the sand (Horrocks and Scott 1991; Sella and Fuentes 2019), etc., that might determine whether more or fewer attempts are made.
Results of the present study corroborate the effect of sandy coast vegetation on marine turtles' nesting because its presence, location, and the degree of cover have a positive impact on the reproductive success of marine green turtles in Guanahacabibes. Therefore, it is necessary to further study the interaction of marine turtles and vegetation to develop adequate management plans for the conservation of this species.
Location of beaches with systematic monitoring of marine turtle nesting in the Guanahacabibes Peninsula, western Cuba. Open circle indicates the study site.
Location of vegetation patches F1 (first vegetation patch with Tournefortia gnaphalodes as dominant shrub species) and F2 (second vegetation patch with Suriana maritima as dominant shrub species) at La Barca Beach, Guanahacabibes Peninsula.
Location of the 3 transects (continuous lines) and the plots of 100 m2 by transect in La Barca Beach, Guanahacabibes Peninsula, Western Cuba. The position of the 21 beacons used as a reference and the distance from the high tide line (in the center) are also presented.
Spatial variation of nesting success and relative frequency of Chelonia mydas nests between 2013 to 2019 nesting seasons in the Guanahacabibes Peninsula, Cuba. Gray rectangles indicate distance covered with a vegetation patch. Letters (a and b) represent groups with no statistical differences, black points and central lines represent the median, and whiskers represent minimum to maximum range.
Spatial variation of hatchling emergence success and incubation period of Chelonia mydas between 2013 to 2019 nesting seasons in Guanahacabibes Peninsula, Cuba. Gray rectangles indicate distance covered with a vegetation patch. Letters represent groups with no statistical differences, black points and central lines represent the median, and whiskers represent minimum to maximum range.
Effect of vegetation cover on the number of nests and nesting attempts per female of marine turtles in La Barca Beach, Guanahacabibes Peninsula.
(a) Number of nests (2013–2019) and (b) physical characteristics of the beach, by section, for La Barca Beach, Guanahacabibes Peninsula, Cuba. The order of the sections corresponds to the east–west direction. Vegetation is presented in gray rectangles with black contours, sand is white, while other physical characteristics such as small or large rocks are presented in black.
Hatchling emergence success and incubation period of Chelonia mydas nests according to the patch of vegetation in which they are located in La Barca Beach, Guanahacabibes Peninsula, Cuba during the 2013–2019 period. F1 (first vegetation patch) and F2 (second vegetation patch).
Contributor Notes
Handling Editor: Jeffrey A. Seminoff
