Spatial Distribution of a Community of Fossorial Snakes of the Genus Geophis (Serpentes: Dipsadidae) in the Central Cordillera of Costa Rica

Study Sites

We conducted the study from April to June 2022 in the town of Las Nubes de Coronado of the Cascajal district in the province of San José, Costa Rica (Fig. 1). The area corresponds to the foothills of the Central Cordillera, a rural landscape with interspersed forest fragments of lower montane rainforest (Holdridge and Tosi, 1967) in a matrix of pastures for dairy farming. Because our sampling requires specific alteration of the environment, we selected five pasture sites to search for fossorial snakes. The sampling sites are located approximately 1,600–1,900 m above sea level. The altitudinal gradient was divided into two sections, 1,600–1,800 m and 1,800–1,900 m, to compare the abundance of snakes in each section. Climatic conditions vary between sites, with a range of average ambient temperatures from 19 °C to 29 °C and monthly rainfall between 20 mm (February) and 479 mm (October), which denotes a high variation in rainfall seasonality (Instituto Meteorológico Nacional, 2023). These sampling sites encompass a total area of approximately 30 ha.

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Sampling of Fossorial Snakes

During the study period, we carried out 11 samplings at the study sites (Table 1). The sampling consisted of searches that lasted six hours, between 0700 h and 1300 h. We conducted searches in the pasture areas and made 1-m² manual excavations using shovels. Additionally, we searched for animals under or inside rotting logs and tree stumps that we turned over, moved, split, or excavated. We conducted sampling in three different types of habitats: (1) slopes of hills available on roadsides between pastures; (2) interiors of pastures, or open areas covered with grass, with less incline; and (3) forest fragments, or areas with remaining natural cover. In forest fragments, we searched under leaf litter and moss using shovels as an additional sampling method. Two researchers invested 55 h/person in the search for fossorial snakes along the altitudinal gradient of the study sites, distributed proportionally to the surface covered by each microhabitat: 12 h on slopes of roads between pastures, 12 h in forest fragments, and 31 h inside pastures.

Table 1.General characterization of five sampling sites for fossorial snakes in Las Nubes de Coronado, Costa Rica.

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We captured, identified, and transported snakes individually, using plastic bags with soil that we placed in plastic coolers to prevent dehydration and overheating. Specimens found together at the same site (under the same log or in the same 1-m² excavation) were placed together in bags and classified as grouped individuals. Snakes were transferred to a small field laboratory where they were sexed and subsequently released at their sites of capture.

Characterization of Capture Sites

For each location where snakes were found, we recorded elevation and geographical coordinates and photographed the specific sites and surroundings. We measured environmental temperature and humidity at time of capture as well as humidity of the substrate where the animal was located, be it earth, a log, or other substrate, using external and internal sensors of a thermohydrometer (Indoor/Outdoor, EXTECH®).

Using the photographs, we described sites where snakes were found. We recorded the substrate type (e.g., soil, logs, leaf litter, moss), level of incline (sloped or flat), macrohabitat (pasture, forest, or slope), and level of natural vegetation cover (no cover, little cover [one to two trees/m²], medium cover [more than two trees/m², but not in a forest], and high cover [in forest area]).

We used a tape measure to measure the depth at which each snake was found. In addition, we indirectly calculated degree of compaction of the substrate by taking measurements of its resistance level (Benevenute et al., 2020). We used a small sports crossbow as a penetrometer (Man Kung brand, model MK-50A1) with 16 cm darts and a constant firing force of 22.7 kg. We shot each dart 50 cm away from the soil or substrate where snakes were found and then measured the depth to which the dart was buried. In cases where darts penetrated the soil at depths greater than 16 cm, we used wooden sticks as extenders to measure the remaining distance between the end of the dart and the entry point. We added both measurements to determine the depth to which the dart was buried in the substrate and to compare different degrees of compaction. Resistance level is proportional to degree of soil compaction (Hamza and Anderson, 2005) and inversely proportional to depth of the dart; therefore, the higher the measured value, the less compact the substrate.

We quantified soil water content gravimetrically and potential prey availability at each capture site. At each site, we collected approximately 40 g of soil and transported it to the laboratory in a labeled plastic bag. We weighed samples (fresh weight) with a digital scale (Entris^® II Sartorius) (± 0.01 g) and subsequently dried them for 10 days in a chamber with an incandescent light bulb. Once dry, we obtained the dry weight and estimated the grams of water in the substrate as the difference. To quantify the relationship between number of earthworms and number of snakes present, we counted the number of worms and snakes at each location.

We also sampled all variables of interest at random locations. We randomly selected 100 sites close to those occupied by snakes to determine whether snakes occupied sites at random.

Data Analysis

We developed a map of the study area using QGIS version 3.36.6 (QGIS Development Team, 2024). We performed statistical analyses in R version 4.4.1 (R Core Team, 2023) and used the ggplot2 package version 3.5.1 (Wickham, 2016) to create figures. We described demographic data using means and standard errors and performed chi-square and t-tests using R (R Core Team, 2023). We performed a principal component analysis (PCA) using the FactoMineR package version 2.11 (Lê et al., 2008) to observe the structure of the distribution of animals in the study based on environmental and soil factors and characteristics. We conducted a PCA analysis to observe the structure of how the species were distributed depending on environmental variables. The variables that we included in the PCA analysis were altitude (m), depth (cm), compaction (cm), substrate temperature (°C), substrate humidity (%), water saturation (g), and number of earthworms. Finally, a logistic regression model was performed to determine whether the recorded environmental variables could predict presence of snakes. The response variable of this model was sites with snakes and sites without snakes (random).

Relative Abundance

We found 115 snakes of four species: G. brachycephalus (41 individuals), G. godmani (39 individuals), G. hoffmanni (25 individuals) and Rhadinella serperaster (10 individuals). The number of snakes found differed among the five sampling sites (χ² = 58.78, df = 4, P < 0.001). Fifty-six snakes were found between 1,700 and 1,800 m above sea level, and 59 snakes were found between 1,800 and 1,900 m above sea level; the number of snakes did not differ significantly between elevations (χ² = 0.08, df = 1, P = 0.78). We did not observe differences in the number of snakes captured throughout the study period (χ² = 1.16, df = 2, P = 0.56), whereas we found monthly variation in proportion of each species in the sample (χ² = 52.7, df = 6, P < 0.001) (Fig. 2). Additionally, we found that the proportion of each sex was similar throughout all months (Fig. 3).

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We observed most snakes in the pastures, both on slopes and in flatter parts of pasture interiors. Pastures, with less natural vegetation cover than forested patches, showed a significantly greater number of snakes in areas with moderate cover than in areas with denser cover (χ² = 19.1, df = 6, P < 0.05). The presence of rotting logs in interior areas of pastures was a significant factor in snake distribution, attracting more snakes, whereas slightly fewer animals were observed on slopes available on roadsides between pastures.

The proportion of individuals of each species differed significantly in each habitat type (χ² = 181, df = 6, P < 0.001) (Fig. 4). We found G. brachycephalus and G. hoffmanni most frequently in rotting logs in pastures and in sites with little or medium forest cover. Geophis godmani were found mainly on hills and slopes of roads with vegetation, both in pastures and in forest fragments. In contrast, R. serperaster were found on four occasions in the company of Geophis on hills with vegetation, on roads and pastures, mainly near forest edges and with medium forest cover.

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Selection of Microenvironments

Comparisons of sites occupied by snakes with random locations indicated that snakes selected microenvironments with specific characteristics. Sites occupied by snakes exhibited substrates with a lower degree of average compaction (t₁₇₁ = 7.97, P < 0.001), lower average temperature (19.3 °C vs. 19.9 °C, t₁₈₅ = 9.20, P < 0.001), and higher humidity (92.2% vs. 89.3%, t₁₄₈ = 3.32, P = 0.001) than nearby random sites (Table 2). Substrates that housed snakes had a lower percentage of water saturation than that recorded in random sites (Table 2) (t₂₀₀ = −3.70, P < 0.001). Similarly, we observed more earthworms in occupied sites than in random ones (Table 2, F_1,213 = 30.25, P < 0.001).

Table 2. Characteristics (X ± SE) of microenvironments occupied by fossorial snakes of the genera Geophis and Rhadinella (encounter sites) and random sites.

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Results of logistic regression (-2LL = 161.09, R2 = 0.62) were consistent with those of univariate analyses. Lower levels of compaction (β = −0.14, P < 0.001), water saturation (β = −0.05, P = 0.001), and temperature (β = −0.56, P = 0.005) of the substrate favored the probability of snake occupancy (0.5 < OR < 0.9 for the three variables). At the same time, higher levels of external temperature (b = 0.63, P < 0.001), humidity (b = 0.08, P = 0.04), and the number of earthworms (b = 0.27, P = 0.003) favored probability of snake occupancy (1.31 < OR < 1.86).

Our PCA analysis allowed us to visualize separation of snake-occupied sites from nearby random sites (Fig. 5A). Despite our previous results, PCA1, which explained 73.76% of the variance, is mainly linked to altitude (loading = 0.98). PCA2 explained 10.6% of the variance and was mainly associated with lower soil compaction (loading = 0.68), substrate water saturation (loading = 0.70), and humidity (loading = 0.12).

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Niche Partitioning at the Microenvironmental Level

Microenvironmental characteristics of sites occupied by different species were not uniform. For instance, average depth (F_3,107 = 5.91, P < 0.001) and humidity at collection sites (F_1,107 = 4.56, P < 0.05) showed significant variation among species (Table 2). Observed differences resulted from the fact that we found G. godmani at greater depth and in wetter sites than members of the other two species in the genus (Table 2). The four species were all found in relatively poorly compacted substrates, but there were differences in the degree of compaction by species (F_3,107 = 3.66, P < 0.05, Table 2). Specifically, R. serper-aster occupied substrates with less compaction than those of Geophis species, highlighting differences in habitat conditions among species or, possibly, habitat selection as a function of morphology.

No study species showed differences between the sexes in terms of depth (F_1,107 = 0.39, P = 0.53), soil compaction (F_1,107 = 0.13, P = 0.71), or humidity (F_1,107 = 0.39, P = 0.53) at occupied sites. Similarly, in the univariate analysis, the mean temperature of sites occupied by snakes did not differ between species or sexes (F_1,107 < 1.61, P > 0.19 in both cases).

Although we observed variation between microenvironmental characteristics of sites occupied by some species, these variations occurred within the same microenvironmental niche. When performing a PCA, we could not see a clear niche partition structure at the microenvironment level in this snake community. On the contrary, significant overlap was evident in microenvironments selected by different species (Fig. 5B). Our PCA1 explained 80.1% of the variance and was mainly related to altitude (loading = 0.98). In comparison, PCA2 explained 7.6% of the variance and was related to less compaction (loading = 0.97).

Snake Groupings

We found both solitary snakes (49% of snakes) and snakes in small groups (more than one snake in the same m²) (51%). Snake groupings were both conspecific (29.4%) or heterospecific (70.6%). Most snake groupings were of two or three individuals, although six snakes were found in the same log on one occasion.

Of heterospecific groupings, four included G. godmani and G. brachycephalus, and three included G. hoffmanni and G. brachycephalus. We also encountered a group that included three Geophis species and a group made up of several members of R. serperaster, G. godmani, and G. brachycephalus. In addition, a pair of R. serperaster was also found with each Geophis species on one occasion each. It is not likely that snake groupings were related to reproductive activities because, in many cases, the individuals of a group were of the same sex or were heterospecific.

Association with Other Organisms

Our observations revealed a wide variety of organisms coexisting with snakes. Notably, earthworms, a key food source for Geophis snakes (Solórzano, 2022), were present at 72% of sites. We found a higher concentration of earthworms at occupied sites than at random sites (Table 2, t₁₅₈ = −0.73, P < 0.001; χ² = 63.19, df = 3, P < 0.001). Therefore, presence of worms is a significant microenvironmental predictor of snake presence. Despite the association between earthworms and snakes, we found no correlation between the number of earthworms and the size of interspecific assemblages (n = 11, S = 128.5, P = 0.20). Additionally, 21% of encounters with Geophis occurred at sites with active nests of the ant subfamily Myrmicinae, on hills, and in rotten logs.

Relative Abundance

Abundance of fossorial snakes per unit effort was relatively high, contrasting with estimates of encounters in other snake assemblages. For example, Ramírez-Arce et al. (2019) reported rates of 0.37 individuals/hour for a community of understory snakes in Braulio Carrillo National Park in Costa Rica. We report a rate of 2.09 individuals/hour, even higher than values recorded in other tropical snake assemblages in other parts of the world, except some marine elapids (Solórzano, 2011; Lillywhite et al., 2015). Willson and Dorcas (2004) noted that small fossorial snakes can occur in extraordinarily high densities, which may represent a significant proportion of vertebrate biomass in temperate ecosystems (Fitch, 1975; Godley, 1980). Our observations suggest that, similarly, density of fossorial snakes can also be very high in tropical regions, especially considering sites of sympatry where several species of Geophis converge. Therefore, contributions that members of Geophis make to local food webs deserve to be studied in detail.

Microenvironment Selection

The ability to select habitats is commonly addressed in ecological studies of snakes and other reptiles (Miller et al., 2012). Microenvironment selection reflects individual response to spatial variation in distribution of favorable environmental conditions, resources, or other organisms as predators, competitors, or prey (Kiesecker and Skelly, 2000; Walther and Gosler, 2001).

At reduced spatial scales, such as that of our study, selection of sites with particular microenvironmental characteristics can occur when the majority of individuals use a relatively small subset of potentially available habitats and their abundance or residence time declines abruptly in other available habitats (Russell and Hanlin, 1999; Shenbrot and Krasnov, 2000; Orr, 2006). Our observations indicated that snakes preferred soft and humid substrates with lower compaction while avoiding sites with dense vegetation and soil with greater water saturation.

Softness and humidity substrates have been pointed out as determining factors in distributions of fossorial squamates (Hecnar and Hecnar, 2011), and preference for less compaction has been verified experimentally (Clark, 1967; Gregory, 1980). For example, in Australia, fossorial skinks Lerista labialis inhabit dune crests with lower substrate compaction. However, dune crests with relatively low substrate compaction are limited to only 2% of available surface area (Greenville and Dickman, 2009). To a more significant extent, this affinity for sites with less compaction is expected because they facilitate mobility of fossorial organisms for quick escapes from predators (Willson and Dorcas, 2004). Lavelle (1988) and Nawaz et al. (2013) report that the level of soil compaction also affects aeration: highly compacted soils can restrict aeration, which in turn depends on soil structure, density, and respiration rate. High compaction can affect bioactivity by reducing microbial activity (aerobic or anaerobic) and the ability of earthworms and other fauna to turn the soil (Whalley et al., 1995).

Soil aeration can be limited by water potential and saturation, which could be a problem for snakes and other fossorial organisms that require a continuous flow of air (Drew, 1990; Stepniewski, Gliński, and Ball, 1994). Although effects of soil aeration are not entirely clear, differences in saturation between sites occupied by snakes and random sites indicate that soil aeration should be considered as a possible factor in site selection by snakes.

On the other hand, minor variations in temperature did not affect the sites selected even though temperature is often important in determining distributions of ectotherms (Lueth, 1941; Seigel et al., 1987). For species of fossorial reptiles, thermoregulation could be less important than it is for non-fossorial species (Bury and Balgooyen, 1976; Lara-Reséndiz et al., 2021). It has been suggested that fossorial snakes possess negative thermotaxis and prefer colder areas (Gregory, 1980). In temperate climates, fossorial snakes achieve stable activity patterns that are like those of non-fossorial snakes (Clark, 1967; Giacometti et al., 2021).

Site humidity is relevant for microenvironment selection, perhaps because water loss rates are relatively high in most fossorial species (Elick and Sealander, 1972). A higher rate of water loss may explain why fossorial reptiles tend to seek substrates with high humidity (Shoemaker and Nagy, 1977). Apart from water loss, skin changes due to abrasion are widespread in fossorial snakes (Jackson and Reno, 1975), as has been observed in Geophis in captivity (López-Goñi, personal observation). To perform adequate ecdysis, snakes require high humidity levels (Hoppmann and Barron, 2007).

Some authors have pointed out that vegetation is a factor that could limit mobility of fossorial lizards, supporting the ideas that fossorial reptiles generally exhibit weak or inconsistent associations with thick vegetation and that they are usually found in areas dominated by grasses (Henle, 1989; James and Losos, 1991; Jellinek et al., 2004). However, it is difficult to separate potential effects of vegetation on the distribution of fossorial snakes from other related factors such as substrate compaction and humidity. One reason could be that open areas tend to be favored by researchers who sample fossorial snakes, which could create a bias for areas with less vegetation.

Snake Groupings

Snake groupings, especially those composed of multiple species, could reflect limitations in the availability of favorable microenvironmental characteristics, such as soil compaction or humidity; an example is the case of rotten logs. Logs offer a substrate that favors snakes. However, they are a limited resource in the study area, perhaps explaining the presence of several individuals, even of different species, in log substrates (Sridhar and Guttal, 2018). Another possible reason for snake aggregations could be protection from predators. Aggregations of prey can cause saturation for predators and reduce the probability of being attacked by other snakes, such as those of the genus Micrurus (Morse, 1977; Lea et al., 2008).

Niche Overlap

Our findings indicated a lack of partitioning of microenvironmental characteristics that would denote clear spatial niche separation in these fossorial snakes. Instead, we observed a significant overlap in environmental niches. Notably, the presence of heterospecific groups at many sites provided strong evidence for high spatial overlap and shared microenvironmental conditions. Our results are surprising given consistent reports of niche partitioning in many studies on other ectotherms in tropical environments (Toft, 1981; Brown and Parker, 1982; Duellman and Hillis, 1987; Donnelly and Guyer, 1994), including some fossorial snake species. For example, in Australia, some species of fossorial elapids show trends regarding differential habitat use among species of the same genus. Simoselaps bertholdi and Brachyurophis semifasciatus are habitat generalists, whereas other species like S.anomalus, B. fasciolatus, and Neelaps bimaculatus were seldom captured in flat areas between sand ridges. Instead, they were found on the crest or sloping areas of sand (Goodyear and Pianka, 2008).

In snakes, resource partitioning between species commonly occurs in the context of diet (Reinert, 1984; Shine, 1987; Luiselli, 2006; Willson et al., 2010; Cardillo and Warren, 2016). However, at least three Geophis species studied here show complete dietary overlap (Solórzano, 2022). Like other species of Geophis, the snakes in our study are specialists on earthworms, with other soft-bodied prey like slugs and leeches only suspected (Solórzano, 2022). Sites occupied by the Geophis species showed a higher presence of earthworms than random sites, which suggests that earthworm availability as prey affects their distribution. However, annelid prey were also present in a significant proportion of random sites, suggesting a high abundance of this resource. Consequently, there is significant overlap in trophic dimension among snake species, and it appears that prey availability is not a limiting resource at the study sites. Availability of abundant prey is also not a strong determinant of microhabitat occupancy of another specialized fossorial reptile, the lizard Lerista labialis, whose distribution in dune ridges is not entirely determined by presence of the termites that constitute their diet (Greenville and Dickman, 2009). Our findings challenge the existing understanding of snake resource allocation, at least in fossorial species that feed on abundant prey.

Association with Other Organisms

All Geophis specimens found inside ant nests were collected in pasturelands and involved individuals of all three snake species. The ants did not appear to harm the snakes. Although these findings have not been reported in other studies on Geophis species, similar observations have been recorded in other fossorial snakes, such as those of the family Lepthotyphlopidae (Watkins et al., 1969). However, it is unknown whether snakes of the genus Geophis produce any chemical repellent as observed in some blind snakes that live in nests and can repel even army ants (Watkins et al., 1969). In the future, it would be interesting to perform chemical analyses with substances from the cloacal sac of Geophis and preform experiments to determine the amount of protection that the snakes’ scutellation provides against the ants.

Our study provides new information on the ecology and natural history and habits of one of the least studied snake genera. Our work reveals the importance of a loosely compacted, slightly humid but not water-saturated microhabitat for Geophis snakes. The heterospecific groupings in this genus are evident, and the species do not show a clear niche partitioning. The information reported here raises new questions to be answered and generates ideas for future work that will allow us to learn even more about these animals. One of the works to be carried out is a population study to estimate how abundant these snakes are and what their role is in the ecosystem.