Are Tropical Reptiles Really Declining? A Six-year Survey of Snakes in Drake Bay, Costa Rica, and the Role of Temperature, Rain and Light

Abstract

Introduction: studies in the last two decades have found declining snake populations in both temperate and tropical sites, including informal reports from Drake Bay, Costa Rica. Objective: to investigate if reports of decreasing snake populations in Drake Bay had a real basis, and if environmental factors, particularly temperature, rain and light, have played a role in that decrease. Methods: we worked at Drake Bay from 2012 through 2017 and made over 4000 h of transect counts. Using head flashlights we surveyed a transect covered by lowland tropical rainforest at an altitude of 12–38 m above sea level, near the Agujas River, mostly at 1930–2200 hours. We counted all the snakes that we could see along the transect. Results: snake counts increase from August to September and then decline rapidly. The May snakes/rainfall peaks coincide, but the second snake peak occurs one month before the rain peak; we counted more snakes in dry nights, with the exception of Imantodes cenchoa which was equally common despite rain conditions. We saw less Leptodeira septentrionalis on bright nights, but all other species were unaffected. Along the six years, the number of species with each diet type remained relatively constant, but the number of individuals declined sharply for those that feed on amphibians and reptiles. We report Rhadinella godmani, a highland species, at 12–38 m of altitude. Conclusion: night field counts of snakes in Drake Bay, Costa Rica, show a strong decline from 2012 through 2017.

Full text

Are tropical reptiles really declining? A six-year survey of snakes in Drake
Bay, Costa Rica, and the role of temperature, rain and light.
Jose Pablo Barquero-González1*, Tracie L. Stice1, Gianfranco Gómez1 & Julián Monge-Nájera2
1. Universidad Nacional, Escuela de Ciencias Biológicas, Laboratorio de Sistemática, Genética y
Evolución (LabSGE), Heredia, Costa Rica; jopbgon@gmail.com, drakebaycostarica@gmail.com,
gianfranco.gomez@gmail.com
2. Universidad Estatal a Distancia (UNED), Vicerrectoría de Investigación, Laboratorio de
Ecología Urbana, 2050 San José, Costa Rica; julianmonge@gmail.com
* Correspondence
Abstract: Introduction: studies in the last two decades have found declining snake populations
in both temperate and tropical sites. Objective: to investigate if reports of decreasing snake
populations in Drake Bay had a real basis, and if environmental factors, particularly temperature
and precipitation, have played a role in that decrease. Methods: we worked at Drake Bay from
2012 through 2017 and made over 4 000 h of transect counts of snakes. Using head flashlights
and a schedule mostly from 1930–2200 hours, several times every month we surveyed one
transect covered by lowland tropical rainforest at an altitude of 12–38 m above sea level, near the
Agujas River. We counted all the snakes along the transect; identified species in situ and also
photographed them. Results: snake counts increase from August to September and then decline
rapidly. The May snakes/rainfall peaks coincide, but the second snake peak occurs one month
before the rain peak; we counted more snakes in dry nights, with the exception of Imantodes
cenchoa which was equally common despite rain conditions. We saw less Leptodeira
septentrionalis on bright nights, but all other species were unaffected. Along the six years, the
number of species with each diet type remained relatively constant, but the number of individuals
declined sharply for those that feed on amphibians and reptiles. We report Rhadinella godmani, a
highland species, at 12–38 m of altitude. Conclusion: night field counts of snakes in Drake Bay,
Costa Rica, show a strong decline from 2012 through 2017.
Key words: snake demography; moonlight; rain; temperature; climate change in Osa.
Total Words: 4025
Snakes are particularly susceptible to population decline because of their long life spans,
late sexual maturity, low reproductive frequency, site fidelity and significant mortality among
neonates and juveniles (Scott & Seigel, 1992; Shetty & Shine, 2002). They are also good
ecological indicators because their populations often reflect fluctuations in the environment and
in the populations of their prey (Moore et al., 2003; Madsen, Ujvari, Shine, & Olsson, 2006).
Population status assessments are difficult because of their cryptic life styles and low or
sporadic activity (Gibbon et al., 2000), but there have been reports of population decline in
temperate regions, including the United States of America (Mount, 1975; Rudolph & Burgdorf,
1997; Conant & Collins, 1998; Hallam, Wheaton, & Fischer, 1998; Tuberville, Bodie, Jensen,
LaClaire, & Gibbons, 2000; Winne, Willson, Todd, Andrews, & Gibbons, 2007) and Europe
(Reading et al., 2010). The situation may be worse in the tropics, where documented studies are
even more scarce (Böhm et al., 2013; Urban, 2015): declines include the extinction of the Round
Island Burrowing Boa, endemic to Mauritius (Bullock, 1986; Greene, 2000), and population

drops of snakes in Nigeria (Reading et al., 2010) and Australia (Lukoschek, Beger, Ceccarelli,
Richards, & Pratchett, 2013; Lukoschek, 2018).
Even though snake declines seem to be a reality in many parts of the world, hundreds of
samples are needed to detect real declines (Kery, 2002; Sewell, Guillera-Arroita, Griffiths, &
Beebee, 2012; Hileman et al., 2018). Furthermore, problematic assumptions used in
mathematical models can lead to suspicious conclusions (e.g. exaggerated extinction rate
estimates: McCallum, 2007).
Reports of snake declines are frequently based on anecdotal evidence and there is a need
for studies that provide intensive counts for prolonged periods (Krysko, 2001; Böhm et al., 2013;
Urban, 2015); for example, local tourist guides in Drake Bay, Costa Rica, have told us that
populations have been declining for nearly two decades. Our objective in this study was to
investigate if their impression is matched by more formal data collection.
MATERIALS AND METHODS
We worked at Drake Bay, South Pacific of Costa Rica (N 08.69420–08.69490; W
083.67421–083.67495), from 2012 through 2017, and made over 4 000 h of transect counts of
snakes. These counts were made while we were accompanied by small groups of tourists as part
of our work as field guides in the area.
We hypothesized that climate changes may reduce local populations of some species and
increase others; and that snakes that feed exclusively on amphibians or insect prey (which
fluctuate strongly with rain or temperature), should be more affected than generalist species.
Snake counts: Using head flashlights we surveyed a transect covered by lowland
tropical rainforest, 12–38 m above sea level, near the Agujas River (Fig. 1 in Digital Appendix
1). Several times every month we counted all the snakes that we could see along one transect;
identified them in situ (guides by Savage, 2002 and Solórzano, 2004), and photographed them
for taxonomic corroboration (Digital Appendix 2). We worked mostly from 1930 to 2200 hours,
but a few counts started at 1730 and ended at 2245 hours (sampling hours per date in Digital
Appendix 2).
Snake diet: Observed species were assigned to different categories considering their type
of diet, in order to see if there were changes in the number of species with certain types of prey
preferences. Categories were not mutually exclusive (Table 1 in Digital Appendix 1).
Precipitation rates and temperature: Precipitation rates and temperature data were
kindly provided by the Instituto Meteorológico Nacional de Costa Rica from the nearest
meteorological station at Rancho Quemado.
Note: Rancho Quemado, where the meteorological station is located, has an altitude of
240 m above sea level while the survey site in Drake Bay has an altitude of 12 to 38 m, so we
expected a difference in temperature between the study site and the meteorological station. To
assess this difference, we made temperature measurements directly in Drake Bay from February
2017 to August 2017 and compared them with Rancho Quemado for that same time period. We
found that average temperatures in Drake Bay are 2 to 3 degrees Celsius higher than
temperatures in Rancho Quemado, but that the trends along the timeline are the same. No
precipitation records were available from January 2012 to July 2012, December 2016 to March

2017 and September 2017 to December 2017. No temperature records were available from
January 2012 to July 2012 and from September 2017 to December 2017.
Moon and in situ rain: Instead of using published moon phase data, we recorded
moonlight conditions on every trip directly in the trail because cloudy skies produce dark nights
even when the moon is full. We used both official rain records and our own classification of rain
condition during the trip (see Results).
Statistical analyses: We analyzed the counts independently for each of the most
common species, and pooled the rare species into an “others” category that we also analyzed
(Table 2 and Table 3 in Digital Appendix 1).
Ethical, conflict of interest and financial statements: the authors declare that they have
fully complied with all pertinent ethical and legal requirements, both during the study and in the
production of the manuscript; that there are no conflicts of interest of any kind; that all financial
sources are fully and clearly stated in the acknowledgements section; and that they fully agree
with the final edited version of the article. We did not need collecting permits because we did not
collect any animals.
RESULTS
Species observed: In total, we recorded 25 snake species, representing five families
(Boidae, Colubridae, Dipsadidae, Elapidae, Viperidae) (Table 1 in Digital Appendix 1).
Effect of diet: Along the six years, the number of species with each diet type remained
relatively constant, fluctuating by a couple of species each year (Fig. 2 in Digital Appendix 1).
However, the numbers of individuals changed visibly along the six-year study period depending
on their main diet items. Species that mostly eat fish and invertebrates were always rare, and thus
insufficient for us to see temporal trends; snakes that mostly feed on birds and mammals, which
had larger populations, declined from 2012 through 2015. Finally, species that feed mostly on
reptiles and amphibians were initially abundant but also have constantly declined over the six-
year period, despite some occasional population peaks (Fig. 3 in Digital Appendix 1).
Annual patterns: When we compared counts of the five most frequent species with
rainfall and temperature during the six-year study period, we noticed several trends (Fig. 4 in
Digital Appendix 1). One is a weak increase in overall temperature along the study period. The
other is that numerically dominant species have highly specific patterns but most started a
decline since 2015. We observed a decrease in L. septentrionalis and I. cenchoa since 2015; E.
sclateri is scarce (except for a peak from August to September of 2012 and 2014) but it has
become even rarer since 2015; S. compresus was not seen after April 2016; finally, M.
melanolomus had no clear tendency to grow or decline from 2012 to 2017, but showed a peak
between August to September (Fig. 4 in Digital Appendix 1).
Monthly pattern: Mean temperature does not change strongly along the year, but
rainfall increases after February and reaches a maximum in October, while snake counts increase

from August to September and then decline rapidly. The May snakes/rainfall peaks coincide, but
the second snake peak occurs one month before the rain peak (Fig. 5 in Digital Appendix 1).
Ecological correlations: The statistical significance values of ANOVA tests appear in
Table 2 and Table 3 (Digital Appendix 1) and the counts/environmental condition relationships
in the appendices,
Effect of rain: We counted more snakes in dry nights, with the exception of I. cenchoa
which was equally common despite rain conditions (Fig. 6 in Digital Appendix 1).
Effect of moonlight: We saw less L. septentrionalis on bright nights, but all other
species were unaffected so they are not presented in the figure (Fig. 7 in Digital Appendix 1).
Final considerations: We did not see differences in leaf litter quantity from the
beginning to the end of the study period (Digital Appendix 2). Our finding of R. godmani is
unexpected because it is a highland species (see Discussion).
DISCUSSION
Food: Snake activity patterns depend on changes in food availability throughout the year
(Henderson, Dixon, & Soini, 1978; Martins, 1994). Snake species that ambush their prey and
rely on sit-and-wait strategies are particularly susceptible because of their low rate of food
acquisition (Webb & Shine, 1998), just like specialist species, which are less likely to exploit
alternative resources in response to shifting environmental conditions (Terborgh & Winter, 1980;
Gaston, 1994). Counts of I. cenchoa, a snake that feeds mainly on reptiles, sharply fell in 2015
and 2017; E. sclateri, a specialist feeder on reptile eggs, declined in 2015 and almost disappeared
in 2016–2017, possibly due to scarce prey. The fall in the numbers of L. septentrionalis matches
the fall in the abundance of prey species like Boana rosenbergi, Smilisca phaeota and
Agalychnis callidryas; nevertheless, other prey items for this species, like Rhinella horribilis and
Craugastor fitizingeri, remained common (Gianfranco Gómez, personal observation).
If we consider that four of the five species affected by rainfall in our study have diets
consisting primarily of amphibians, reptiles, or both, our results are consistent with those of a
study in Mexico, where more rain lead to more amphibian activity and to increased populations
of the snakes that feed on them (Duellman, 1958).
Rhadinella godmani is a small leaf litter snake of uncertain diet and considered a highland
species (Savage, 2002; Solórzano, 2004); we ignore if its presence at near sea level in Drake is in
any way related to changes in environmental factors.
Temperature: Higher temperatures reduce the metabolic rate of snakes and restrain their
activity and visibility (Seigel, Collins, & Novak, 1987; Zamora-Camacho, Moreno-Rueda, &
Pleguezuelos, 2010; Rugiero, Milana, Petrozzi, Capula, & Luiselli, 2013). In Drake Bay, average
monthly temperatures did not vary widely, so we are not surprised that there were no strong,
generalized trends in species abundance that could be related with temperature. This matches
previous work with tropical species (e.g. Shine & Madsen, 1996; Luiselli & Akani, 2002). Only
one species, S. compressus, which needs fresh, shady habitats, was not recorded at all from our
sampling site along 2016 and 2017.

Rain: There are reports of no correlation between counts of Neotropical snakes and
rainfall (Henderson & Hoevers, 1977; Martins, 1994; Bernarde & Abe, 2006) and this is similar
to our finding that the arboreal I. cenchoa was equally common despite rain conditions. Other
species become more active with rain (Daltry, Ross, Thorpe, & Wüster, 1998; Oliveira &
Martins, 2001; Morrison & Bolger, 2002), but we did not see any species more often in rainy
nights in Drake, quite the opposite, Drake snake counts were higher in dry nights. Perhaps they
avoid the cold rainwater (rain is cold in the tropics, too).
Moonlight: Snakes may increase activity in full moon nights, when prey are more visible
(Lillywhite & Brischoux, 2012; Connoly & Orrock, 2018); for example, the tropical tree snake
Boiga irregularis even moves to areas where moonlight is stronger (Campbell, Mackessy, &
Clarke, 2008). However, Crotalus viridis avoids bright moonlight, possibly to escape detection
by its predators (Clarke, Chopko, & Mackessy, 1996). In our study, the fewer sightings of L.
septentrionalis on nights with strong moonlight may also mean that it is avoiding predation, but
we saw all the other species at Drake with the same frequency in dark and illuminated nights.
Final remarks: The clear decline in snake counts at Drake along the years might mean
that their populations have decreased, that they moved out of sight or that they migrated to
higher, cooler areas. They did not seem to avoid the transect because of our presence there
(actually a few species remained constant in our counts along the years) and we do not think they
found a suitable habitat at higher altitude because of human alteration of habitats around the
reserve. We believe that the population decline in Drake is real and needs attention from the
conservation authorities.
ACKNOWLEDGMENTS
We thank Carolina Seas for her assistance with data analysis, Sergio Aguilar for his help
in the elaboration of the images, Alejandro Solórzano, Héctor Zumbado and Mahmood Sasa for
recommendations to improve the manuscript, and Instituto Meteorológico Nacional for climatic
data. This study was financed by the authors.
RESUMEN
¿Están disminuyendo los reptiles tropicales? Seis años de monitoreo en las serpientes de
Bahía Drake, Costa Rica, y el papel de la temperatura, la lluvia y la luz. Introducción: los
estudios realizados en las últimas dos décadas han encontrado una disminución de las
poblaciones de serpientes en los sitios templados y tropicales. Objetivo: investigar si los
informes de disminución de las poblaciones de serpientes en Bahía Drake tuvieron una base real,
y si los factores ambientales, particularmente la temperatura y la precipitación, han jugado un
papel en esa disminución. Métodos: trabajamos en Bahía Drake desde el 2012 hasta el 2017 y
realizamos más de 4 000 h de recuentos de serpientes en transectos. Usando linternas de cabeza y
en un horario mayormente entre las 1930-2200 horas, examinamos un transecto de bosque
tropical de tierras bajas a una altitud de 12–38 m.s.n.m, cerca del río Agujas. Contamos todas las
serpientes a lo largo del transecto; identificamos las especies in situ y también las fotografiamos.
Resultados: los conteos de serpientes aumentan de agosto a setiembre y luego disminuyen
rápidamente. Los picos de las serpientes/precipitaciones de mayo coinciden, pero el segundo
pico de serpientes ocurre un mes antes del pico de lluvia; contamos más serpientes en las noches
secas, con la excepción de Imantodes cenchoa que era igualmente común a pesar de las
condiciones de lluvia. Vimos menos Leptodeira septentrionalis en noches brillantes, pero todas

las demás especies no se vieron afectadas. A lo largo de los seis años, el número de especies con
cada tipo de dieta se mantuvo relativamente constante, pero el número de individuos disminuyó
considerablemente para aquellos que se alimentan de anfibios y reptiles. Reportamos Rhadinella.
godmani, una especie de montaña, a 12–38 m de altitud. Conclusión: los conteos nocturnos de
serpientes en Bahía Drake, Costa Rica, muestran una fuerte disminución en el periodo del 2012
hasta el 2017.
Palabras clave: demografía de serpientes; luz de la luna; lluvia; temperatura; cambio climático
en Osa.
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