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Title
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Behavioral Ecology of the Tabasco Mud Turtle
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Creator
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McAvinchey, Collin
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Identifier
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Thesis_MES_2023_McAvincheyC
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extracted text
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BEHAVIORAL ECOLOGY OF THE TABASCO MUD TURTLE (KINOSTERNON ACUTUM)
IN A SEASONALLY DRY TROPICAL RAINFOREST OF BELIZE
by
Collin McAvinchey
A Thesis
Submitted in partial fulfillment
Of the requirements for the degree
Master of Environmental Studies
The Evergreen State College
June 2023
©2023 by Collin McAvinchey. All rights reserved.
This Thesis for the Master of Environmental Studies Degree
by
Collin McAvinchey
has been approved for
The Evergreen State College
by
_______________________________
John Withey, Ph. D.
Member of Faculty
June 16, 2023
_______________________________
Date
ABSTRACT
Behavioral Ecology of the Tabasco Mud Turtle (Kinosternon acutum) in a Seasonally Dry
Tropical Rainforest of Belize
Collin McAvinchey
We studied movement patterns and microhabitat use of Tabasco mud turtles (Kinosternon
acutum) in a seasonally dry tropical rainforest in the Toledo District of Belize. The Tabasco mud
turtle faces conservation threats from local consumption, habitat loss, and changing climate
patterns across its limited range in eastern Mexico, Guatemala, and Belize. The natural history of
the Tabasco mud turtle remains largely undescribed in the literature and this project is among the
first to make a detailed analysis of K. acutum’s movement and behavior using radiotelemetry.
We made near-daily radiotelemetry relocations and visual observations at the end of the dry
season from July 4th to July 20th, 2022. Mean movement observed for male turtles was 34
meters/day and 26 meters/day for females. Maximum male movement observed from Jul 4-20
during a 24h period was 205 meters, and female maximum movement in 24h was 103 meters.
Measured rainfall in between observations was checked against movement over the same time
period for each individual, yielding a statistically significant relationship between rainfall and
distance traveled for one individual out of six with sufficient relocations. Microhabitat was
recorded for each observation. Individual observations occurred mostly in leaf litter, at the base
of trees, and beneath small woody debris. Notably, this semiaquatic species was rarely observed
in water (diurnal observations only). Our findings expand on the understudied natural history of
the Tabasco mud turtle and yields insights on microhabitat use, home range, and potentially
novel terrestrial habitat utilization.
Table of Contents
Table of Contents ........................................................................................................................... iv
List of Figures ................................................................................................................................. v
List of Tables ................................................................................................................................. vi
Acknowledgements ....................................................................................................................... vii
Introduction ..................................................................................................................................... 1
Literature Review............................................................................................................................ 4
I: Social and Environmental Context .......................................................................................... 4
II: The Mud Turtle Family, Kinosternidae .................................................................................. 6
III: Key Environmental Adaptations ......................................................................................... 12
i: Nesting Forays and Precipitation ....................................................................................... 12
ii: Home Range and Dispersal ............................................................................................... 13
iii: Drought ............................................................................................................................ 15
iv: Heat Mortality and Secondary Life History Effects ......................................................... 16
v: Anthropogenic Habitat Change ......................................................................................... 20
vi: Mud Turtle Response to Climate Change ........................................................................ 21
Methods......................................................................................................................................... 23
Results ........................................................................................................................................... 30
Discussion ..................................................................................................................................... 35
Conclusion .................................................................................................................................... 40
Bibliography ................................................................................................................................. 41
iv
List of Figures
Figure 1: Distribution of the eastern musk turtle, Sternotherus odoratus. Adapted from The
United States Geological Survey - Eastern Musk Turtle (Sternotherus odoratus). ........................ 7
Figure 2: Distribution of known populations of Claudius angustatus in Central America.
Adapted from de Jesus Cervantes-Lopez et al., 2021. .................................................................... 8
Figure 3: Known distribution of Staurotypus triporcatus, the giant Mexican musk turtle. Adapted
from Reynoso et al., 2016. .............................................................................................................. 9
Figure 4: Range distribution of the white-lipped mud turtle, Kinosternon leucostomum. Adapted
from Berry and Iverson (2001). .................................................................................................... 10
Figure 5: Distribution of the eastern mud turtle, Kinosternon subrumum. Adapted from the
United States Geological Survey, (Eastern Mud Turtle (Kinosternon subrubrum) - Species
Profile, n.d.). ................................................................................................................................. 11
Figure 6: Distribution of the Tabasco mud turtle, Kinosternon acutum in Mexico, Guatemala, and
Belize. Adapted from Iverson & Vogt (2011). ............................................................................. 11
Figure 7: Adult Kinosternon acutum. ........................................................................................... 12
Figure 8: Critical thermal maxima in several turtle species. Adapted from Hutchinson et al.,
1966............................................................................................................................................... 18
Figure 9: Map showing extent of Belize Foundation for Research and Environmental Education
in southern Belize.. ........................................................................Error! Bookmark not defined.
Figure 10: Adult K. acutum in a shallow ephemeral pool after release with transmitter attached.
....................................................................................................................................................... 25
Figure 11: Mud obscuring white color of adhesive epoxy on adult K. acutum. ........................... 26
Figure 12: Cohune seeds in ephemeral pools bearing a striking resemblance to adult K. acutum.
....................................................................................................................................................... 28
Figure 13: Adult K. acutum in ephemeral pool bearing a striking resemblace to Cohune palm
seeds. ............................................................................................................................................. 29
Figure 14: GPS points of relocated K. acutum in the northeast corner of the BFREE preserve.
........................................................................................................Error! Bookmark not defined.
Figure 15: K. acutum utilizing small woody debris and leaves, presumably for cover from heat
and predators. ................................................................................................................................ 32
Figure 16: Cohune palm frond and leaf litter creating microhabitat for K. acutum, turtle was
buried beneath this debris and is not shown. Photo by Rebecca Cozad. ...................................... 32
Figure 17: Relative frequency of microhabitat use across turtles. ................................................ 33
v
List of Tables
Table 1: Mean and maximum movement by sex…………………………………………... 30
Table 2: Correlation coefficients between precipitation and observed movement………… 33
vi
Acknowledgements
Immeasurable thanks go to Eric Munscher, my friend and mentor, who identified the
need for this project and did the heavy lifting for getting equipment funding and facilitating
research trips to BFREE. Tabitha Hootman and Becca Cozad taught me the ropes of
radiotelemetry tracking on site in Belize and were incredibly patient while they watched me
fumble with the radio receivers while trying to avoid rain in the jungle. Barney Hall was my
primary research assistant while I was on site and continued to lead the study during the wet
season period and I couldn’t have done it without him. Thank you, Barney. Thanks to Tom Pop
for his humor and immense jungle knowledge and for continuing to track these turtles during the
wet season. Eternal gratitude goes to Jacob Marlin and Heather Barrett; without whom there
would be no BFREE. Thanks to you both for your generosity in housing us during this survey
and lending us so much aid in so many ways. Joe Pignatelli took the lead of the simultaneous
population survey of the area while I was off tracking (and supposed to be leading the population
work) and I am forever grateful to him for that. Extra special thanks to Cheryl Decker and
Sophie Wilhoit for their support and encouragement at the National Park Service, where I was
supposed to be working for the duration of this study as well. Thanks also to my faculty advisor,
John Withey, for his tireless edits and ability to see the larger picture of the project when I was
tunnel-visioning. And finally, special thanks to all my friends and family who have supported me
throughout this process and let me rant incessantly about turtles to them.
vii
Introduction
Freshwater turtles are among the most vulnerable vertebrates on Earth (Rhodin, et al.,
2011). There around 330 species inhabiting rivers, lakes, streams, and ponds across all the
continents save Antarctica, around 45% of which are considered endangered (Rhodin et al.,
2011). Possibly as a result of their somewhat cryptic life histories, freshwater turtles often don’t
receive the same level of research and conservation attention as some of their more charismatic
relatives like sea turtles or large tortoises. Many species have received the “common” moniker,
like the common snapping turtle (Chelydra serpentina) or the common musk turtle (Sternotherus
odoratus), although the extents of their distributions and potential ecological threats remain
understudied (Munscher et al., 2020).
The mud turtle genus (Kinosternon) and its encompassing family, Kinosternidae, is
composed primarily of semi- to mostly aquatic animals. They spend a great deal of their lives in
water, often in slow-moving streams, lakes, or muddy ponds (Lee, 1996). Mud turtles are
considered “opportunistic omnivores” and can be found trundling along stream, pond, and lake
bottoms foraging for a diverse array of foods ranging from benthic macroinvertebrates, small
fish, amphibians, and the occasional bit of vegetation (Legler & Vogt, 2013; Andresen, 2019). In
general, they tend to inhabit waters that undergo significant seasonal variability and are therefore
often required to make movements over land to reach more suitable habitat in times of water
scarcity (Stone, 2001). Being primarily aquatic animals, mud turtles are particularly sensitive to
changes in hydrologic regimes, with the absence or presence of fresh water dictating much of the
animals’ lives.
1
This thesis examines aspects of the Tabasco mud turtle’s natural history in a seasonally
dry tropical rain forest in Belize. The Tabasco mud turtle (Kinosternon acutum) is a small,
partially aquatic member of the mud turtle family Kinosternidae (Lee, 1996). Originally
described by Gray in 1831, the Tabasco mud turtle is found sporadically across Belize,
Guatemala, and southeastern Mexico where it inhabits tropical, lowland rainforest environments
(Iverson & Vogt, 2011; Legler & Vogt, 2013). Its habitat is characterized by cohune palm
(Attalea cohune), Cecropia spp., Ficus spp., and many other tropical, mostly broadleaved, plants.
Primarily carnivorous, K. acutum seems to dine opportunistically on invertebrates during
nighttime forays and rainfall events (Iverson & Vogt, 2011). Like many other species in its
family, K. acutum appears to be dependent on the presence of fresh water for critical life history
processes like foraging and reproduction (Burke et al., 1994; Geller, 2022; Iverson & Vogt,
2011).
The research for this project was undertaken with the assistance and administration of the
Turtle Survival Alliance (TSA), a global nonprofit committed to zero future turtle extinctions.
The field team leadership was made up of longtime volunteer community researchers with the
North American Freshwater Turtle Research Group (NAFTRG). Since 1999, NAFTRG has
involved local community members in freshwater turtle conservation by including them in every
step of the wildlife research process; from trapping, capturing, and tagging animals to accurately
recording biometric data to analyzing population data and presenting results at professional
conferences. We attached radio transmitters to 10 adult individuals and tracked 6 of them nearly
daily during a field expedition from Jul 4-20, 2022. We observed mean and maximum
movement across individuals and noted microhabitat utilization. Our results provide potentially
2
novel insight into the behavioral ecology of the Tabasco mud turtle at the transition from the dry
season to the wet season at the eastern and southern extent of their range in Belize.
3
Literature Review
This literature review discusses environmental and ecological factors impacting the life
history and behavioral ecology of the Tabasco mud turtle (Kinosternon acutum) relevant to the
radiotelemetry study we conducted in the tropical rainforest of Toledo District, Belize, Central
America during July of 2022. Necessary to an understanding of K. acutum’s dynamics are an
examination first of its habitat, both ecological and socioeconomically. Next follows a brief
description of K. acutum’s phylogeny, closest relatives, and their geographical distributions. We
then examine key environmental factors affecting Kinosternon life history processes precipitation patterns, heat effects and habitat fragmentation. Finally, we discuss potential
climate changes that can be expected to impact be turtles overall, the family Kinosternidae, and
K. acutum itself.
I: Social and Environmental Context
The human geography of the Maya Mountains in south central Belize (Toledo District) is
relevant to freshwater turtle conservation and biology. K. acutum and other species (notably the
critically endangered Dermatemys mawii) are hunted and eaten as delicacies by local people
(Iverson & Vogt, 2011; Rainwater et al., 2012). Iverson & Vogt (2011) note recent efforts by the
Mexican government to quell consumption of Kinosternid turtles by outlawing their sale but that
consumption nonetheless continues.
The Maya Mountain foothills region is currently dominated by both conventional and
hack-and-slash agriculture. The region produces beef, poultry, fruits, and seafood towards the
4
coast. Much of the population is involved in subsistence farming in small, rural villages (B. Hall,
personal communication, July, 2022).
Belize is a diverse melting pot of cultures. Historically and prior to European contact, the
region was a part of the Mayan civilization, with many local people still speaking one of several
Maya languages (Nations, 2006). Ancient Maya infrastructure can still be found in numerous
temples and city sites, as well as more subtle marks left on the landscape itself (J. Marlin,
personal communication, July 2021). The research for this project was conducted in and around
probable ancient Maya roadworks and house mounds.
European colonization introduced additional cultural elements to Belize. Like much of
Central and South America, Belize retains strong aspects of Spanish colonial culture, with many
people speaking Spanish as a second language. Uniquely, however, Belize remained a British
colony until the 1980s, which has resulted in most of the population learning English as a
primary language in the home and in schools (M. Canti, personal communication, July 2022).
Belize borders the Caribbean Sea along the East, and a strong Afro-Caribbean cultural presence
is also felt. Caribbean influences are particularly notable in cuisine and dialects of local peoples.
The Maya Forest
The research for this project was conducted on the grounds of the Belize Foundation for
Research and Environmental Education (BFREE). BFREE borders the Bladen Nature Reserve
and a complex of wildlife sanctuaries and protected areas in the Maya Mountains. The area
receives around 4 liters of rain annually and fluctuates between a dry season from about
November through June and a wet season from around July to November (Bridgewater, 2012).
Temperatures remain fairly constant in the range of 26-32 degrees C, with 20 C being considered
quite cold by locals. Forsyth and Miyata (2011) describe the tropical rainforest temperature
5
experience as being much more consistent than many temperate climes, with significantly much
less temperature variation throughout the year.
The tropical rainforests of the Maya mountains are incredibly biodiverse. There are an
estimated 3400 plant species, 40 amphibian species, 16 species of turtle, over 70 snake species,
and a host of bats, birds, and other mammals (Bridgewater, 2012). Of Belize’s 16 species of
turtle, 8 occur within or directly adjacent to the bounds of BFREE and the Bladen Nature
Reserve. Five of these are Kinosternid turtles, representing a considerable concentration of the
family’s diversity at this study site.
II: The Mud Turtle Family, Kinosternidae
As covered in the Introduction, the family Kinosternidae is composed primarily of semito mostly aquatic animals. Most species possess large heads and accompanying muscles adapted
for crushing the calcareous shells of invertebrates or even smaller turtles (Lee, 1996; Ernst &
Lovich, 2009). The largest Kinosternid species, Staurotypus triporcatus, measures in at around
40 centimeters in carapace length. Most species are quite small, with K. acutum being considered
one of the smallest turtle species in the world at adulthood 80 mm (Iverson & Vogt, 2011; Legler
& Vogt, 2013).
The range of Kinosternid turtles stretches across the eastern parts of North America,
through Central America, and into South America (Ernst and Lovich, 2009; Lee, 1996). The
family’s probable original site of evolution is in Mexico, where the greatest amount of species
diversity can be found (Ernst & Lovich, 2009). Kinosternidae encompasses four distinct genera:
Sternotherus, Claudius, Staurotypus, and Kinosternon (Ernst & Lovich, 2009; Pempelfort, 2018).
A summary of distinctive traits of each genus follows hereafter.
6
Sternotherus
Sternotherus is widely represented across the eastern United States and Canada and are
among the smaller members of Kinosternidae. Commonly known as musk turtles because of the
aromatic excretions released from their posteriors (though this trait is not unique to this genus),
there are four species of Sternotherus, all of whom are endemic to the eastern regions of the
United States (Ernst & Lovich, 2009). The most widely distributed species is the stink pot,
Sternotherus odoratus, which ranges along the eastern coast of the United States as far north as
Maine and south along the Gulf Coast into Texas (Fig. 1).
Figure 1: Distribution of the eastern musk turtle, Sternotherus odoratus. Adapted from The United States Geological Survey Eastern Musk Turtle (Sternotherus odoratus).
One of the two genera of Kinosternid endemic to Central America, Claudius is comprised
of only one species, the Narrow-bridged musk turtle Claudius angustatus, de Jesús CervantesLópez et al., 2021). Claudius angustatus are known for their distinctive cusped jaws that give
them a vampiric appearance, earning them the nickname “vampire turtle”. Claudius has a
7
particularly restricted range; it occurs only in Belize, Guatemala, and southeast Mexico (Fig. 2).
A population of narrow-bridged musk turtles was recently located within a few hundred meters
of the BFREE research center, expanding their range considerably both south and east of its
previous extent (Munscher et al., 2022).
Figure 2: Distribution of known populations of Claudius angustatus in Central America. Adapted from de Jesus Cervantes-Lopez
et al., 2021.
Staurotypus
Staurotypus are giants among mud turtles, with large adults reaching up to 40 centimeters
in length (Lee, 1996). The two extant species, Staurotypus tricporcatus and Staurotypus salvinii
(the giant Mexican musk turtle and the Chiapas giant musk turtle), inhabit a limited range in
8
Central America (Fig. 3). Staurotypus spp. are known both for their size and for their ability to
consume other hard-shelled turtles (J. Brian Hauge, personal communication, July 2021).
Figure 3: Known distribution of Staurotypus triporcatus, the giant Mexican musk turtle. Adapted from Reynoso et al., 2016.
Kinosternon
Genus Kinosternon encompasses fifteen species (Lee, 1996). Commonly known as mud
turtles, this genus contains most species in Kinosternidae and enjoys the widest distribution
across the Americas. Some species occur across Central and South America (Fig. 4), while
others are distributed across the southeastern United States (Fig. 5).
Kinosternon acutum
This literature review outlines the basics of K. acutum’s life history, though limited in
temporal and geographic range. Legler & Vogt (2013) mentions K. acutum diets as being
primarily composed of various available invertebrates. Vogt observed night-time foraging during
the wet season at a site in Veracruz, Mexico; Legler observed the same phenomena at another
site in Belize. Legler & Vogt note that K. acutum uses local vegetation or woody debris as
9
shelter during the day. They reference a study on K. acutum in Veracruz, Mexico conducted by
one of the authors (Vogt), and Legler & Vogt (2013) later refer to this work, but it refers to an
abstract from a conference.
Given the relatively thin measure of the established literature on K. acutum in the wild,
comparisons must be made by examining life history habits of other Kinosternid turtles, turtles in
general, and other reptiles when applicable. The following are a series of case studies detailing
documented turtle and reptilian adaptations to climate phenomena including precipitation,
seasonality, heat, and habitat destruction and fragmentation. These examples may illuminate
possible related responses evolved by K. acutum in lieu of further published research on the
species itself.
Figure 4: Range distribution of the white-lipped mud turtle, Kinosternon leucostomum. Adapted from Berry and Iverson (2001).
10
Figure 5: Distribution of the eastern mud turtle, Kinosternon subrumum. Adapted from the United States Geological Survey,
(Eastern Mud Turtle (Kinosternon subrubrum) - Species Profile, n.d.).
Figure 6: Distribution of the Tabasco mud turtle, Kinosternon acutum in Mexico,
Guatemala, and Belize. Adapted from Iverson & Vogt (2011).
11
Figure 7: Adult Kinosternon acutum. Photo by Collin McAvinchey.
III: Key Environmental Adaptations
i: Nesting Forays and Precipitation
Precipitation and the presence of fresh water plays a major role in the reproductive and
life history habits of Kinosternid turtles. Burke et al. (1994) studied the relationship between
eastern mud turtle (Kinosternon subrumum) nesting behavior and the onset of rainstorms.
Precipitation events appeared to be the primary factor in initiating nesting forays by gravid
females. Over the course of nearly a month, these gravid females left the bay in which they spent
most of their lives and buried themselves in nearby sediment (Burke et al., 1994). The females
then waited until the next rainfall event to construct their nest and deposit their eggs, whereafter
they buried themselves in another location and waited for another storm before returning to their
12
original aquatic habitat. The authors remain unsure as to why these turtles used rainfall as an
indicator to begin the nesting process, but rain events appeared to be the primary trigger; being
unrelated both to overcast cloud conditions and ambient temperature (Burke et al., 1994).
Geller (2022), in a review examining several different studies on the relationship between
freshwater turtle behavior and precipitation, corroborates and expands on Burke’s (1994)
findings. Species besides the eastern mud turtle tie their reproductive efforts to precipitation
events, but documentation of this phenomenon is lacking in many species, painting a
complicated picture of overall turtle reproductive ecology and its relation to rainfall events.
Rainfall does appear to be positively associated with Kinosternon nesting, however. Geller posits
that turtle embarkation on nesting forays is probably a predation deterrent—that olfactory clues
left behind by nesting turtles may be obscured by rainfall and that turtles, whether consciously or
not, are using precipitation events as cover from predators.
The response of mud turtles at the species level to changes in amounts and timing of
rainfall due to climate change remains unknown. However, major disturbances in precipitation
regimes may have significant effects on the life histories of these animals. Changes in timing or
amount of rainfall may disrupt vital life history events.
ii: Home Range and Dispersal
Crucial to an examination of the effects of climate change on mud turtles is a discussion
of the home range size of a given animal and its ability to escape conditions that might be
detrimental to survival, subsistence, or reproduction. Size appears to have a direct relationship on
the ability of Kinosternids to physically move themselves around and disperse great distances. In
turtles, size appears to be correlated with overall dispersal ability of species (Aparicio et al.,
13
2018; Slavenko, 2016). Dispersal can be a dangerous activity for turtles, especially when they
inhabit fluctuating bodies of water in highly modified areas. Habitat connectivity becomes key
when populations are forced to disperse, as mortality from predation and vehicle strikes can
increase when turtles are on the move (Anthonysamy et al., 2013).
Kinosternid turtles display a remarkable ability to disperse themselves on land and in the
water. K. integrum enjoys a particularly wide range in its native Mexico, where it can be found
inhabiting permanent and fluctuating waters from around sea level to over 2000 meters in
elevation (Aparicio et al., 2018). This species was found to be highly mobile, relative to their
size, with ranges up to about 2.75 hectares (Aparicio et al. 2018).
Other Kinosternids demonstrate similar terrestrial dispersal abilities. The yellow mud
turtle (Kinosternon flavescens) has been observed moving up to 8 kilometers in search of suitable
aquatic habitat (Ernst, 2009). The Sonoran mud turtle (Kinosternon sonoriense), the scorpion
mud turtle (Kinosternon scorpioides), and the white-lipped mud turtle (K. leucostomum) have all
been observed moving between 0.5 and 1 kilometer over the course of a year (Cordero, 2010;
Hall & Steidle, 2007; Stone, 2001).
While Kinosternids may be capable of an unusual amount of terrestrial motion compared
to other members of their family, their ability to travel long distances and escape some of the
landscape-scale effects of anthropogenic climate change may be greatly limited when compared
with more mobile taxa. This relative immobility may be offset by how widespread the family is
and by the diversity of the ecosystems they inhabit and the degree to which each species can
respond may be highly variable. Family Kinosternidae itself may not be in mortal peril, but the
same may not be able to be said for individual species.
14
iii: Drought
Drought can play a major role in determining turtle movement. The predominant
drought-mitigation strategies observed in freshwater turtles are dispersal (Anthonysamy et al.,
2013) and estivation (Ultsch, 2006). With limited research on mud turtle response to drought,
studies on related turtle taxa or other reptiles must be used as a rough model for Kinosternid
response. Anthonysamy et al. (2013) examined responses of a population of Blanding’s turtle
(Emys blandingii) to a particularly dry summer and found a significant amount of movement
resulting from decreases in freshwater levels. Subject turtles were observed greatly increasing
overland movement while travelling from drying bodies of water, with many individuals found
retreating to nearby riparian areas for access to water. Turtles in this study tended to prefer
permanent sources of water during drought rather than seasonally fluctuating shallower ponds
and wetlands (Anthonysamy, 2013). Turtles were found to begin estivating, with some
individuals dramatically decreasing their movement for longer than a month at a time during the
height of summer heat and drought.
The second major adaptation employed by Kinosternids is to engage in estivation when
faced with extremely hot or dry conditions. Estivation is like hibernation, only it appears to have
evolved as a response to arid conditions rather than cold ones (Anthonysamy et al., 2013).
Estivating animals sequester themselves in protected areas like crevices in rocks, burrows in
mud, or deposited plant material (Anthonysamy et al., 2013; Stone, 2001). Periods of estivation
allow turtles to dramatically reduce their body’s metabolism and their need for water and food
during times of resource scarcity (Aparicio et al., 2018). Estivation periods can last a
considerable amount of time; from six months to a year depending on the species and availability
of water (Iverson, 1988; Ligon & Stone, 2003). Stone (2001) cites a study by Rose (1980) that
15
claims the yellow mud turtle (Kinosternon flavescens) was observed estivating for a two-year
period in a laboratory setting.
Stone (2001) studied Sonoran mud turtles (Kinosternon sonoriense) in arid southern New
Mexico over a period of drought lasting three years and found no significant reduction in
resident turtle populations in the area. The surveyed area had remained nearly completely dry
throughout that period, yet the turtles’ ability to reproduce and maintain a stable population
appeared largely unaffected (Stone, 2001). Indeed, the Sonoran mud turtle appears to flourish
under such variable conditions. Aparicio’s (2018) study on Mexican mud turtles describes
estivation periods lasting up to nine months in parts of Mexico, with subject turtles observed
utilizing microhabitats like dead trees, old stone walls, and piles of leaf litter as shelter from heat.
Mud turtles’ ability to estivate may prove one of their most significant advantages as the global
climate continues to shift towards more extreme conditions. Compared to those of other aquatic
animals (like fish, or even fully aquatic turtles), this adaptation may provide mud turtles with a
significant amount of climate resilience. It is possible that estivation among mud turtles may
prove an invaluable offset for their relatively limited dispersal ability as the climate changes.
iv: Heat Mortality and Secondary Life History Effects
Mud turtles, and turtles in general, are relatively resistant to extremes of heat (being
reptiles and therefore somewhat dependent on it), but only within certain limits. The ability of an
animal to tolerate extremes in heat is known as “critical thermal maxima”. Hutchinson’s (1966)
study on critical thermal maxima subjected an array of turtle species to ever-increasing amounts
of heat until they lost the ability to right themselves when tipped over (known as the “righting
response”), using this as an approximation of temperatures that would cause mortality. The study
16
looked at three species of Kinosternid turtles (though many other turtle species besides):
Sternotherus minor, Sternotherus odoratus, and Kinosternon bauri palmarum (Fig. 8).
Hutchinson found a loss of righting response between the three species to be around 40 degrees
Celsius. In general, land-based turtles were found to have a higher tolerance for thermal
extremes, fully aquatic turtles the lowest, with semiaquatic species like Kinosternids about
roughly in the middle. Mud turtles will certainly be affected by increases in temperature due to
global climate change, but they may be less susceptible to outright mortality than other, more
fully aquatic turtles.
17
Figure 8: Critical thermal maxima in several turtle species. Adapted from Hutchinson et al.,
(1966).
The literature is thin on sublethal effects of temperature extremes on turtles, especially
among freshwater turtles and even more so for Kinosternids. However, secondary heat effects
have been observed in detail on sea turtle populations. Studies on sea turtle nests, like those
18
conducted on olive ridley turtles by Cavallo et al., (2015), have demonstrated significant effects
of increasing temperature on egg development. Cavallo et al., (2015) estimate that the sand
comprising beaches where sea turtles build nests could see an increase between 2 and 3.4 degrees
Celsius over the next six decades. This change has the potential to cause dramatic shifts across
several different life history traits. For example, they found that hatchlings exposed to higher
temperatures were slower swimmers and generally weaker, but that they had a greater stock of
energy fresh out of the egg (Cavallo et al. 2015). On the other hand, increased water temperature
(to a point) contributes to overall faster swimming speed for sea turtles. These seeming
contradictions illustrate the dynamic and uncertain future of turtles’ adaptive capacity in the face
of climate change and how changes in climate may affect multiple stages of an animal’s life
history.
There are additional effects of increasing temperatures on embryonic development of
turtles. The sex of gestating infants of many turtle species depends on the ambient temperature
the embryos are exposed to while in the egg (Ewert & Nelson, 1991). Two genera in
Kinosternidae are temperature-dependent in this way, both Sternotherus and Kinosternon.
Temperature-dependent sex determination is divided into two main classes: Pattern I, in which a
threshold of increasing temperature is reached past which all hatchlings develop as males and
Pattern II, which presents a more “normal” distribution; after a certain temperature is reached,
embryos develop into males while females develop in both the lower and higher extremes of
temperature (Ewert & Nelson, 1991). Interestingly, Staurotypus was observed to largely be
unaffected by temperature in terms of sex determination and is instead dependent on genetic
factors to determine male: female sex ratios (Ewert & Nelson, 1991).
19
The variability seen across genera in this family further complicate the picture that
comprises mud turtle response to climate change. Detailed analyses of expected temperature
fluctuations over the ranges of Kinosternid species would illustrate potentially significant
changes in sex among and between mud turtle populations.
v: Anthropogenic Habitat Change
In addition to mud turtles having to cope with future perturbations in climate, they have
been and will continue to be faced with habitat changes driven by more direct human impacts.
Bernstein and Christiansen’s 2011 study on the yellow mud turtle (Kinosternon flavescens)
describes mud turtles enduring just this sort of change. Yellow mud turtle populations observed
in this study inhabited a series of wetlands that were formerly connected to a reach of the
Mississippi River in Iowa until installation of a levee system and industrial development
separated them. The landscape was made up of a patchwork of marsh, forests, and sand prairie,
which would have been ideal habitat for mud turtles prior to development (Bernstein &
Christiansen, 2011). Disconnecting this habitat complex from much of the riverine input of water
from the Mississippi River resulted in lowered water levels that prevented turtles from accessing
water to rehydrate themselves following periods of estivation and hibernation. Bernstein and
Christiansen found that yellow mud turtles moved into industrial gravel pits where water levels
remained high enough to provide suitable habitat. However, these refuges were only a temporary
respite; much of the native forests, prairies, and wetlands vital to the survival or yellow mud
turtles in the American Midwest is heavily modified and dispersed. The species is in decline,
likely due to a lack of habitat connectivity that prevents turtles from reaching refugia during
drought or extreme winter temperatures.
20
vi: Mud Turtle Response to Climate Change
Species in genus Kinosternon are expected to struggle as the climate changes over the
coming decades and centuries. In a review covering many mud turtle species, Berriozabal-Islas
(2020) examines Kinosternon ranges and how they might be expected to expand or contract
under different climatic regimes. The majority of Kinosternon species will be losing considerable
amounts of habitat under high emission futures. The authors estimate a 4.5% habitat loss under
RCP 8.5 by 2050 for the Tabasco mud turtle, rising to a 14.42% loss in habitat suitability by
2070. Counterintuitively, even species whose ranges are expected to expand may still be
imperiled. The white-lipped mud turtle, K. leucostomum (believed to be a very close relative and
sharing much habitat with K. acutum), loses 45% of its habitat under an RCP 2.6 scenario by
2050 but gains 11.84% by 2050 under RCP 8.5 (Berriozabal-Islas, 2020; Iverson and Vogt,
2011).
Butler et al. (2016) suggest further possible futures for other Kinosternid species. The
striped mud turtle (K. baurii) and the rough-footed mud turtle (K. hirtipes) are both expected to
see dramatic contractions of their climatic envelope under high emission scenarios. Conversely,
the Sonoran mud turtle’s (K. sonoriense) climate envelope will probably remain somewhat
constant and the envelopes of both the yellow mud turtle (K. flavescens) and the eastern mud
turtle (K. subrumum) may see considerable expansions under high-emission climate scenarios in
the future (Butler et al., 2016; Berriozabal-Islas, 2020).
21
Conclusion of Literature Review
Mud turtles’ resilience in the face of climate change will be influenced by the key
environmental and biological factors examined above – their relatively limited dispersal ability,
their dependence on precipitation and freshwater for reproduction and foraging, and their ability
to cope with extremes in temperature (Vogt and Flores-Villela, 1992; Cavallo et al., 2015;
Berriozabal-Islas et al., 2020). Their ecological success will also depend on the availability of
suitable habitat, much of which may face fragmentation by increasing human development
(Bernstein & Christiansen, 2011).
The goal of this thesis is to provide novel insights into the behavioral ecology of the
Tabasco mud turtle. Research efforts like this that focus on fine-scale zoological phenomena are
vital to preparing and informing conservation efforts that protect lesser-known species like
Kinosternon acutum in this ongoing period of environmental upheaval.
22
Methods
Study Area
The field research portion of this study was undertaken from Jun 30, 2022 - Jul 22, 2022
on the grounds of the wildlife preserve at the Belize Foundation for Research and Environmental
Education (BFREE, Fig. 9). BFREE is a 1,153 acre privately held nature preserve bordering the
Maya Mountains rainforest complex in the Toledo district of Belize. The preserve is dominated
by native tropical broadleaf forest and interspersed with ephemeral wetlands and incursions by
the nearby Bladen River. The majority of K. acutum captures were made along an ATV and foot
track that follows the boundaries of the preserve.
Figure 9: Map showing extent of Belize Foundation for Research and Environmental Education in southern Belize.
23
Capture and Tagging
In total, 10 individual K. acutum were captured opportunistically during surveys along
the northern and eastern boundaries of BFREE from Jul 4-20, 2023. Captures all occurred during
daylight hours in standing pools, usually during or immediately following rainfall. Iverson and
Vogt (2011) claim K. acutum is primarily nocturnal in habit, but extensive nighttime capture
efforts were not undertaken for safety reasons.
All K. acutum captures were achieved by hand. Animals were placed in a breathable
mesh bag and either carried by hand or stowed safely in a backpack. The location of each capture
was noted using a Garmin GPS Map 64s unit. Flagging was affixed to each mesh capture bag
and labeled appropriately to ensure each animal was returned to its original capture point.
Animals were carried back, between 1-3 km, to a processing station on the Boundary
Road where biometric data was recorded, numerical shell marking identification number etched
(a modified version of Cagle, 1939) and a PIT tag was implanted if the animal was large enough
(carapace length greater than 70 mm, as outlined in Munscher et al., 2020). Biometric data
collected included carapace length, carapace width, shell height, plastron width, plastron length,
and mass.
Holohil PD-2 transmitter units weighing 3.8 grams each were attached to each captured
turtle. A combined mass of the transmitter unit and epoxy of no more than 8% of total body mass
was considered ideal. The transmitters were calibrated and tested prior to use and affixation to
animals. The frequency of each unit was confirmed to be functioning and readable by handheld
radio units with Yagi antennae attachments. Care was taken to apply as little epoxy as possible to
securely affix each transmitter without adding unnecessary mass to each animal. This
consideration further limited suitable Tabasco mud turtles, as individuals had to be above about
24
90 grams in mass to be large enough to tolerate transmitter affixation. Epoxy was activated while
mixing by hand and then used to encase transmitter units which were then attached to the reartop-center of the carapace (Fig. 10). Turtles were then placed in containment bins while epoxy
cured. Each animal was placed on its side after transmitter affixation to ensure that their righting
response remained available despite the added weight of the transmitter. Animals were released
at their original capture location after epoxy was deemed to have cured sufficiently. The decision
was made not to mix local mud into the epoxy (i.e., for camouflage) because of the remoteness
of the site and our inability to obtain more epoxy if we incorrectly calculated the amount of mud
to be mixed in and rendered the epoxy useless. Fortunately, the animals were observed to have
managed to camouflage themselves while moving about (Fig. 11).
Figure 10: Adult K. acutum in a shallow ephemeral pool after release with transmitter attached.
Photo by Collin McAvinchey.
25
Figure 11: Mud obscuring white color of adhesive epoxy on adult K. acutum.
Photo by Collin McAvinchey.
Relocation Data
Radiotelemetry observations began the day following each animal’s release. Surveys
were conducted in teams of two researchers—one to operate radiotelemetry equipment and the
other to record notes and act as a spotter and mitigator against potential hazards. The research
team daily (usually starting in the mornings before afternoon rains began) set out on foot from
the BFREE basecamp. We followed the Boundary Road to the most distant turtle capture point,
about 3.2 km away. We started with the turtle farthest away and worked backwards along the
transect of the Boundary Road.
The radio receiver unit was activated upon arrival at the last known location of each turtle
and tuned to the frequency broadcast by each transmitter. Each animal was then located to within
1 meter using radio and antennae. A flashlight was used for visual verification of each animal if
they were present on the surface or visible in substrate, but substrate was not disturbed if animals
were not visible.
26
The GPS unit was held motionless during a triangulation process to gain the most accurate
position. Upon calibration, coordinates were saved to the unit’s memory and written in a
notebook along with date, time, turtle ID number, and notes about microhabitat utilization.
Relocations were collected every day from Jul 4 - 20, 2023 except for (Jul 5 and 18) when
staffing or safety issues (lightning storms and illness) prevented data collection.
Weather Data
Ambient weather data (precipitation, temperature, relative humidity, atmospheric
pressure, and wind speed and direction) was collected by passive two H0B0 units present within
the wildlife reserve; one directly adjacent to the processing station and another within two
kilometers of most capture locations. A reading was collected every five minutes over the
duration of the study period. Two variants of precipitation were calculated to be measured
against turtle straightline movement. Rain coincident, which was a sum of measured rainfall in
between observations from one day to the next; and accumulated rain, which was a measure of
the total amount of precipitation that had fallen since the start of the study period on Jul 4.
Data Analysis Methods
The relationship between movement and precipitation was analyzed in JMP to obtain
correlation values (both Pearson’s and Spearman’s). Precipitation data was examined in two
analyses: 1) distance between consecutive relocations, and cumulative rainfall during the same
time period (for each individual), and 2) distance between relocations correlated with total
accumulated rainfall over the study period.
27
We performed a χ2 test in JMP in order to test the null hypothesis of no difference in
proportion between individual microhabitat utilization occurrences. Microhabitat classes were
designated to capture the full extent of utilized structure variation and are defined as such:
Wood:
animal was observed in and/or under small woody debris like sticks and logs
Water:
animal was observed at least partially submerged in a body of water like a
stream or puddle
Tree:
animal was observed at the base of a tree
Leaves: animal was observed in and/or under fallen leaf litter
Cohune: animal was observed in association with a cohune palm.
Cohune palm seeds look strikingly like K. acutum carapaces when submerged in shallow water
and many were mistakenly captured (Figs. 12 & 13). Their resemblance to adult Tabasco mud
turtles led to the cohune’s inclusion for analysis as a potential microhabitat factor.
Figure 12: Cohune seeds in ephemeral pools bearing a striking resemblance to adult K. acutum.
Photo by Collin McAvinchey.
28
Figure 13: Adult K. acutum in ephemeral pool bearing a striking resemblace to Cohune palm seeds.
Photo by Collin McAvinchey.
29
Results
Mean movement between near-daily observations for male turtles was 34 m and 26 m for
females (Table 1). Maximum straight-line movement observed between individual consecutive
observations was 205 meters for males and 103 meters for females. The maximum straight-line
distance across all relocations of individual turtles (Total max in Table 1) across the entire study
period was 196 meters for females and 275 for males. Distribution of all individual observations
is shown below (Fig 14).
Figure 14: GPS points of relocated K. acutum in the northeast corner of the BFREE preserve.
30
Table 1: Mean and maximum movement by sex. Mean is average of total observed straight-line movements. Max straight-line is
the maximum distance observed between two adjacent movement observations. Total max is maximum distance traveled between
any two observations, whether subsequent or not.
ID #
1
2
3
4
5
6
Sex
F
M
F
M
F
F
Mean (m) SD Max straight-line (m) Total max (m)
14
7
71
105
16 11
67
92
29 29
29
196
52 13
205
275
18
6
103
151
28 22
93
174
Individual turtles were observed in microhabitat types in similar proportions (χ220 = 21.4,
p > 0.37). Microhabitat feature classes were not mutually exclusive, for example it was possible
for an individual to have utilized both woody debris and leaf litter at a single relocation.
Individuals were found to utilize each microhabitat type except for water, with only half of
individuals observed in standing or moving water over the near-daily study period. Leaves were
observed as the dominant microhabitat utilization type, followed by an association with the base
of trees and then by cohune palm and small woody debris (Figs 15, 16, 17).
31
Figure 15: K. acutum utilizing small woody debris and leaves, presumably for cover from heat and
predators.Photo by Collin McAvinchey.
Figure 16: Cohune palm frond and leaf litter creating microhabitat for K. acutum, turtle was buried
beneath this debris and is not shown. Photo by Rebecca Cozad.
32
Figure 17: Relative frequency of microhabitat use across turtles.
Most individuals had no significant correlations between movement distances and either
coincident or accumulated precipitation (Table 2). Movement vs. rain coincident refers to the
amount of movement observed and rain measured in between near-daily observations, while
movement vs. accumulated rain refers to the correlation coefficients of near-daily observed
movement and cumulative rainfall over the study period. H0B0 loggers in and adjacent to the
study site recorded 91 millimeters of rain over the course of the study period from Jul 4 – 20.
One individual (turtle #6, Table 2) had a significant positive correlation of movement with
coincident rain (Pearson’s r = 0.77, Spearman’s rho = 0.80, both p-values < 0.001). The strength
of these coefficients, along with the low p-value, allow us to reject the null hypothesis of no
relationship between rainfall and movement of K. acutum #6.
33
Table 2: Correlation coefficients between precipitation and observed movement (m). Rain coincident refers to accumulated
rainfall in between observations; accumulated rain is the relationship between observed movement and total rainfall over the July
2022 study period.
Turtle #
1
2
3
4
5
6
Movement vs. rain coincident
Movement vs. accumulated rain
Pearson's r P-value Spearman's rho Pearson's r P-value Spearman's rho
0.22
0.73
-0.10
-0.10 0.35
-0.27
0.36
0.33
0.28
-0.29 0.31
-0.29
-0.21
0.55
-0.17
-0.43 0.90
-0.04
0.37
0.20
0.36
-0.12 0.77
-0.08
-0.14
0.77
0.09
0.15 0.50
0.19
0.77 <0.001
0.80
0.31 0.93
-0.03
34
Discussion
i: Precipitation, Movement, and Terrestrial Microhabitat Use
Our results demonstrate a positive relationship between rainfall and movement in one
individual K. acutum. Given that only one animal examined produced statistically significant
results and that n=6 for all individuals, caution should be taken when attempting to draw
conclusions about patterns of behavioral ecology for K. acutum as a whole. However, this is the
first documented evidence of a correlation between K. acutum movement and precipitation in
their environment; a relationship that has been anecdotally taken for granted.
The statistically significant relationship found between precipitation and turtle #6’s
movement may support the notion that the Tabasco mud turtle’s forays are driven, at least in
part, by rainfall events. Burke et al., (1994) document Kinosternon subrumum in the southeast
United States remaining stationary in burrows until the advent of rainfall events that trigger
nesting behavior. The authors hypothesize that rainfall may be acting as camouflage from
predators; eliminating odors and tracks left by the nesting turtles. We did not observe any nesting
behavior but suggest that #6’s spikes in movement after rainfall may serve a similar function in
foraging or reproduction.
Our findings of statistically significant relationships between precipitation and movement
extended to only one animal out of the six examined in this study. The remaining five animals’
movement does not appear to be correlated with rainfall as we might have expected. We have
identified three potential explanations for this occurrence: 1) that the Tabasco mud turtle is not as
reliant on the presence of fresh water as previously thought (Iverson & Vogt, 2011); 2) that
conducting surveys during daylight hours may have missed nocturnal aquatic foraging behavior
35
by these animals and; 3) that our survey took place during an abnormally dry beginning on the
wet season in this region of Belize.
Our analysis of K. acutum’s microhabitat use may support the notion that the Tabasco
mud turtle is not as dependent on dry land as previous researchers have identified (Legler &
Vogt, 2013; Iverson & Vogt, 2011). K. acutum is considered a semi-aquatic animal and this
study focused on observing its behavior at the transition from dry- to wet-season in this region of
Belize. The vast majority (92%) of observations were made on dry land, despite the presence of
ephemeral pools, wetlands, and streams nearby. The question of why these K. acutum were not
utilizing available aquatic habitat remains open. Consulting freshwater turtle and tortoise experts
were surprised to hear our preliminary results indicating much greater use of land-based
microhabitats than aquatic (Fig. 17) by the animals in this study, and made the claim that these
Kinosternon were behaving much more like wood turtles of the genus Glyptemys than their other
congenerics (Eric Munscher, personal communication). Perhaps the amount of precipitation
during the study period was not sufficient to stimulate an adapted rainy-season response. We
measured 91 mm of rain during the first weeks of July, which was below average for this time of
year in southern Belize (Bridgewater, 2012; Heyman, 1999).
Stone (2001) notes that the Sonoran mud turtle (Kinosternon sonoriense) is forced to
make use of terrestrial habitat for aestivation during periods of drought and heat but that their
populations don’t necessarily suffer negatively during extended periods of adverse conditions.
The subject animals for this project were located during daytime hours when ambient
temperatures were at their highest; perhaps these turtles were engaging in aestivation behavior,
as documented by Iverson & Vogt (2011). Their high use rate of leaf litter and tree cover (leaf
litter and tree cover made up over 2/3 of our microhabitat use observations) may support this
36
assertion. Aparicio et al. (2018) note the use of heat-sheltering microhabitat among Mexican
mud turtles during their aestivation periods lasting up to six months. Perhaps the Tabasco mud
turtles in this study were engaging in similar behavior.
Our movement results contrast sharply with movement described by other authors like
Aparicio et al. (2018). They found the Mexican mud turtle’s movement range to up to 27,000
meters, while our maximum straight-line movement observed was only 275 meters, though we
did not perform a home range analysis. The limited distance our turtles traveled over the course
of this study may also contribute to a corroboration of findings by Slavenko et al. (2016), which
state that a turtle’s range size is closely linked with the size of its body.
Iverson and Vogt (2011) report that K. acutum is largely nocturnal but do not present this
data so it remains anecdotal. Primarily nocturnal foraging behavior may account for the lack of
observations made in water bodies; surveys were conducted exclusively during the day, and it is
certainly possible that the animals were utilizing aquatic habitat at nighttime and returning to a
day-time resting location. Animals were also rarely located in motion; most observations were of
stationary animals hiding in vegetative material. It is possible that the turtles were aware of the
research team’s presence and deliberately concealed themselves before the team was close
enough for visual observation.
Regardless, our findings highlight literature gaps in K. acutum’s natural history and
behavioral ecology. Future research is needed to establish the extent to which K. acutum’s
movement and behavior is influenced by local precipitation patterns, the extent to which it may
or may not be nocturnal, and its use of terrestrial habitat.
37
ii: Animal Size
We had trouble locating enough individuals of sufficient size to affix transmitters to. We
decided not to attach more than 8% by body weight of transmitter and epoxy to each animal and
this proved a significant deterrent to our eventual sample size. Our original goal was to have 20
animals tracked over the course of the study period. After 5 days of searching yielded only 6
animals massive enough to bear the weight of the transmitters, we decided to use half of the
transmitters on another species present at the site, Claudius angustatus, which is also greatly
underrepresented in the literature (those results will be presented elsewhere).
We located numerous juveniles and subadults while searching for adult K. acutum and
have speculated on the reason for a dearth in adequately sized adults. We surveyed the site
during the summer of 2021 and located numerous adequately sized adults (Munscher et al., 2023,
in press). We suspect the difference between the initial survey in 2021 and the 2022 period may
have been amount of precipitation. 2021 saw a much wetter beginning to the dry season than did
2022 and this may account for continued torpor in the local Tabasco mud turtles and thus our
less successful capture rates.
It's also possible that K. acutum is in competition with the white-lipped mud turtle
(Kinosternon leucostomum) at this site in Belize. Numerous K. leucostomum were captured using
baited hoop and net traps while only a few K. acutum were netted in this manner. K.
leucostomum inhabits a similar ecological niche as K. acutum and may be preventing Tabasco
mud turtles from utilizing, through competitive exclusion, the same aquatic habitats the whitelipped mud turtles are enjoying. This would account for the small amount of K. acutum captured
in aquatic traps despite their being considered a semi-aquatic species.
38
iii: Cohune Palm
Finally, we included the cohune palm (Attalea cohune) in microhabitat use analysis due
to its ubiquity across the study site and its seeds' similarity in appearance to the carapace of an
adult K. acutum when partially submerged in water. They appear so similar at a glance that many
Attalea cohune seeds were ‘captured’ in lieu of Tabasco mud turtles. The turtles could have been
subject to natural selection favoring a resemblance to cohune seeds to act as camouflage from
predators (Duarte, 2018). This is of course speculative, but the similarity is so striking it seems
worth further investigation.
39
Conclusion
In conclusion, we present this expansion of the Tabasco mud turtle’s known natural
history. This thesis has examined relationships between precipitation and movement in a
population of Kinosternon acutum in a seasonally-dry tropical rainforest of southern Belize. Our
results, while limited in temporal and geographic scope, are at least suggestive of a potentially
contradictory duality in the Tabasco mud turtle’s behavioral ecology. We uncovered a
statistically significant relationship between movement and rainfall for one individual while
failing to achieve the same results for the remaining animals studied. Far from being
disappointing, this seeming contradiction opens the door for further research and speculation on
the Tabasco mud turtle’s life history by potentially undermining assumptions about its use of
terrestrial habitat. We hope that this project will pave the way for future studies of K. acutum and
provide further illumination of this animal’s unique life history.
40
Bibliography
Allan, R. P., & Soden, B. J. (2008). Atmospheric Warming and the Amplification of Precipitation
Extremes. Science, 321(5895), 1481–1484.
Andresen, C. (2019). Kinosternon sonoriense (Sonoran Mud Turtle). Herpetological Review,
50(4), 773–774.
Anthonysamy, W. J. B., Dreslik, M. J., & Phillips, C. A. (2013). Disruptive Influences of
Drought on the Activity of a Freshwater Turtle. American Midland Naturalist, 169(2), 322–
335.
Acosta, G., Beramendi, L. E., González, G., Rivera, I., Eudave, I., Hernández, E., Sánchez, S.,
Morales, P., Cienfuegos, E., & Otero, F. (2018). Climate change and peopling of the
Neotropics during the Pleistocene-Holocene transition. Boletín de La Sociedad Geológica
Mexicana, 70(1), 1–19.
Aparicio, Á., Mercado, I. E., Ugalde, A. M., Gaona-Murillo, E., Butterfield, T., & Macip-Ríos, R.
(2018). Ecological Observations of the Mexican Mud Turtle (Kinosternon integrum) in the
Pátzcuaro Basin, Michoacán, México. Chelonian Conservation & Biology, 17(2), 284–290.
Ashton, K. G., & Feldman, C. R. (2003). Bergmann’s Rule in Nonavian Reptiles: Turtles Follow
It, Lizards and Snakes Reverse It. Evolution, 57(5), 1151–1163.
Bernstein, N. P., & Christiansen, J. L. (2011). Response of a Yellow Mud Turtle (Kinosternon
flavescens Agassiz) Community to Habitat Change: Management Implications for a Nature
Preserve. Natural Areas Journal, 31(4), 414–419.
Berriozabal-Islas, C., Ramírez-Bautista, A., Torres-Ángeles, F., Mota Rodrigues, J. F., MacipRíos, R., & Octavio-Aguilar, P. (2020). Climate change effects on turtles of the genus
41
Kinosternon (Testudines: Kinosternidae): an assessment of habitat suitability and climate
niche conservatism. Hydrobiologia, 847(19), 4091–4110.
Bridgewater, S. (2012). A Natural History of Belize: Inside the Maya Forest. University of Texas
Press.
Burke, V. J., & Gibbons, J. W. (1994). Prolonged nesting forays by common mud turtles
(Kinosternon subrubrum). American Midland Naturalist, 131(1), 190.
Butler, C. J., Stanila, B. D., Iverson, J. B., Stone, P. A., & Bryson, M. (2016). Projected changes
in climatic suitability for Kinosternon turtles by 2050 and 2070. Ecology and Evolution,
6(21), 7690–7705.
Butterfield, T. G., Scoville, A., García, A., & Beck, D. D. (2018). Habitat Use and Activity
Patterns of a Terrestrial Turtle (Rhinoclemmys rubida perixantha) in a Seasonally Dry
Tropical Forest. Herpetologica, 74(3), 226–235.
Campbell, J. A. (1998). Amphibians and Reptiles of Northern Guatemala, the Yucatan, and
Belize. University of Oklahoma Press.
Cavallo, C., Dempster, T., Kearney, M. R., Kelly, E., Booth, D., Hadden, K. M., & Jessop, T. S.
(2015). Predicting climate warming effects on green turtle hatchling viability and dispersal
performance. Functional Ecology, 29(6), 768–778.
Chou, C., Chen, C.-A., Tan, P.-H., & Chen, K. T. (2012). Mechanisms for Global Warming
Impacts on Precipitation Frequency and Intensity. Journal of Climate, 25(9), 3291–3306.
Chou, C., & Lan, C.-W. (2012). Changes in the Annual Range of Precipitation under Global
Warming. Journal of Climate, 25(1), 222–235.
Cordero, G. A., & Swarth, C. W. (2010). Notes on the movement and aquatic behavior of some
kinosternid turtles. Acta Zoológica Mexicana, 26(1), 233–235.
42
de Jesús Cervantes-López, M., Arasa-Gisbert, R., Hérnandez-Ordóñez, O., & Arroyo-Rodríguez,
V. (2021). Distribution extension and first verified records for Narrow-bridged Musk Turtle,
Claudius angustatus Cope, 1865 (Testudines, Kinosternidae) in the Selva Lacandona,
Mexico. Check List, 17(6), 1639–1646.
Duarte, R. C., Stevens, M., & Flores, A. A. V. (2018). The adaptive value of camouflage and
colour change in a polymorphic prawn. Scientific Reports, 8(1), Article 1.
Eastern Mud Turtle (Kinosternon subrubrum)—Species Profile. (n.d.). USGS Nonindigenous
Aquatic Species Database. Retrieved June 4, 2023, from
https://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=1267
Eastern Musk Turtle (Sternotherus odoratus)—Species Profile. (n.d.). USGS Nonindigenous
Aquatic Species Database. Retrieved June 4, 2023, from
https://nas.er.usgs.gov/queries/FactSheet.aspx?speciesID=1269
Ernst, C. H. & Lovich, Jeffrey. (2009). Turtles of the United States and Canada. Johns Hopkins
University Press.
Ewert, M. A., & Nelson, C. E. (1991). Sex Determination in Turtles: Diverse Patterns and Some
Possible Adaptive Values. Copeia, 1991(1), 50–69.
Forsyth, A., & Miyata, K. (1984). Tropical Nature. Scribner.
Geller, G. A., Doody, J. S., Clulow, S., & Duncan, R. P. (2022). Do Freshwater Turtles Use
Rainfall to Increase Nest Success? Frontiers in Ecology and Evolution, 10.
Gray, J. E. (1831). Synopsis reptilium: Or short descriptions of the species of reptiles Part I
Cataphracta. Tortoises, crocodiles, and enaliosaurians (Vol. 1831). Treuttel, Wurtz, and
Co.
43
Hall, D. H., & Steidl, R. J. (2007). Movements, Activity, and Spacing of Sonoran Mud Turtles
(Kinosternon sonoriense) in Interrupted Mountain Streams. Copeia, 2007(2), 403–412.
Heyman, W. D., & Kjerfve, B. (1999). Hydrological and Oceanographic Considerations for
Integrated Coastal Zone Management in Southern Belize. Environmental Management,
24(2), 229–245.
Hutchison, V. H., Vinegar, A., & Kosh, R. J. (1966). Critical Thermal Maxima in Turtles.
Herpetologica, 22(1), 32–41.
Iverson, J. B. (1976). The Genus Kinosternon in Belize (Testudines: Kinosternidae).
Herpetologica, 32(3), 258–262.
Iverson, J. B. (1986). Notes on the Natural History of the Oaxaca Mud Turtle, Kinosternon
oaxacae. Journal of Herpetology, 20(1), 119–123.
Iverson, J. B. (1989). Natural History of the Alamos Mud Turtle, Kinosternon alamosae
(Kinosternidae). The Southwestern Naturalist, 34(1), 134–142.
Iverson, J. B. (1999). Reproduction in the Mexican Mud Turtle Kinosternon integrum. Journal of
Herpetology, 33(1), 144–148.
Iverson, J. B., Le, M., & Ingram, C. (2013). Molecular phylogenetics of the mud and musk turtle
family Kinosternidae. Molecular Phylogenetics and Evolution, 69(3), 929–939.
Iverson, J. B., & Vogt, R. C. (2011). Kinosternon acutum Gray 1831—Tabasco Mud Turtle,
Montera, Chechagua de Monte. Chelonian Research Monographs, No. 5, 062.1-062.6.
Kricher, J. (2017). The New Neotropical Companion. Princeton University Press.
Lee, Julian. (1996). The Amphibians and Reptiles of the Yucatan Peninsula. Cornell University
Press.
44
Legler, J., & Vogt, R. C. (2013). The Turtles of Mexico: Land and Freshwater Forms. University
of California Press.
Morales-Verdeja, S. A., & Vogt, R. C. (1997). Terrestrial Movements in Relation to Aestivation
and the Annual Reproductive Cycle of Kinosternon leucostomum. Copeia, 1997(1), 123–
130.
Munscher, E. C., Walde, A. D., Riedle, J. D., Hootman, T., Weber, A. S., Osborne, W., Brown,
J., Butterfield, B. P., & Hauge, J. B. (2020). Demographics of Sympatric Musk Turtles: The
Loggerhead Musk Turtle (Sternotherus minor) and Eastern Musk Turtle (Sternotherus
odoratus) in a Florida Spring Ecosystem. Chelonian Conservation & Biology, 19(1), 36–47.
Munscher, E., Walde, A. D., Stratmann, T., & Butterfield, B. P. (2015). Exceptional Growth
Rates Observed in Immature Pseudemys from a Protected Spring System in Florida.
Herpetology Notes, 8, 133–140.
Munscher, E., Pop, T., Pearson, L., Barrett, H., Knauss, G., Marlin, J., McAvinchey, C.,
Morrison, M., Pigneatelli, J., Stein, J., Tuggle, A., & Walde, A. (2022). Range Extension
and First Verified Observation of the Narrow-bridged Musk Turtle Claudius angustatus
from the Toledo District of Southern Belize. Herpetology Notes, 15, 735–740.
Nations, J. (2006). The Maya Tropical Forest: People, parks, and ancient cities. University of
Texas Press.
Nguyen, P., Thorstensen, A., Sorooshian, S., Hsu, K., Aghakouchak, A., Ashouri, H., Tran, H., &
Braithwaite, D. (2018). Global Precipitation Trends across Spatial Scales Using Satellite
Observations. Bulletin of the American Meteorological Society, 99(4), 689–698.
Pempelfort, H. (2018). Mud Turtles—An Introduction. Radiata-English Edition, 27(1), 4–9.
45
Rainwater, T. R., Pop, T., Cal, O., Garel, A., Platt, S. G., & Hudson, R. (2012). A Recent
Countrywide Status Survey of the Critically Endangered Central American River Turtle
(Dermatemys mawii) in Belize. Chelonian Conservation and Biology, 11(1), 97–107.
Reneker, J. L., & Kamel, S. J. (2016). Climate change increases the production of female
hatchlings at a northern sea turtle rookery. Ecology, 97(12), 3257–3264.
Reyes-Velasco, J., Iverson, J. B., & Flores-Villela, O. (2013). The Conservation Status of Several
Endemic Mexican Kinosternid Turtles. Chelonian Conservation & Biology, 12(1), 203–208.
Rhodin, A., Pritchard, P., van Dijk, P. P., Saumure, R., Buhlmann, K., Iverson, J., & Mittermeier,
R. (Eds.). (2011). Conservation Biology of Freshwater Turtles and Tortoises (First).
Chelonian Research Foundation.
Rowe, J. W., Gradel, J., & Bunce, C. F. (2013). Effects of Weather Conditions and Drought on
Activity of Spotted Turtles (Clemmys guttata) in a Southwestern Michigan Wetland.
American Midland Naturalist, 169(1), 97–110.
Semlitsch, R. D., & Bodie, J. R. (2003). Biological Criteria for Buffer Zones around Wetlands
and Riparian Habitats for Amphibians and Reptiles. Conservation Biology, 17(5), 1219–
1228.
Slavenko, A., Itescu, Y., Ihlow, F., & Meiri, S. (2016). Home is where the shell is: Predicting
turtle home range sizes. Journal of Animal Ecology, 85(1), 106–114.
Stone, P. A. (2001). Movements and Demography of the Sonoran Mud Turtle, Kinosternon
sonoriense. The Southwestern Naturalist, 46(1), 41–53.
Ultsch, G. R. (2006). The ecology of overwintering among turtles: Where turtles overwinter and
its consequences. Biological Reviews, 81(3), 339–367.
46
Vogt, R. C., & Flores-Villela, O. (1992). Effects of Incubation Temperature on Sex
Determination in a Community of Neotropical Freshwater Turtles in Southern Mexico.
Herpetologica, 48(3), 265–270.
Waldock, C., Dornelas, M., & Bates, A. E. (2018). Temperature-Driven Biodiversity Change:
Disentangling Space and Time. BioScience, 68(11), 873–884.
Walker, D., & Avise, J. C. (1998). Principles of Phylogeography as Illustrated by Freshwater and
Terrestrial Turtles in the Southeastern United States. Annual Review of Ecology &
Systematics, 29, 23.
Waterson, A. M., Schmidt, D. N., Valdes, P. J., Holroyd, P. A., Nicholson, D. B., Farnsworth, A.,
& Barrett, P. M. (2016). Modelling the climatic niche of turtles: A deep-time perspective.
Proceedings: Biological Sciences, 283(1839), 1–9.
Wilhelm, C. E., & Plummer, M. V. (2012). Diet of Radiotracked Musk Turtles, Sternotherus
odoratus, in a Small, Urban Stream. Herpetological Conservation and Biology. 7(2):258–
264.
Zhang, W., & Zhou, T. (2019). Significant Increases in Extreme Precipitation and the
Associations with Global Warming over the Global Land Monsoon Regions. Journal of
Climate, 32(24), 8465–8488.
47
