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Morphology, Diet, and Population Structure of the Southern White-lipped Mud Turtle Kinosternon leucostomum postinguinale (Testudines: Kinosternidae) in the Nus River Drainage, Colombia

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Most existing studies on the White-lipped Mud Turtle, Kinosternon leucostomum, have been based on northern Central American populations, leaving a lack of information on populations from southern Central America and South America. Herein we studied morphology, diet, and population structure of a population of the southern Kinosternon leucostomum postinguinale inhabiting four creeks in Colombia. Observed habitats used were highly variable, ranging from relatively clean waters to streams used for sewage disposal of wastewater from a human settlement. Body size was smaller than that of other populations of southern K. l. postinguinale and also than that of the northern K. l. leucostomum. Sexual dimorphism was evident, with males heavier, longer, and wider than females. Body size was associated with the habitat of origin, with Barrio Nuevo individuals being the largest. The main components of the diet were plant material, insects, snails, and algae. We did not find evidence of sexual differences in the diet, but we found geographic differences in the body size. The population with the largest individuals, from Barrio Nuevo Creek, consumed more snails while those from Totumo Creek, the population with the smallest individuals, consumed more ants and plant material as compared to the other creeks. Additionally, we found a highly male-biased sex ratio, with 2.5 adult males per female, very few juveniles, and no nests, which suggests a dangerous risk of population decline. We suggest continued monitoring of the demography of this population, emphasizing its reproductive biology.
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Journal of Herpetology, Vol. 0, No. 0, 000–000, 0000
Copyright 2016 Society for the Study of Amphibians and Reptiles
Morphology, Diet, and Population Structure of the Southern White-lipped Mud Turtle
Kinosternon leucostomum postinguinale (Testudines: Kinosternidae) in the Nus River
Drainage, Colombia
CLAUDIA P. C EBALLOS,
1,2
DANIEL ZAPATA,
1
CAROLINA ALVARADO,
1
AND EISINHOWER RINC ´
ON
3
1
Grupo Centauro, Escuela de Medicina Veterinaria, Facultad de Ciencias Agrarias, Universidad de Antioquia, Medellı´n, Colombia
3
Escuela Ambiental, Facultad de Ingenieria, Universidad de Antioquia, Puerto Berrı´o, Colombia
ABSTRACT.—Most existing studies on the White-lipped Mud Turtle, Kinosternon leucostomum, have been based on northern Central
American populations, leaving a lack of information on populations from southern Central America and South America. Herein we
studied morphology, diet, and population structure of a population of the southern Kinosternon leucostomum postinguinale inhabiting
four creeks in Colombia. Observed habitats used were highly variable, ranging from relatively clean waters to streams used for sewage
disposal of wastewater from a human settlement. Body size was smaller than that of other populations of southern K. l. postinguinale and
also than that of the northern K. l. leucostomum. Sexual dimorphism was evident, with males heavier, longer, and wider than females.
Body size was associated with the habitat of origin, with Barrio Nuevo individuals being the largest. The main components of the diet
were plant material, insects, snails, and algae. We did not find evidence of sexual differences in the diet, but we found geographic
differences in the body size. The population with the largest individuals, from Barrio Nuevo Creek, consumed more snails while those
from Totumo Creek, the population with the smallest individuals, consumed more ants and plant material as compared to the other
creeks. Additionally, we found a highly male-biased sex ratio, with 2.5 adult males per female, very few juveniles, and no nests, which
suggests a dangerous risk of population decline. We suggest continued monitoring of the demography of this population, emphasizing
its reproductive biology.
Resumen.—La informaci ´
on existente sobre la Tortuga Tapaculo, Kinosternon leucostomum, ha sido generalmente basada en las
poblaciones del norte de Centro Ame´rica, dejando un desconocimiento sobre las poblaciones del sur de Centro Ame´rica y Sur Ame´rica.
En este trabajo nosotros documentamos la morfologı´a, dieta, y estructura de una poblaci ´
on de la subespecie el sur K. l. postinguinale que
habita en 4 quebradas en Colombia. Los ha´bitats observados fueron muy variables, desde quebradas relativamente limpias hasta
quebradas que reciben aguas negras de asentamientos humanos. El taman˜o corporal fue menor a lo reportado por otras poblaciones de la
misma subespecie e incluso de la subespecie del norte, K. l. leucostomum. El dimorfismo sexual fue evidente, con machos ma´s pesados,
largos, y anchos que las hembras. El taman˜ o corporal estuvo asociado al ha´bitat de origen, siendo las tortugas de Barrio Nuevo las ma´s
grandes. La dieta estuvo compuesta de material vegetal, insectos, caracoles, y algas. Nosotros no encontramos diferencias sexuales en la
dieta pero si diferencias geogra´ficas en el taman˜ o. Las tortugas de Barrio Nuevo que fueron las ma´ s grandes consumieron ma´s caracoles,
mientras que las tortugas ma´ s pequen˜ as de El Totumo consumieron ma´s plantas y hormigas en compariaci ´
on con los otras quebradas.
Adicionalmente, encontramos una proporci ´
on sexual sesgada hacia los machos, con 2.5 machos por hembra, muy pocos juveniles y
ning ´
un nido, lo que sugiere un riesgo peligroso de disminuci ´
on poblacional. Recomendamos un monitoreo continuo de la demografı´a de
esta poblaci ´
on y sobre su biologı´a reproductiva en particular.
Within the order Testudines is the Neotropical family
Kinosternidae, comprised of 26 species and 38 subspecies
distributed from Canada to Argentina (van Dijk et al., 2014).
The traditional phylogeny of Kinosternidae has been challenged
by a recently proposed phylogenetic hypothesis (Iverson et al.,
2013) in which some species were reallocated to a new genus
and some subspecies were supported as distinct species. Other
authors have objected to these new phylogenetic relationships
(Spinks et al., 2014). Nevertheless, this debate highlights the
need for further genetic and biologic studies covering the widest
possible distributional range of all entities.
Within this family is the White-lipped Mud Turtle, Kinoster-
non leucostomum (Dume´ril and Bibr ´
on, in Dume´ril and Dume´ril
1851), with its two subspecies: the Northern White-lipped Mud
Tur tle , Kinosternon leucostomum leucostomum,rangingfrom
Me´xico to Nicaragua, and the Southern White-lipped Mud
Turtle , Kinosternon leucostomum postinguinale, ranging from
Nicaragua to Peru (van Dijk et al., 2014). This species is not
currently assessed by the International Union for Conservation
of Nature (IUCN, 2015) but it was listed as Least Concern in
1996 (van Dijk et al., 2014). Turtle specialists, however, have
suggested listing it as Least Concern (van Dijk et al., 2014). In
Colombia, K. leucostomum faces numerous problems including
habitat degradation, human consumption, exploitation for the
crafting of ornaments, and as pets (Giraldo et al., 2012).
In general, K. leucostomum is recognized for its unicarinate
carapace, plastron with two hinges, and head with a yellow to
brown stripe that extends from the eye to the neck (Berry and
Iverson, 2001; Giraldo et al., 2012). Kinosternon leucostomum
exhibits sexual dimorphism (e.g., males are recognized by a
longer and thicker tail and the presence of a patch of horny
scales on the inner surface of the hind limbs; Berry and Iverson,
2001). Their habitat includes slow waters with soft substrates
and abundant vegetation (Ernst et al., 1997) but also creeks with
abundant rocks and fast-flowing water (Acun˜ a-Mese´n, 1993).
Turtles may move 2–3 m away from their aquatic habitat and
between 50–200 m parallel to the shoreline, though they can
move up to 600 m away to nest or aestivate (Morales-Verdeja
and Vogt, 1997). This species is omnivorous with its diet
including snails, grasses, algae, aquatic insects, and seeds
consumed in an opportunistic pattern (depending on the
habitat quality or displacement in the feeding niche by
coexisting turtle species; Vogt and Guzman, 1988; Acun˜a-
Mese´n, 1993). Most of the studies of their ecology have been
2
Corresponding Author. E-mail: claudiaceb@gmail.com
DOI: 10.1670/15-035
conducted on the northern subspecies, with fewer on the
southern subspecies and none in Colombia (Giraldo et al., 2012).
Given the lack of information on the southern subspecies, K. l.
postinguinale, we monitored a population inhabiting the
Corregimiento San Jose´ del Nus, Departmento de Antioquia,
Colombia. During four field trips in 2013–2014 we trapped
turtles in four creeks that drain into the Nus River. Herein we
report on the morphometrics of this subspecies and test for
differences associated with sex and creek of origin. We identify
and quantify the diet at each site from fecal samples and
quantify the population abundance, structure, and the sex
ratios. We also describe habitat quality by identifying and
quantifying the aquatic macroinvertebrates and some physical
parameters of each creek to discuss potential relationships
between habitat, morphology, and diet. In spite of its wide
distribution in Colombia, K. l. postinguinale populations have
not been studied, so we provide new information on the biology
of this southern subspecies. We expect this information will
contribute to the understanding of conservation status for this
species and provide insight for future management plans at the
local and national levels.
MATERIALS AND METHODS
Site Description.—We conducted this study in Corregimiento
San Jose´ del Nus, Municipio San Roque, Departmento de
Antioquia, Colombia. San Jose´ del Nus has an average
temperature of 23.38C; two rainy seasons, April–May and
October–November; and two dry seasons, January–March and
July–September. The main land use is cattle grazing (CORNARE,
2012).
Habitats.—We trapped turtles in four shallow creeks that drain
into the Nus River during four field trips of 4–7 days each: Barrio
Nuevo, Puente Tierra, Totumo, and Vega (Fig. 1). The Nus River
drains into the Magdalena River, a Caribbean drainage. Trips
were done in June, August, and October 2013 and in April 2014.
To characterize the four creeks, we measured four variables at
each site: water velocity (m/s), water depth (cm), transparency
(percentage of visibility of the water depth), and water
temperature (8C) recorded between 0700–0900 h. To determine
water velocity, we measured the time it took for a leaf to drift 5 m
downstream. To measure water depth, we used a pole and a
metric tape in the deepest point, where the traps were then set.
We used a Secchi disk to measure water transparency and a
thermometer submerged 30 cm for 1 min to measure tempera-
ture.
Because populations of the same species may have different
feeding habits, depending on habitat quality (Vogt and Guz-
man, 1988), we also surveyed the aquatic macroinvertebrates of
each creek (indicative of water quality). These organisms have
relatively long life cycles and are widely distributed and
sedentary; therefore, their presence is considered to correspond
with their tolerance of the water quality (Rolda´n-Pe´ rez, 1999;
Aguirre-Ramı´rez and Caicedo-Quintero, 2013). For this purpose
we collected all macroinvertebrates present in the water with a
nylon fish net during 1 h in a 10-m long transect along the
shoreline at each trapping site. We separated all collected
macroinvertebrates from organic material, stored them in 70%
ethanol, and transported them to the lab to be identified to the
lowest taxonomic level possible. We used a taxonomic key of the
most-commonly found macroinvertebrate families in Antioquia,
Colombia (Rolda´ n-Pe´ rez, 1988). We assigned a tolerance score to
each family and placed the sum of all scores into six habitat
quality categories: <15 indicated the water is critically polluted,
16–36 very polluted, 36–60 moderately polluted, 61–100 slightly
polluted, 101–150 clean, and >150 very clean (Rolda´ n-Pe´rez,
1999).
Turtle Sampling.—Because our objective was to trap the largest
number of individuals possible, we set 2, 1, 4, and 3 traps on
Barrio Nuevo, Puente Tierra, Totumo, and Vega creeks, respec-
tively, depending on water depth in each creek. We captured
turtles using hand-made hoop traps (175 cm long ·80 cm in
diameter) from 3-inch fishing-net mesh. We baited the traps with
small pieces of fresh pork viscera (lung, liver, heart, or spleen),
checked them every morning, and replaced the baits daily. All
captured turtles were taken to a nearby fish culture station,
property of the Universidad de Antioquia (682902300
N,
FIG. 1. Map of San Jose´ del Nus, Antioquia, Colombia, indicating sampling sites of Kinosternon leucostomum postinguinale in this study.
0 C. P. CEBALLOS ET AL.
7485902400
W) (Wildlife Conservation Society, Bogota´), for pro-
cessing.
We cleaned, weighed (g), measured, and marked turtles by
notching the carapace (Cagle, 1939). We also photographed
them with a digital camera (Nikon Coolpix P510) set on a tripod
to confirm identification when recaptured. We took linear and
curved measurements of the carapace and plastron along the
medial axis with a Brown & Sharpe 30 cm (12 inch) digital
caliper (Hexagon Manufacturing Intelligence, North Kingstown,
Rhode Island, U.S.A.) to the nearest 0.01 mm and with a metric
tape to the nearest 1 mm, respectively.
Diet.— As a defensive mechanism, turtles usually defecate
when being manipulated; therefore, feces were collected directly
from the cloacal orifice or from the plastic containers in which
they were temporally housed for 1–3 h. Each collected sample
was preserved in 70% ethanol to examine dietary content. All
fecal samples were refrigerated until their arrival at the Escuela
de Veterinaria at the Universidad de Antioquia. Once in the
Parasitology Lab, feces were separated into five categories: plant
material (leaves, stems, seeds), gastropods (snails), insects, algae,
and unidentified items. Individuals of Gastropoda were identi-
fied to the species level by a specialist from the Programa de
Estudio y Control de Enfermedades Tropicales (PECET) at the
Universidad de Antioquia, and insects were identified to the
family level following the taxonomic key of a guide to the
macroinvertebrates of Antioquia (Rolda´n-Pe´rez, 1988). Algae
were identified by a specialist from the herbarium of the
Universidad de Antioquia.
Data Analyses.—Morphological data were normally distributed
except for body weight and linear carapace width of females. To
test for sexual dimorphism and morphological differences
associated with habitat quality, we used an analysis of variance
(ANOVA) for data that were normally distributed and a Kruskal-
Wallis test for data not normally distributed. To test for
differences in the diet associated to the habitat of origin, we
used the overall sex ratio as the null hypothesis. Pairwise
comparisons were tested using a Bonferroni-corrected alpha
(0.05/6 =0.0083). To test for differences in linear carapace length
(LCL) and body weight (BW) distributions of males and females,
we used a Kolmogorov-Smirnov test. All data analyses were
completed with R 3.1.1 software (R Core Team, 2014).
RESULTS
Turtle Habitats.—All four creeks were perennial streams and
their channels were shallow and slow moving (1.8 m deep,
0.3 m/s); however, during the rainy season the water volume
may increase drastically and form temporary waterfalls which
may flood nearby cattle pastures. We estimated physical
parameters (Table 1) and a water contamination index based on
the identified macroinvertebrate families (Appendix 1) for each
creek.
Barrio Nuevo Creek takes its name from a human settlement
along the creek and a railroad line; residents use this creek for
sewage disposal. Accordingly, the biological monitoring work-
ing party (BMWP) scores (Appendix 1) indicated this creek to be
heavily polluted, the worst water quality of all four creeks.
Puente Tierra Creek was the shortest of the four study creeks,
originating in a small gallery forest and draining into Vega
Creek; we set up only one trap because the creek was too
shallow. The BMWP score in this creek suggested a slightly
polluted water quality. Totumo Creek was surrounded by open
areas of cattle pasture and fed a small pond that was densely
covered by a patch of gallery forest. The BMWP index
suggested a slightly polluted to very polluted water quality.
Finally, Vega Creek also was surrounded by cattle pastures and
had the fastest water velocity of all the creeks. The BMWP index
suggested the water quality of this creek was slightly to
moderately polluted.
Population Structure and Sex Ratio.—We recaptured 12 of the
total 80 turtles. Most of the time turtles were captured in traps (n
=79, 85.9%), but several were opportunistically captured by
hand (n=13, 14.1%). Totumo Creek was the site with the highest
number of turtles captured (n=35, with 8 recaptures) followed
by Barrio Nuevo (n=21, with 1 recapture), Vega (n=18, with 1
recapture), and Puente Tierra (n=6, with 2 recaptures). We
opportunistically captured turtles by hand in Barrio Nuevo and
Vega ( n=6 and 7, respectively) but none in the other two creeks.
The capture success (number of turtles captured per trap per day)
TABLE 1. Average physical and water quality characteristics calculated from the number of macroinvertebrate families observed at each creek
where Kinosternon leucostomum was captured (* indicates that the minimum and maximum values are reported when there were 2+sampling sites; n
=number of sampling sites at each creek).
Variable Barrio Nuevo (n=2) Puente Tierra (n=1) Totumo (n=4) Vega (n=3)
Water velocity, m/s (range) 0.09 (0–0.19) 0.06 (0.04–0.07) 0.08 (0–0.25) 0.25 (0.21–0.30)
Water depth, cm (range) 29.4 (8–50) 34.5 (21–48) 100.6 (29–184) 53.5 (24–104)
Transparency, % (range) 23 (8–40) 84 (79–95) 36.3 (13–100) 44 (16–100)
Water temperature, 8C (range) 24.5 23.3 (24–22.5) 23.2 (23–24) 23.2 (21.5– 26)
Number of macroinvertebrate families 1–2* 12 5–10* 6–11*
BMWP index 10–11* 84 32–67* 40–76*
Water quality Heavily
contaminated Slightly
polluted Slightly to
moderately polluted Slightly to
moderately polluted
TABLE 2. Abundance and sex distribution of Kinosternon leucostomum in San Jose´ del Nus, Antioquia, Colombia. (NA =______)
Creek Males Females Total Male-biased structure?
Barrio Nuevo 16 5 21 Yes (v
2
=5.7619, df =1, P=0.0163)
Puente Tierra 4 2 6 NA
Totumo 24 10 35 Yes (v
2
=4.8286, df =1, P=0.0279)
Vega 11 5 18 No (v
2
=2.25, df =1, P=0.1336)
Total 55 22 80 Yes (v
2
=13.254, df =1, P=0.0002)
BIOLOGY OF KINOSTERNON LEUCOSTOMUM POSTINGUINALE 0
was 0.67, 0.58, 028, and 0.46 for Totumo, Barrio Nuevo, Vega, and
Puente Tierra, respectively.
The overall observed sex ratio (28 male : 11 female) was 2.5 :
1, which deviated significantly from an expectation of 1 : 1. This
highly masculinized sex ratio was observed overall and at two
creeks, Barrio Nuevo and Totumo (Table 2). The small number
of turtles captured at Puente Tierra precluded analysis of the sex
ratio at that site.
Turtle Morphology.—Body measurements of adult turtles are
summarized in Table 3. The smallest individual was a neonate
captured by hand on the beach of Vega Creek on June 11, 2013. It
had an LCL =35.3 mm, linear carapace width (LCW) =25.8 mm,
linear plastron length (LPL) =27.5 mm, and it weighed 6.4 g.
We found significant sexual size dimorphism with males
being heavier, longer, and wider than females (Table 3). The LCL
and BW distributions of males and females differed significantly
(P<0.001 for LCL and P<0.001 for BW; Fig. 2). Most males
measured between 120–150 mm of LCL while most females
measured between 110–130 mm.
Given the habitat differences among the four creeks, we
tested for morphological differences related to the creek of
origin. Overall, turtles from Barrio Nuevo were heavier, longer,
and wider than were turtles from Totumo Creek (Table 4). This
was interesting given that aquatic macroinvertebrates found in
Barrio Nuevo Creek categorized it as heavily contaminated, yet
the turtles were the largest. On the other hand, Totumo Creek
was the site with the highest number of captures (see below) but
the turtles were the smallest.
Diet.—Of the 80 turtles captured, we collected a fecal sample
from 40 individuals. From this total, 65% had consumed plant
material (seeds, leaves, roots, or flower parts), 50% consumed
insects, 35% consumed snails, 17.5% consumed algae, and 17.5%
TABLE 3. Sexual dimorphism of Kinosternon leucostomum in San Jose´ del Nus, Antioquia, Colombia. Abbreviations: BW =Body weight (g), LCL =
Linear carapace length (mm), LCW =linear carapace width (mm), LPL =linear plastron length (mm), CCL =curved carapace length (mm), CCW =
curved carapace width (mm). Sexual dimorphism was significantly male biased in all variables (P<0.001).
Variable
Females (n=23) Males (n=54)
Male-biased sexual size dimorphismMean Min Max SD Mean Min Max SD
BW 201.4 100.0 382.6 60.2 285.5 125.0 475.0 83.5 29.5% heavier
LCL 118.2 105.2 136.2 7.6 132.8 105.0 156.0 12.1 11% longer
LCW 75.8 67.6 95.5 7.0 83.4 66.0 117.1 8.6 9.1% wider
LPL 104.9 94.2 119.0 6.1 113.0 92.0 132.3 8.1 7.2% longer
CCL 132.0 118.0 148.0 8.9 154.1 117.0 188.0 14.6 14.4% longer
CCW 115.5 96.0 140.0 10.3 125.9 93.0 152.0 12.7 8.3% longer
FIG. 2. Size class (A) and body weight (B) distributions of a population of Kinosternon leucostomum postinguinale in San Jose´ del Nus, Antioquia,
Colombia.
0 C. P. CEBALLOS ET AL.
consumed unidentified or animal material (e.g., shed skin,
unidentified muscle tissue). Specifically, we identified six insects:
leafcutter ants Atta sp. (n=15 turtles) as well as individuals, or
parts, of Gyrinidae (n=3), Gerridae (n=1), Gryllidae (n=1),
Odonata (n=1), and Hebridae (n=1). Snail (Gastropoda) shells
were barely digested, so we identified them to the species level:
Melanoides tuberculata (n=12), Pomacea palmeri (n=4), Subulina
octona (n=1), Aroapyrgus sp. (n=1), and Marisa cornuarietis (n=
1). The only green alga identified was Spirogyra sp. (n=4).
To account for the observed strong male-biased sex ratio, we
tested for diet differences associated with sex and the habitat of
origin. We did not find sexual differences in the consumption of
plant material (n
males
=22, n
females
=4, v
2
=2.11, P=0.146),
insects (n
males
=14, n
females
=6, v
2
=0.031, P=0.858), snails
(n
males
=10, n
females
=4, v
2
<0.001,P=0.976), or algae (n
males
=3, n
females
=3, v
2
=0.34, P=0.559). To test for geographic
differences, our null hypothesis tested the overall frequency of
the five food types (proportions of each category out of all 74
food items found in all creeks: 0.35 plant material, 0.27 insects,
0.19 snails, 0.095 algae, and 0.095 unidentified items). The
analysis was repeated for each creek. Food type occurrence in
Barrio Nuevo (v
2
=22.58, df =4, P=0.0001), Puente Tierra (v
2
=86.87, df =4, P<0.0001), and Vega (v
2
=58.47, df =4, P<
0.001) differed from the overall percentages, but not those in
Totumo Creek (v
2
=4.85, df =4, P=0.30). In Barrio Nuevo,
snails were consumed almost twice (35%) as much as overall
(Fig. 3). In Puente Tierra, algae were consumed more than three
times (33%) as much as overall, and no snails were found. In
Vega, the main food type was plant material (56%) and no algae
were found.
DISCUSSION
The habitat of K. l. postinguinale in northern Colombia was
highly variable. This turtle can live in heavily contaminated
environments that receive wastewater and garbage from rural
human settlements but also in muddy habitats, cleaner water
with abundant vegetation shading the stream, or in creeks with
rocks and fast-flowing water. Interestingly in this region, this
turtle also persists where waterfalls with a strong current form
during the rainy seasons, and these relatively small turtles
manage not to be washed away, as suggested from our
recaptures (6.7%). A similar habitat with cascades was reported
for this same subspecies in Costa Rica (Acun˜ a-Mese´ n, 1993).
Body size was smaller than in other populations of the same
subspecies and of the species overall. For example, on average
we found an LCL of 132.8 and 118.2 mm for males and females,
but K. l. postinguinale in Costa Rica is larger, measuring 174 and
158 mm, respectively (Acun˜ a-Mese´n, 1993). Similarly, maximum
LCL for males and females was 156 mm and 136 mm,
TABLE 4. Geographic differences in the morphometrics of Kinosternon leucostomum in four creeks in San Jose´ del Nus, Antioquia, Colombia.
Significant geographic differences were found in all variables.
Variable
Group means
Geographic
differences Pairwise comparisons
Barrio Nuevo (BN)
(n=21)
Puente Tierra (PT)
(n=6)
Totumo (T)
(n=34)
Vega (V)
(n=16)
BW 331.0 240.0 221.0 263.0 (P<0.001) BN >T(P<0.001)
LCL 138.3 122.4 124.8 126.3 (P<0.001) BN >T(P=0.0001),
BN >V(P=0.0061)
LCW 87.0 77.3 79.3 79.4 (P=0.0041) BN >T(P=0.0063)
LPL 116.6 106.1 104.8 110.4 (P=0.0193) None
CCL 157.6 140.0 143.1 148.1 (P=0.0071) BN >T(P=0.0064)
CCW 130.2 115.7 118.1 126.7 (P=0.0009) BN >T(P=0.0017)
FIG. 3. Frequency of occurrence of five food types found in the diet of Kinosternon leucostomum postinguinale in four creeks in San Jose´ del Nus,
Antioquia, Colombia.
BIOLOGY OF KINOSTERNON LEUCOSTOMUM POSTINGUINALE 0
respectively, while the maximum LCL reported for the species is
larger (175 mm and 165 mm, respectively; Berry and Iverson,
2001). Body size can vary with genetics, but also with the diet,
which in turn depends on food availability (Vogt and Guzman,
1988; Moll, 1990). Indeed, the larger individuals in our study
came from Barrio Nuevo Creek, the most-heavily contaminated
habitat; however, the main component of the diet at this stream
was snails, which are higher in protein than are insects and
plant material (mean nitrogen contents of Melanoides tuberculata
and freshwater angiosperms =9% and 2.4% dry weight,
respectively; Duarte, 1992; Mehler and Acharya, 2014). In
addition, the smaller and lighter individuals came from Totumo
Creek, where plant material and insects constituted 70% of the
diet.
Our findings agree with other studies that reported K. l.
leucostomum as an omnivorous generalist (i.e., they consume
insects, snails, fish, seeds, fruits, leaves, and even carrion in
Me´xico, northern Belize, and Costa Rica; Moll and Legler, 1971;
Vogt and Guzman, 1988; Moll, 1990; Acun˜a-Mese´ n, 1993). Other
authors have suggested that this species is primarily carnivo-
rous and eats plant material when meat is not available
(Medem, 1962). We did not find sexual differences in diet,
suggesting both sexes are similarly generalists or opportunists.
Finding aquatic snails and algae in their diet suggests they eat in
the water, as suggested by Medem (1962) and Moll and Legler
(1971). We also found terrestrial leafcutter ants in the diet,
however, and given the opportunistic nature of this species and
that it frequently moves on land (Moll and Legler 1971,
Morales-Verdeja and Vogt, 1997), it may feed on land as well
(Acun˜ a-Mese´ n, 1993).
We found a strong male-biased sex ratio (55 : 22) overall as
well as locally at the two sites with the most turtles trapped:
Barrio Nuevo (16 : 5) and Totumo (24 : 10). Factors that may
help explain the observed male-biased sex ratio of this
population include differential mortality, differential migration,
biased primary sex ratios, and even sexual size dimorphism of
the species (Gibbons, 1990; Girondot and Pieau, 1993; Lovich et
al., 2014). Regardless of the reason, the situation is of critical
concern as it suggests a serious risk of population extirpation.
And there is precedent for this concern: A population of
Clemmys insculpta in the United States, monitored for 20 yr,
revealed a reduction in the number of females and an increase in
age associated with human development until the turtle
population disappeared (Garber and Burger, 1995). We urge
further monitoring of the demography and reproduction of this
population, especially regarding the number of eggs and
clutches produced and the specific mechanism of sex determi-
nation.
Acknowledgments.—We thank our undergraduate students
and the staff of the Estaci ´
on Piscı´cola in San Jose´ del Nus,
particularly O. Franco, for logistical support during fieldwork. J.
F. Toro granted us access to the Experimental Station El Nus of
Corpoica. We thank L. E. Vela´ squez from the PECET for
gastropod identification and F. Cardona for algae identification.
This study was sponsored by a research grant from Convoca-
toria de proyectos de investigaci ´
on (CODI), Regionalizaci ´
on
2012 to CC, and the Programa de Sostenibilidad 2014–2015 of
the Universidad de Antioquia. This research was approved by
the Comite´de ´
Etica para la Experimentaci ´
on con Animales of
the Universidad de Antioquia as stated in Act 85 of 2013 and
research permit 135–0079 issued by the local government
authority CORNARE in 2012.
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0 C. P. CEBALLOS ET AL.
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APPENDIX 1. Aquatic macroinvertebrate families identified at each of the 10 trapping sites in Barrio Nuevo, Puente Tierra, Totumo, and Vega creeks
and the BMWP scores (Rolda´n-Pe´rez, 1999) assigned to each family to estimate water quality of the creek.
Macroinvertebrate
Barrio Nuevo Puente Tierra Totumo Vega
1 2 3 4 5678 9 10
Aeshnidae - - - - - 6 - - - -
Belostomatidae 5 - 5 - - - 5 - - -
Calopterygidae - - 7 - - - - - 7 7
Coenagrionidae - - - - 7 7 - - - 7
Corixidae - - 7 - - - - - 7 -
Dytiscidae - - - - 9 - - - - -
Elmidae - - - 6 - - - 6 - -
Ephemerellidae - - - - - - - - 9 -
Gelastocoridae - - - - - - - 5 5 5
Gerridae - - 8 - 8 8 8 8 8 -
Gomphidae - - 10 - 10 10 - - - 10
Gyrinidae - - 9 - - - 9 - 1 -
Hebridae - - - 8 - - 8 - - -
Hidrometridae - - - - - 4 - - - -
Hydropsychidae - - 7 - - - - - - -
Libellulidae 6 - 6 6 6 6 - - 6 6
Mesovelidae - - - 5 - - - - 5 -
Naucoridae - - 7 - 7 7 - - - -
Nepidae - - - - - - - - 5 5
Noteridae - - 4 - - 4 - - - -
Notonectidae - - - 7 7 - 7 - 7 -
Planariidae - - - - - - - 7 - -
Pleidae - - - - - - - 8 - -
Ptylodactylidae - 10 - - - - - - - -
Saldidae - - - - - - - - 8 -
Scirtidae - - - - 7 7 - - - -
Staphylinidae - - 6 - - - 6 - - -
Veliidae - - 8 - - 8 8 8 - -
Total BMWP 11 10 84 32 61 67 51 42 68 40
Water quality Heavily polluted Slightly polluted Slightly to
very polluted Slightly to
moderately polluted
BIOLOGY OF KINOSTERNON LEUCOSTOMUM POSTINGUINALE 0
... In the MorphoJ 1.06d® program (Klingenberg, 2008), the generated coordinates were overlapped by Generalized Procrustes analysis, producing a matrix with the scores of partial deformations. This procedure removes the variation in size, position, and orientation, transforming it into a unit of centroid size (square root of the sum of squares of the distances of each reference point from the centroid), patterns (Cabrera and Colantonio, 1997;Ceballos et al., 2016;Fachín-Terán et al., 2003;Gosnell et al., 2009;Lovich et al., 2010;Vieira and Costa, 2006;Forero-Medina et al., 2007). Some authors report that K. scorpioides has evident sexual dimorphism, based on macroscopic evaluations of adult individuals, evidencing males are generally larger than females, with a longer tail and concave plastron, and females with a smaller tail and straight plastron (Castro, 2006;Pereira andLemos, 2007, Ferrara et al., 2017). ...
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A study of the community ecology of neotropical freshwater turtles revealed feeding differences between Kinosternon leucostomum, Staurotypus triporcatus, and Trachemys scripta. Quantitative analysis of the flushed stomach contents showed a wide degree of food overlap between the species. The Shanon-Wiener diversity index H′ suggested that Staurotypus was a mollusk specialist under some conditions, but consumed a much higher quantity of plant material (seeds) than previously assumed. Kinosternon leucostomum was an omnivorous generalist in both populations studied. In one lake, in which Staurotypus was absent, the quantity of animal prey consumed by Kinosternon was significantly higher than in the other lake in which Staurotypus also occurred. The population of Kinosternon consuming more animal prey grew faster and larger, and had larger clutches of larger eggs. Sexual dimorphism of head size in Kinosternon was not related to dietary differences in the populations studied.
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This study documents the detrimental effects of human recreation on the North American wood turtle (Clemmys insculpta) in Connecticut. We chronicled the dynamics of two allopatric wood turtle populations in a protected southern New England wildlife reserve for 20 yr (1974-1993). Both wood turtle populations were reproductively isolated from one another, physically separated \approx100 yr ago when a 1.5 km long human-made pond was constructed. We conducted a mark-and-recapture study on a 1000-ha section of a protected watershed in south-central Connecticut (New Haven County). During this study we monitored 133 different wood turtles, observing them a total of 1176 times. Human and wood turtle demographics were recorded throughout this period. The data support the following conclusions: (1) following a period of apparent stability, two populations of wood turtles declined; (2) the declines were more or less synchronous in both populations; (3) the beginning of each decline corresponded to the opening of the habitat for recreation; (4) an increase in mean turtle age suggests a failure of recruitment; however, (5) a simultaneous reduction in numbers of adult females suggests that the failure of recruitment alone is not sufficient to explain the declines. Throughout our study the size of the forest remained the same, road building was restricted, and the quality of the air and water were constant. The wood turtle populations remained stable when people were denied access to the property. When this area was opened to human recreation (hiking, fishing) the two discrete wood turtle populations declined steadily; the total number of turtles in both populations declined by 100% in 10 yr. As wilderness areas become mixed-use recreation areas, wood turtle populations may suffer. We conclude that without proper management, the increasing recreational use of parks, reservoirs, and wildlife reserves will adversely affect the long-term survival of the North American wood turtle.
Article
Movements in the water and on land were recorded for Kinosternon leucostomum at a temporary lake in southern Veracruz, Mexico. Turtles were marked and followed on land with radio transmitters and relocated with the help of a trained dog. Turtles had a linear home range in the lake of 50-200 m, parallel to the shoreline, of which 10-50% was most actively used (activity range). Turtles moved up to 600 m away from their activity areas to nesting areas and aestivating sites. During the two years of this study, turtles returned to the same activity areas after aestivation in the surrounding tropical rainforest. Because K. leucostomum utilized only part of the available aquatic habitat, caution should be used when determining biomass estimates of turtle populations in lakes and rivers from trapping along shorelines.
Article
The attainment of sexual maturity has been shown to affect measures of sexual size dimorphism (SSD) and adult sex ratios in several groups of vertebrates. Using data for turtles, we tested the model that sex ratios are expected to be male-biased when females are larger than males and female-biased when males are larger than females because of the relationship of each with the attainment of maturity. Our model is based on the premise that the earlier-maturing sex remains smaller, on average throughout life, and predominates numerically unless the sexes are strongly affected by differential mortality, differential emigration, and immigration, or biased primary sex ratios. Based on data for 24 species in seven families, SSD and sex ratios were significantly negatively correlated for most analyses, even after the effect of phylogenetic bias was removed. The analyses provide support for the model that SSD and adult sex ratios are correlated in turtles as a result of simultaneous correlation of each with sexual differences in attainment of maturity (bimaturism). Environmental sex determination provides a possible mechanism for the phenomenon in turtles and some other organisms. © 2014 The Authors. Biological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ●●, ●●–●●.
Article
A goal of modern taxonomy is to develop classifications that reflect current phylogenetic relationships and are as stable as possible given the inherent uncertainties in much of the tree of life. Here, we provide an in-depth phylogenetic analysis, based on 14 nuclear loci comprising 10,305 base pairs of aligned sequence data from all but two species of the turtle family Kinosternidae, to determine whether recent proposed changes to the group's classification are justified and necessary. We conclude that those proposed changes were based on 1) mtDNA gene tree anomalies, 2) preliminary analyses that do not fully capture the breadth of geographic variation necessary to motivate taxonomic changes, and 3) changes in rank that are not motivated by non-monophyletic groups. Our recommendation, for this and other similar cases, is that taxonomic changes be made only when phylogenetic results that are statistically well-supported and corroborated by multiple independent lines of genetic evidence indicate that non-monophyletic groups are currently recognized and need to be corrected. We hope that other members of the phylogenetics community will join us in proposing taxonomic changes only when the strongest phylogenetic data demand such changes, and in so doing that we can move toward stable, phylogenetically informed classifications of lasting value.
Article
Compilation of data for 96 phytoplankton species, 46 macroalgal species, 27 seagrass species, 11 species of freshwater angiosperms, and several mixed phytoplankton and macroalgal communities revealed a tendency toward higher concentrations of N and P in phytoplankton compared to those of macrophytes. The depletion of P, and to a lesser extent N, in macrophytes, particularly macroalgae, appears to reflect a greater degree of P and N limitation of growth of natural macrophyte populations, rather than an intrinsic difference in their chemical composition relative to that of phytoplankton. -from Author