Chemosphere 175 (2017) 373e382

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Chemosphere
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Effect of landscape tree cover, sex and season on the bioaccumulation

of persistent organochlorine pesticides in fruit bats of riparian
corridors in eastern Mexico
Carolina Valdespino a, *, Vinicio J. Sosa b
a
Red de Biología y Conservacio!n de Vertebrados, Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, Xalapa, Ver., 91070, Mexico
b
Red de Ecología Funcional, Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, Xalapa, Ver., 91070, Mexico

h i g h l i g h t s

! Persistent organochlorine pesticides (OCPs) are present in neotropical fruit bats.

! Most bats were positive for at least two of six OCPs families.
! Landscape tree cover, season or bat sex affects OCPs concentrations.
! Some high concentrations of OCPs were found.
! This is of great environmental concern considering that wild fruit is the bats' diet.

a r t i c l e i n f o a b s t r a c t

Article history: Riparian forests are recognized as important ecosystems for biodiversity conservation in transformed
Received 7 November 2016 landscapes. Many animal species that use this type of vegetation facilitate its recovery through polli-
Received in revised form nation and seed dispersal. In landscapes dominated by agrosystems and cattle ranching, persistent
10 February 2017
organochlorine pesticides (OCPs) in the riparian system may have an effect on the physiology and fitness
Accepted 12 February 2017
Available online 15 February 2017
of animals. In this study, we measured bioaccumulation of OCPs in the most abundant frugivorous bat,
Sturnira hondurensis, from the upper part of La Antigua basin, Veracruz, Mexico and, from these data,
Handling Editor: Myrto Petreas estimated accumulation by the frugivorous bat community of riparian forests in contrasting, transformed
(TL) and forested (FL) landscapes. Concentration of SDDT, Sdrines, Sclordano, SHCH, Sheptachlor and
Keywords: Sendosulfan was measured by gas-chromatography in 23 female and 33 male adult Sturnira captured
Bio-indicator during the dry and rainy seasons. Using censored data statistics, we found that the sex of the individual
La Antigua was significant for SHCH, and that interactions of landscape type (TL vs. FL) and season (dry vs. wet), and
Organochlorine compounds sex and season were significant for Sendosulfan and Sdrines, respectively. Mean SDDT (6.86 mg/g) and
Phyllostomidae
SHCH (28.22 mg/g) concentrations were lower than those reported for frugivorous bats in India but
Riparian corridor forests
concentrations of Sdrines (13.86 mg/g) were higher than those reported in insectivorous bats. In our
Frugivorous
study sites, frugivorous bats are bioaccumulating higher amounts of OCPs in TL than in FL. We discuss the
potential of this species as a bio-indicator of OCPs contamination in river basins.
© 2017 Published by Elsevier Ltd.

1. Introduction on reproductive morpho-physiological traits, thus threatening the

Persistent organochlorine compounds (POCs) are deemed a
potential risk for the survival of species. High concentrations of
POCs can lead to death while trace amounts have negative effects
* Corresponding author. Tel.: þ52 2288421853.
E-mail addresses: carolina.valdespino@inecol.mx (C. Valdespino), vinicio.sosa@
inecol.mx (V.J. Sosa).
capacity to leave progeny (Matthiessen, 2000; Rattner, 2009). The
POCs include the persistent organochlorine pesticides (OCPs), used
in agriculture and livestock and domestic animals ectoparasite
control, and polychlorobiphenyls (PCBs) used as industrial flame-
retardants.
From the site of their application, OCPs are transported by water
in organic matter particles (O'Brien et al., 2016) and, due to their
lipophilic nature and complex molecular structure, they are

http://dx.doi.org/10.1016/j.chemosphere.2017.02.071
0045-6535/© 2017 Published by Elsevier Ltd.
374 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382
bioaccumulated by organisms that feed on the contaminated ma-
terial. Biomagnification takes place throughout the food chain
when plants or animals that have bioaccumulated OCPs are sub-
sequently consumed by herbivores or predators. While their pro-
duction has been prohibited since the last century (ONU, PNUMA &
FAO, 2008), their lipophilic and bioaccumulative nature has main-
tained OCPs in the environment and their presence has been re-
ported far from where they were originally applied 20e60 years
after usage (Nakataa et al., 2005; Bajaj and Singh, 2015) and, in
some developing countries, they are still illegally used (Albert and
Loera-Gallardo, 2014; Herna !ndez-Antonio and Hansen, 2011;
Hinojosa-Garro et al., 2016).
Information on the use of OCPs in Mexico is scarce and impre-
cise. The use of significant quantities of DDT, aldrin, endrin, lindane
and dieldrin has been reported since 1971 (Albert, 2014; Benítez
and Ba !rcenas, 1996; Chanon et al., 2003; Lo !pez-Carrillo et al.,
1996), but their application was prohibited in 2000 (Chi-coyoc
et al., 2016). The presence of OCPs in wildlife has been reported
at < 500 m a.s.l. in the Gulf of Mexico region (García-Besne ! et al.,
2015; Gonzalez-Jaregui et al., 2012; Gonza !lez-Ja
!uregui et al.,
2014; Valdespino et al., 2105).
In individuals that have bioaccumulated OCPs, endocrine
disruption (Rattner, 2009) has been reported in the development of
embryos, the formation of the reproductive tract and on the con-
centration of sexual steroids. Sexual differences have been
described in bioaccumulation of OCPs (Thies et al., 1996; Guille !n
et al., 1994; Allinson et al., 2006; Mispagel et al., 2004; Gonzalez-
Jauregui et al., 2012; García-Besne ! et al., 2015), with females nor-
mally showing lower concentrations than males. The physiological
explanation of this pattern is that females eliminate OCPs through
transference to their offspring in the lipid content of the yolk during
egg formation in oviparous species and in the milk produced during
lactation in mammals (Orlando and Guillette, 2007).
Recent research has cited riverine corridors as important eco-
systems for biodiversity conservation (Ramos and dos Anjos, 2014;
Hilty and Merenlender, 2004). These are maintained either because
they are situated in inaccessible slopes or because they provide
useful shade for farm animals. Nearly 70% of vertebrate species in a
region will use riparian corridors in some significant way during
their life cycle (Naiman et al., 1993). Therefore, biodiversity con-
servation strategies have recommended maintaining and con-
necting riverine vegetation at both local and national levels
(Fremier et al., 2015; Bleich et al., 2014).
Because of their position alongside rivers, riparian strips provide
important ecosystem services, such as the deposition of organic
matter, capture of chemicals and sediments from the watershed
(Jackson et al., 2015) and temperature buffering (Ferna !ndez et al.,
2014). Contaminants that are used on livestock ranches and crop
fields adjacent to the river will reach the riparian strip by trans-
portation in runoff from the farmlands within the catchment
(Tabacchi et al., 1998). Wider riparian forests strips have been re-
ported to have naturally higher metabolic rates, primary production,
organic material cycling, and nitrogen intake than in narrow strips
(Bott et al., 2006; Sweeney et al., 2004). Therefore, the ability of wider
strips to keep and cycle the contaminants retained in organic matter
will probably be higher than that of their narrow counterparts.
The presence of organic matter (Tabacchi et al., 1998) and con-
taminants retained in the riparian forest soil and sediment (Díaz-
C!ardenas, 2013) may lead to higher risks of acquisition of disrup-
tive compounds for the wildlife using riparian corridors (Bartels
et al., 2012). Contaminants that are absorbed through root sys-
tems might be transported to the aerial parts of the plant, including
fruits, depending on soil texture, the affinity of the contaminant for
lipids and the lipid content of the plant (Collins et al., 2006). At the
same time, seasonal fluctuations in flow level cause changes in
contaminant concentrations (Latorre, 2013; Ramos-Rosas et al.,
2013) that may have a consequence on the quantities of these
contaminants that are accumulated by the animals.
Bats are one of the vertebrate groups that use riparian forests to
move between habitats and as a source for food and water. Clark
(2001), Clark et al. (1995), Geluso et al. (1976) and Guille !n et al.
(1994) studied bats in sites where population reduction was asso-
ciated with the effect of persistent contaminants. Bioaccumulation
of OCPs by bats has now been reported in different species
worldwide (23 insectivorous, three frugivorous and one nectar-
ivorous) and its long-term prevalence in bat populations was
recently reviewed (Bayat et al., 2014). However, assessment at the
community level in a particular location may be important for the
accurate evaluation of OCPs bioaccumulation in a given animal
group; for example, differences in the abundance of bat species
within a riparian forest may imply a differential risk of intoxication.
Bat communities are important due to the number of species
they normally comprise and the ecosystem services they provide,
such as arthropod control, pollination and seed dispersal
(Muscarella and Fleming, 2007; Kalka et al., 2008; Kunz et al., 2011).
Along with rodents, bats are among the ecologically most diverse
and specious groups of mammals, accounting for most of Earth's
mammal biomass (Simmons, 2005). In the wild, the effect of OCPs
on insect density and the presence of insectivorous bats has been
described (Kalcounis-Rueppell et al., 2007); however, the effect on
bats of another type of foraging guild may not be as direct and has
not been reported to date. For example, we lack information
regarding the effect on Neotropical frugivorous bats, a guild of great
importance for seed dispersal and forest regeneration. In this re-
gard, Bayat el al. (2014) recommend the collation of a more
comprehensive and standardized database of accumulation con-
centrations and to investigate an improved prediction and defini-
tion of toxicity end points in bats. Finally, due to their abundance
and relative easiness of capture, bats could be used as indicator
species in pollutant monitoring programs.
Here, we investigated the presence of OCPs in frugivorous bats
at high elevations on the eastern (Gulf of Mexico) slope of the
central mountain range of the state of Veracruz, Mexico. Land use in
this region is mainly livestock production and agriculture and man-
made pastures, a few forest remnants and riparian forest corridors
characterize the landscape. This represents a common land use
throughout tropical Central and South America at an elevation of
between 1400 and 2500 m a.s.l. where tropical montane cloud
forest was originally distributed.
In order to minimize the impact on the bat community, we
quantified the OCPs bioaccumulated by the most abundant frugiv-
orous bat species in the riverine system and extrapolated these
values to the entire frugivorous bat community of the upper part of
the La Antigua watershed. This species was the highland yellow-
shouldered bat, Sturnira hondurensis (Velazco and Patterson,
2013). Our objectives were: (1) To analyse differences in the con-
centration of OCPs bioaccumulated by Sturnira from riparian sys-
tems immersed in contrasting forested (FL) and transformed (TL)
landscapes; (2) to determine whether there were differences in the
quantities of OCPs bioaccumulated by Sturnira females and males
and between the dry and the rainy seasons; and (3) to infer the
health status of the bat community in terms of the concentrations of
OCPs that may be present in the riverine systems studied.
2. Materials and methods
2.1. Study sites
Second and third order independent rivers were selected from
the highest portion of the La Antigua basin (1700-1400 m a.s.l.) in
 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382 375

Veracruz, Mexico (Fig. 1). Two sites, Pixquiac and Piedra Blanca,
were selected within a more conserved and forested landscape (FL)
with 60% tree cover (including secondary growth vegetation) and
the other two, Monte Grande and Puente de Dios, in a less forested
and more transformed landscape (TL) with 40% tree cover. The ri-
parian forests are disturbed or secondary tropical montane cloud
forest (Williams-Linera, 2007) that border man-made pastures. The
study site characteristics have been fully described as part of a
previous study (Va!zquez et al., 2015).
2.2. Bat community
The bat community at each study site was characterized by
species richness (S ¼ number of species), abundance, and species
composition (Magurran, 2004). We used mist-nets to capture the
bats; this method is biased against insectivorous bat families that
have a more efficient echolocation system or that forage in the
higher tree strata or above the canopy. The community variables
and concentrations of OCPs estimated at the community level are
therefore only valid for bat species of the Stenodermatinae and

Fig. 1. Location of four riparian cloud forests where bats were screened for persistent organochlorine pesticides (OCPs) in eastern Mexico. Note that the landscape in the upper right
window has more vegetation cover than the landscape in the lower right window.
376 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382

Carollinae subfamilies within the nose-leafed Phyllostomidae
family. These two subfamilies accounted for 90% of overall bat
abundance at the study sites (Table 1). This also permits the
assumption that, because of their phylogenetic affinity, bat species
in these subfamilies share similar digestive and assimilation ca-
pacities of their main food (wild fruit). At each site and climatic
season, and for one night only, seven mist nets, all of mesh size
38 mm, were set from sunset to midnight; three mist nets
(10 $ 3 m) were set at random throughout the riparian forest and
four monofilament mist nets (two 9 $ 3 m nets and two 6 $ 3 m)
were placed across the river or creek. In all sites, the riparian forest
strips, wider than 10 m, extend for a distance of at least 500 m.
2.3. Determination of concentrations of OCPs
After the first sampling year of a bat diversity study conducted
in the same study sites, Sturnira hondurensis was found to be the
most abundant species and therefore the bioaccumulation report
was focused on this species. Most captured bats were identified,
weighed, sexed and released. For screening of OCPs, 23 female and
33 male adult bats were maintained in cotton bags until laboratory
processing. In the lab, the animals were anesthetized to death with
chloroform in a gas chamber. Dead bats were weighed in order to
report contaminant loads per individual mass and were kept at -
20 % C until extraction.
Samples were analyzed at the Laboratorio de Contaminacio !n e
Impacto Ambiental of the Instituto de Ecología, Pesquerías y Oce-
anografía del Golfo de Me !xico (EPOMEX) at the Universidad
Auto! noma de Campeche. Extraction of OCPs from bat tissues fol-
lowed Otake et al. (2008). Bat bodies were dried at 45 % C for
24e48 h, cut down in pieces, and OCPs were then extracted with
25 ml of 1:1 hexane-dichloromethane at 110 % C for 25 min in a
microwave oven (MARs-from CEM laboratories). The carcass
extract was filtered using Whatman No. 2 fine-pore paper and left
to dry. A chromatographic column packed with Florisil and sodium
sulphate was used for purification. Elutions were carried out with
20 mL hexane, 15 mL dichloromethane, and 15 mL hexane:di-
chloromethane (4:1, v/v).
A 1 ml volume of hexane was used to reconstitute the sample for
analysis by EC detection Gas Chromatography (Varian 3800), using
a 60 cm $ 0.25 mm SGE chromatographic column, mod. HT8-PCB at
370 % C. The temperature of the detector was 320 % C and ultra high
purity (UHP) nitrogen was used as the carrier. Injection was per-
formed with an auto sampler system CP8410. Quantitative data
were obtained by calculating the area under the curve with the
software Star Chromatography Workstation version 6 and the
calibration standard.
For quality assurance, a pool tissue of ten oysters was used in
triplicate in order to determine percentage of recovery. One milli-
liter of a 100 ng/mL pesticide mix (SUPELCO 47426-U CLP, Organ-
ochlorine Pesticide Mix) was added to the samples prior to
extraction and subsequently refrigerated for 48 h. One of the sub-
samples was not spiked with the standard as a positive blank. The
contaminants were then extracted and processed in an identical
manner to the remaining samples. The percentage of recovery was
85e100%.
To identify and quantify the OCPs, a mix of standards was used:
a, b, g, dHCH; heptachlor; aldrin; heptachlor epoxide; endosulfan I;
dieldrin; p, p’-DDE; endrin; endrin cetone; endosulfan I and II;
endrin aldehyde; p, p’-DDD; endosulfan sulphate; p, p’-DDT;
metoxichlor and a chlordane (SUPELCO 47426-U CLP Organochlo-
rine Pesticide Mix). The concentration values of OCPs are presented
as families (SHCH ¼ a, b, g, dHCH; Sdrines ¼ aldrin, dieldrin, endrin
aldehyde, endrin cetone; S endosulfan ¼ endosulfan I and II,
endosulfan sulphate; SDDT ¼ p, p’-DDE, p, p’-DDD, p, p’-DDT,
Sheptachlor ¼ heptachlor, heptachlor epoxide;
Schlordane ¼ metoxichlor, a chlordane) and the results are re-
ported as mg/g wet weight. Limits of detection (LOD) were 10 mg/ml
for a, g, dHCH; heptachlor; aldrin; heptachlor epoxide; 50 mg/ml for
bHCH; endosulfan; a chlordane; p, p’ DDE; dieldrin; endrin; endrin
cetone; 100 mg/ml for endosulfan II; p, p’ DDD; p, p’ DDT; and
150 mg/ml for endrin aldehyde; endrin cetone; metoxichlor; and
endosulfan sulphate.
2.4. Data analysis
As is the norm with contaminant concentrations, the data did not
show a normal distribution and many of them were non-detects
(<LOD). Tobit regressions for left-censored data, with a lognormal
distribution for concentration, were therefore run to test for the
main and interaction effects of three factors: plant cover, season and
sex. However, since the Maximum Likelihood Estimation Method
(MLE) is very sensitive to a high proportion of non-detects and small
sample size (>50), drawing unrealistic estimated values, estimations

Table 1
Bat species captured in four riparian systems in the upper part of the La Antigua basin, Veracruz, Mexico.

Species Forested landscape (FL) Transformed landscape (TL) Total

Piedra Blanca Vega del Pixquiac Monte Grande Puente de Dios

Anoura geoffroyi
Artibeus jamaicensis
Artibeus toltecus
Carollia sowelli
Centurio senex
Choeroniscus godmani
Desmodus rotundus
Enchisthenes hartii
Glossophaga soricina
Lasiurus cinereus
Lasiurus intermedius
Mormoops megalophylla
Myotis californicus
Myotis keaysi
Pteronotus personatus
Sturnira parvidens
Sturnira hondurensis
4 2 0 0 6
0 0 7 0 7
2 0 1 1 4
5 30 1 14 50
0 1 0 0 1
0 5 0 0 5
0 2 2 0 4
0 0 1 0 1
0 10 0 1 11
1 5 1 0 7
1 0 0 0 1
0 2 1 0 3
1 0 0 0 1
4 2 0 0 6
0 0 0 1 1
1 1 0 0 2
27 107 56 36 226

Total 46 167 70 53 336

Number of species 9 11 8 5 17
 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382 377

of median and mean concentrations for each family of OCPs were
made with the semi-parametric Regression in Order Statistics (ROS)
method (Bolks et al., 2014; Helsel, 2012). All analyses were per-
formed using the NADA library of the software R, version 3.2.4 (R
Development Core Team, 2015).
2.5. Health status of bat community
The rank abundance index (proportion of individuals of each
species in the total number of animals captured) for each frugivo-
rous bat species was used to estimate bioaccumulation of OCPs by
the other frugivorous bats of the FL and TL sites, assuming a similar
rate of OCPs ingestion. Calculations were made only for those OCPs
with <50% of non-detected values (SHCH, SDDT, Sdrines). The
median concentration was used in these calculations because it
more accurately represents a central measure of the log-normal
distributed data we obtained. The median concentrations calcu-
lated for the other frugivorous species were transformed to grams
per bat using the mean body weight of all captured bats of each
species to obtain an approximation of the concentrations in a whole
individual.
3. Results
Seventeen (ten in the TL and fourteen in the FL) species formed
the bat community of the upper part of La Antigua basin that it was
possible to capture (Table 1) while six species were shared by both
landscape types. The fruit bat Sturnira hondurensis was the most
abundant species, accounting for 67% of all captures. With the
exception of three individuals, all bats yielded detectable concen-
trations (>LOD) for at least one of the groups of OCPs screened.
Most individuals tested positive for detectable concentrations of
OCPs for two groups of OCPs, while none tested positive for all six
groups of OCPs. Descriptive statistics of the observed and estimated
concentrations of the non-detects for all six of the families of OCPs
are presented in Fig. 2. With the exception of SHCH, median and
mean values were relatively low while, for all six families, there
were several outliers at high concentrations. Values of concentra-
tions of OCPs obtained for S. hondurensis from the upper part of the
La Antigua basin are compared with those recorded in other
frugivorous bat species in Table 3.
Regarding the possible association of concentrations of OCPs with
the three factors sex, season and landscape tree cover, we found no

Fig. 2. Boxplots for concentrations of six OCPs families with left-censored data estimated using the Regression in Order Statistics (ROS) method. The median is indicated by a thick
solid line and the mean by a dotted line. The box is the interquartile range and the whiskers extend 1.5 times the interquartile range beyond the box edges. Open small circles are
outliers above the minimum LOD. Note the logarithmic scale of the Y axis.
378 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382

Table 2
Summary of Tobit regression analyses on OCPs concentrations on the Sturnira hondurensis bat tissues. Only significant effects are presented. In all cases the model tested was
OCPs concentration ~ Sex þ Season þ Plant cover þ Sex:Season þ Sex:Plant cover þ Sex:Season:Plant cover, assuming a lognormal distribution of data; P is probability of
wrongly rejecting the null hypothesis of no effect.

OCPs concentration (Response variable) Number of non-detects (%) Significant main or interaction effect Deviancea P

SHCH 17 (30.4) Sex 5.43 0.020

SDrines 28 (50.0) Sex:season 4.56 0.033
SEndosulfan 44 (78.6) Season:Plant cover 4.37 0.036
SChlordane 41 (73.2) e e e
SDDT 34 (60.7) e e e
SHeptachlor 46 (82.1) e e e
a
LogLikelihood ratio test, with 1 d. f.

Table 3
Persistent Organochlorine Pesticides (OCPs) average concentrations reported for different frugivorous and nectarivorous bat species.

Author Species Main diet item Base (units) DDT HCH Heptachlor Endosulfan CHL Drines

Senthilkumar et al. (2001) Pteropus marianus Fruit Wet weight (ng/g) 24.00 58.00 e e 0.10 e
Cynopterus sphinx Fruit Wet weight (ng/g) 3.70 62.00 e e 0.20 e
Best (1973) Pteropus alecto gouldii Fruit Lipid (mg/g) 0.11 0.10 e e e e
Reindinger (1976) Leptonycteris sanborni Nectar Wet weight (mg/g) 0.13 e e e e
This study Sturnira hondurensis Fruit Wet weight (mg/g) 6.86 28.22 2.62 4.60 3.24 14.23

effect in the case of Schlordane, SDDT and Sheptachlor (Table 2). For
SHCH, the median concentration was significantly higher in male
than in female bats. For Sdrines, we found a significant interaction of
sex and climate season explained by the low concentration (<LOD) of
three females captured during the dry season (Fig. 3). For
Sendosulfan a significant interaction was found between season and
tree cover, explained by the lower median concentration of this
family in specimens captured during the wet season in the FL.
Overall, the estimated bioaccumulation of OCPs at fruit bat
community level was higher in the TL than in the FL (Fig. 4). This
bioaccumulation is mostly accounted for by S. hondurensis; bio-
accumulation of OCPs for Carollia sowelli and Artibeus toltecus was
comparable between landscapes. In the TL with lower vegetation
cover, Artibeus jamaicensis ranked second as a bioaccumulator in
spite of ranking third in abundance. This was due to the higher
body mass of this species. Four species contributed with a small
amount of total bioaccumulation in one or other of the two land-
scapes (Sturnira parvidens, Centurio senex, A. jamaicensis, and
Enchistenes hartii).
4. Discussion
Significant differences between the FL and the TL, in terms of the
OCPs bioaccumulated by S. hondurensis, were found for SHCH,
Sdrines and Sendosulfan. Previous studies have reported the bio-
accumulation of these OCPs in frugivorous bats from India
(Senthilkumar et al., 2001), and in insectivorous bats from Africa
(Stechert et al., 2014), Scotland and England (Swanepoel et al.,
1999), Mexico (Clark et al., 1995), New Mexico (Clark, 2001), New
York (Kannan et al., 2010) and Spain (Guille !n et al., 1994;
Herna!ndez et al., 1993), and in nectarivorous bats from New
Mexico and Oklahoma (Clark, 2001; Thies et al., 1996).

Fig. 3. Significant effects of: sex in SHCH concentration, the interaction of sex and season in Sdrines concentration and the interaction of season and landscape in Sendosulfan
concentration in Sturnira hondurensis bats in riparian cloud forests. Treatments are: Fem.Dry ¼ Female-dry season, Mal.Dry ¼ male-dry season, Fem.Wet ¼ female-wet season,
Mal.Wet ¼ male-wet season; Dry:FL ¼ dry season-forested landscape, Dry:TL ¼ dry season-transformed landscape, Wet:FL ¼ wet season-forested landscape, Wet:TL ¼ wet season-
transformed landscape. Boxplots and Y axis scale are as in Fig. 2.
 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382
Fig. 4. Trends in the bioaccumulation of families of OCPs (SHCH, SDDT, Sdrines) in fruit bat species in the riparian forests of two landscape types: forested, FL (upper plot) and
transformed, TL (lower plot).
Concentrations of 4 of the groups of OCPs that we quantified
(SHCH, Sdrines, SDDT and Sendosulfan) were higher in bats
captured in the riparian forest of the TL. In fact, all of the three
compounds groups with significant differences among the factor
levels, showed high concentrations in one of the sites located in TL
(Monte Grande). While there are higher amounts of organic matter
in the riparian forests of the FL (Gladyshev et al., 2011; Bartels et al.,
2012), increasing the chances of retention of OCPs in the soil, bio-
accumulated by plants and trees and ingested by bats when feeding
on contaminated fruit, our study showed this was not the case in
the sampled landscapes. One possible explanation for our finding
might be linked to the feeding sites visited by Sturnira in the TL
located in the farms and surrounding vegetation where OCPs have
been used and become trapped, thus favouring their ingestion. In
contrast, bats from FL visit mainly wild fruiting shrubs and trees
that have absorbed OCPs from the soil in lower concentrations.
The median concentrations of SHCH measured in female
S. hondurensis were lower than those for males, with the exception
of female bats from one of the TL sites (Monte Grande), where
concentrations were very high. Lower concentrations of OCPs in
female bats confirm the reports from other mammal groups (Thies
et al., 1996; Guille
!n et al., 1994; Allinson et al., 2006; Mispagel et al.,
2004). SHCH concentrations found in S. hondurensis (26.99 mg/g)
379
are an order of magnitude higher than values reported in frugivo-
rous bats from India three decades ago (Best, 1973) and four orders
of magnitude higher than frugivorous bats studied earlier this
century (Senthilkumar et al., 2001). Most of the HCH concentra-
tions we recorded were of bHCH and dHCH, while lindane was only
found in one individual.
With respect to the concentration of Sdrines, there was an
interaction between sex and season with female bats during the dry
months presenting lower concentrations than both males and fe-
males in the wet months. Data pertaining to the reproductive
condition of bats in the study sites indicate the dry season as the
period when most of the females are lactating. The lower concen-
trations in female bats may be the result of mobilization of the OCPs
when feeding their pups (Frouin et al., 2012); however, because the
number of females we trapped during the dry season was small,
this result should be examined in detail in future studies. Con-
centrations of Sdrines in S. hondurensis (13.57 mg/g) are similar to
those reported in studies of insectivorous bats in different parts of
the world during the late decade of the past century (Clark et al.,
1978, 1998; Herna !ndez et al., 1993; O'Shea et al., 2001; Stansley
et al., 2001) but one or two orders of magnitude higher than
those found in insectivorous bats studied during the early 2000s
(Allinson et al., 2006; Eidels and Whitaker, 2007). No previous
380 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382
reports are available of Sdrines in other frugivorous bat species.
In contrast to Sdrines and SHCH, the concentrations of
Sendosulfan found were higher in females than in males, but lower
than those for the other organochlorine pesticides. During the wet
season, concentrations of Sendosulfan were lower but still higher
in TL riverine systems than in FL. It has previously been reported
that differences found in bioaccumulation of OCPs may reflect a
differential use of habitat or foraging habits (Hickey et al., 2001),
with animals visiting sites far away from the sampled sites. Fruit
bats can cover long distances when commuting from their roost to
their foraging sites (reviewed by Galindo-Gonza !lez, 1998). Sturnira
hondurensis, in particular, can travel up to 1.5 km (Cortes-Delgado
and Sosa, 2014); this allows the bats to visit several microbasins
in the same night and even visit commercial fruit trees or shrubs in
nearby yards and orchards. Concentrations of 1.29 ± 0.11 mg/g and
70 mg/g of bioaccumulated Sendosulfan in frogs and rats, respec-
tively, resulted in 50% mortality of the animals (Lawrence and
Isioma, 2010; Brinati et al., 2016) but no similar information is
available for frugivorous bats. Administration of endosulfan in trace
concentrations to Artibeus lituratus, the great fruit-eating bat, had
an effect on forelimb muscle mass but no effect on breast muscle
mass (Brinati et al., 2016). In addition to its known endocrine
disruptive effect (Wade et al., 1997; Mrema et al., 2013), endosulfan
in mammals may induce neurotoxic and motor diseases that may
affect brain functions such as memory, learning and aggressiveness
(Lafuente and Pereiro, 2013). Several studies have reported its
presence in different taxonomic groups in Mexico (pigmy owl,
Arrona-Rivera et al., 2016; fish, Hinojosa-Garro et al., 2016; croco-
diles, Gonz!alez-J!
auregui et al., 2014; frogs, Valdespino et al., 2015)
and domestic animals (cows, Murga et al., 2016). In our study sites,
the presence of endosulfan was recorded in the soil of some pas-
tures and crop fields (Valdespino, unpublished results).
No difference was found in SHCH between seasons, which is
most likely related to the fact that bats are long-lived animals
(Hickey et al., 2001; Hernout et al., 2015) with consequently long
periods of bioaccumulation that cannot be seasonally differentiated
in their tissues. Differences between seasons in Sendosulfan and
Sdrines concentrations might be explained by the relatively short
time required by these contaminants for degradation (several
months according to Riedler et al., 2015).
While we did not find differences in concentrations of SDDT
between the two types of landscapes, or between sexes or seasons,
the presence of this compound in bats of the upper section of the La
Antigua basin is of interest because DDT was the first OCP for which
an endocrine disruptive effect was described. Concentrations of
SDDT found in S. hondurensis (6.86 mg/g) are lower than those re-
ported in Australian frugivorous bats during the last century (Best,
1973), but similar to those in studies of Pteropus marianus
(0.024 mg/g) and Cyanopterus sphinx (0.0002 mg/g) in the early
2000s (Senthilkumar et al., 2001). A study of two frog species of
different sizes inhabiting the same riparian systems (Valdespino
et al., 2015) showed concentrations (large size ¼ 190.49 mg/g,
small size ¼ 235.19 mg/g) that are two orders of magnitude higher
than those we found in S. hondurensis (5.412 mg/g).
It has previously been stated that top predators such as bats at
the interface of aquatic and terrestrial zones are a good model with
which to understand the impact of water quality on higher trophic
levels (Ballinger and Lake, 2006; Baxter et al., 2004). By calculating
the potential bioaccumulation of the other bat species, captured but
not sacrificed, using the concentrations registered in S. hondurensis,
we have attempted to overcome the economic limitations of
expensive analyses of OCPs as well as the ecological impact of
sacrificing the less abundant species. Of the species capture,
S. hondurensis represents 58 (FL) e 80 (TL) % of the bat community
(frugivorous and insectivorous bats), depending on the riparian
system, and therefore most of the contaminants are being main-
tained in the system by this species. This proportion of frugivorous
vs. insectivorous bats in bat communities has previously been re-
ported for insectivorous bats, showing a higher diversity in
conserved habitats and the ability of the frugivorous bats to exploit
resources in secondary vegetation (Cisneros et al., 2015). However,
due to their body weight, some of the concentrations might be
higher than we calculated in the other, less abundant species such
as Artibeus jamaicensis and A. toltecus, because the daily con-
sumption of fruits with potential OCPs would be higher. Finding
OCPs in a common frugivorous bat is a warning about the extent to
which bioaccumulation of pesticides can permeate trophic nets,
considering that more than 50% of the Sturnira diet is based on wild
fruit belonging to the Solanaceae and Piperaceae plant families
(Fleming, 1986; Sanchez and Dos Santos, 2015). Since some studies
show the potential occurrence of resource partitioning (Aguiar and
Marinho-Filho, 2007) among bat species of frugivorous guilds, our
estimates of the total quantities of OCPs that persist in each riparian
system should be treated with some caution. Nevertheless, they do
represent a current and reasonable approximation of the potential
risk that could be facing the species that were not directly studied.
Due to the relative ease of capturing fruit bats, this guild might
represent a better option for calculation of bioaccumulated con-
taminants in a given location.
Because of differences in movement and degradation rate of
OCPs, heavier pesticides (DDT, chlordane) tend to remain closer to
the place where they were originally applied, compared to Sdrines,
Sendosulfan and SHCHs that can travel long distances over a
similar period of time (Mendez et al., 2016; Smith et al., 2007). At
landscape scale, differences in concentrations between low and
high mobility OCPs could be a useful tool for diagnosing the toxi-
cological conditions of fauna. Four of the OCPs measured (both with
high or low mobility) in Sturnira showed higher concentrations in
the TL (twice the amount in the case of SHCH), which constitutes a
warning that ecological conditions in TL riparian forests are in
poorer condition, and their inhabitants may be facing chronic
stressful conditions. The concentrations we recorded are not of
toxicological concern since they do not exceed the values reported
to cause mortality in frogs and rats (Lawrence and Isioma, 2010;
Brinati et al., 2016); however they could have long-term physio-
logical effects on bats using the riverine corridor of TL, since the
bats have a long lifespan. In the afore mentioned study of
A. lituratus (Brinati et al., 2016), necropsy of the animals showed
mobilization of fatty acids from peripheral reserves, producing a
significant decrease of energy reserves and, in a similar study on
Mystacine tuberculata, application of diphacinone resulted in a
decreased immune response (Dennis and Gartrell, 2015).
5. Conclusions
In this study, we reported for the first time the presence of OCPs
in the tissues of a common Neotropical bat of tropical montane
cloud forest riparian strips. While most concentrations of these
compounds were below the LOD, some bats showed alarmingly
elevated concentrations of prohibited pesticides considering that
the main food of these animals is fruit rather than insects. For some
organochlorine compound families, concentrations depended on
sex, or on interaction among sex, season and degree of landscape
deforestation. We recommend further studies on the effect of these
factors and suggest that common fruit bats could play a useful role
as indicators of the presence and magnitude of contaminant
pesticides.
Sturnira hondurensis, the most abundant frugivorous bat species
in the sampled riverine systems allowed us to determine that there
are differences in the presence of OCPs in landscapes with
 C. Valdespino, V.J. Sosa / Chemosphere 175 (2017) 373e382
contrasting vegetation cover. Higher concentrations of SHCH,
Sdrines, SDDT and Sendosulfan were found in TL riparian forest.
Sex differences in bioaccumulated concentrations were inconsis-
tent; females showed higher concentrations of Sendosulfan while
males had Sdrines and SHCH in higher quantities. The seasonal
differences observed in concentrations of this latter compound are
probably related to its degradation rate.
Determination of the abundance rank of frugivorous bat species
in the riverine systems, and calculation of bioaccumulation of OCPs
using concentrations measured in the most abundant species,
could be used as a methodology for estimating bioaccumulation at
the community level in other regions, reducing the impact on other
less abundant and more vulnerable species.
Competing interests
We declare that we have no actual or potential financial, per-
sonal, or any other form of relationship that would constitute a
conflict of interest that could inappropriately influence, or be
perceived to influence, this research.
Acknowledgements
We thank the Consejo Nacional de Ciencia y Tecnología (CON-
ACYT) of Mexico for funding the Ciencia B!asica Project Project No.
101542: Biodiversidad y funcio !n de ecosistemas riparios en un
paisaje fragmentado. Fieldwork and euthanasia of the animals was
conducted with a permit from SEMARNAT- FAUT 0145. Rosario
Landgrave designed Fig. 1. Antonio Guille
!n kindly provided micro-
filament mist nets. Jaime Pelayo and Don Antonio Vasquez Blanco
graciously assisted with fieldwork and driving. Aldo Huerta-Pen ~a
dissected the bats prior to extraction. We thank Brenda Díaz-
C!
ardenas, Alberto Tabares and Sergio Izoteco for lab analysis per-
formed at Instituto EPOMEX. Keith MacMillan revised the English.
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