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Phthalates are ubiquitous contaminants and endocrine-disrupting chemicals that can become trapped in the cuticles of insects, including ants which were recognized as good bioindicators for such pollution. Because phthalates have been noted in developed countries and because they also have been found in the Arctic, a region isolated from direct anthropogenic influence, we hypothesized that they are widespread. So, we looked for their presence on the cuticle of ants gathered from isolated areas of the Amazonian rainforest and along an anthropogenic gradient of pollution (rainforest vs. road sides vs. cities in French Guiana). Phthalate pollution (mainly di(2-ethylhexyl) phthalate (DEHP)) was higher on ants gathered in cities and along road sides than on those collected in the pristine rainforest, indicating that it follows a human-mediated gradient of disturbance related to the use of plastics and many other products that contain phthalates in urban zones. Their presence varied with the ant species; the cuticle of Solenopsis saevissima traps higher amount of phthalates than that of compared species. However, the presence of phthalates in isolated areas of pristine rainforests suggests that they are associated both with atmospheric particles and in gaseous form and are transported over long distances by wind, resulting in a worldwide diffusion. These findings suggest that there is no such thing as a “pristine” zone.
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SHORT RESEARCH AND DISCUSSION ARTICLE
Phthalate pollution in an Amazonian rainforest
Alain Lenoir
1
&Raphaël Boulay
1
&Alain Dejean
2,3
&Axel Touchard
3
&
Virginie Cuvillier-Hot
4
Received: 7 March 2016 /Accepted: 23 June 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract Phthalates are ubiquitous contaminants and
endocrine-disrupting chemicals that can become trapped in
the cuticles of insects, including ants which were recognized
as good bioindicators for such pollution. Because phthalates
have been noted in developed countries and because they also
have been found in the Arctic, a region isolated from direct
anthropogenic influence, we hypothesized that they are wide-
spread. So, we looked for their presence on the cuticle of ants
gathered from isolated areas of the Amazonian rainforest and
along an anthropogenic gradient of pollution (rainforest vs.
road sides vs. cities in French Guiana). Phthalate pollution
(mainly di(2-ethylhexyl) phthalate (DEHP)) was higher on
ants gathered in cities and along road sides than on those
collected in the pristine rainforest, indicating that it follows a
human-mediated gradient of disturbance related to the use of
plastics and many other products that contain phthalates in
urban zones. Their presence varied with the ant species; the
cuticle of Solenopsis saevissima traps higher amount of
phthalates than that of compared species. However, the pres-
ence of phthalates in isolated areas of pristine rainforests sug-
gests that they are associated both with atmospheric particles
and in gaseous form and are transported over long distances
by wind, resulting in a worldwide diffusion. These findings
suggest that there is no such thing as a Bpristine^zone.
Keywords Phthalates .Pollution .Tropical rainforests .
Ants .DEHP
Introduction
Of all of the pollutants found across the globe, phthalates
(mainly di(2-ethylhexyl) phthalate (DEHP)) are some of the
most widely distributed. Phthalate esters are used in many
industrially made products, such as cosmetics, pesticide car-
riers, insect repellents, vinyl, cables, tubing, films, paints, ad-
hesives, PVC, and inks. They are also used as plasticizers (i.e.,
to make plastics more flexible). Because phthalate esters do
not chemically bind to plastic polymers, they migrate to the
surface of the polymer matrix where they may more easily
leach into the air, water, or food. They have been detected in
the air (including in aerosols), water, soil, different sediments,
Editorial Responsible: Constantini Samara
Electronic supplementary material The online version of this article
(doi:10.1007/s11356-016-7141-z) contains supplementary material,
which is available to authorized users.
*Alain Lenoir
alain.lenoir@univ-tours.fr
Raphaël Boulay
raphael.boulay@univ-tours.fr
Alain Dejean
Alain.dejean@wanadoo.fr
Axel Touchard
t.axel@hotmail.fr
Virginie Cuvillier-Hot
virginie.cuvillier@univ-lille1.fr
1
IRBI, Institut de Recherche sur la Biologie de lInsecte, CNRS UMR
7261, Université de Tours, Faculté des Sciences, Parc de Grandmont,
37200 Tours, France
2
Ecolab, Université de Toulouse, CNRS, INPT, UPS,
Toulouse, France
3
CNRS, UMR EcoFoG, AgroParisTech, Cirad, INRA, Université des
Antilles, Université de Guyane, 97310 Kourou, France
4
CNRS; UMR 8198, Unité Évolution, Écologie et Paléontologie,
Université de Lille, Lille, France
Environ Sci Pollut Res
DOI 10.1007/s11356-016-7141-z
and animal tissue, including that of humans (Teil et al. 2006;
Alves et al. 2007; Babich and Osterhout 2010; Williams et al.
2010;Gaudinetal.2011; Salapasidou et al. 2011;Choietal.
2012; Huang et al. 2013).
Hundreds of scientific papers and many newspaper articles
have chronicled the effects of endocrine-disrupting chemicals
(EDCs, mainlyphthalates, and bisphenol A), which have been
associated with human pathologies (e.g., negative effects on
the male reproductive tract, breast and testicular cancers, dis-
ruption of the neuroendocrine system, allergies, and asthma)
(Saillenfait and Laudet-Hesbert 2005a,b; Desdoits-
Lethimonier et al. 2012; Manzetti et al. 2014). Moreover, we
know that the toxicity of certain pollutants is greater than
previously thought and frequently results in transgenerational
effects (e.g., in fish; Schwindt et al. 2014). Furthermore, the
impact can be exacerbated by interactions between contami-
nants or Bcocktail effects^(e.g., pesticide combinations on
bees) (Vidau et al. 2011;Gilletal.2012) or between contam-
inants and natural stressors, including malnutrition, osmotic
perturbations, and global warming (Rhind 2009; Holmstrup
et al. 2010).
Phthalate air pollution has both acute and chronic effects
ranging from minor upper respiratory irritations to chronic
respiratory and heart diseases, lung cancer, acute respiratory
infections in children, and chronic bronchitis in adults. In ad-
dition, short- and long-term exposure to phthalate pollution
has also been linked to premature mortality and reduced life
expectancy (Kampa and Castanas 2008) and transgenerational
effects through epigenetic mechanisms (Doyle et al. 2013;
Manikkam et al. 2013; Rissman and Adli 2014). Many reports
have indicated that the phthalates found in dust in houses are
associated with asthma and allergies in both children and
adults (Ait Bamai et al. 2014).
Phthalates have been found on insect cuticles such as those
of ants, crickets, and honey bees, something which has been
taken as evidence of their ubiquity (Cavill and Houghton
1974;Katheretal.2011; Lenoir et al. 2012); they can also
become trapped in the wax of honey bee combs (Gómez-
Ramos et al. 2016). DEHP and dibutyl phthalate (DBP) are
toxic at high doses for Folsomia candida springtails, causing
modifications in symmetry (Jensen et al. 2001; Kristensen
et al. 2004). Phthalates deposited in large quantities on
Lasius niger ant cuticle remained in dead, control individuals,
while they were adsorbed and metabolized in less than 5 days
and so returned to their basic level, in live individuals (Lenoir
et al. 2014). At doses corresponding to chronic exposure
levels, phthalates reduce ant queen fecundity and stimulate
an immune response in workers (Cuvillier-Hot et al. 2014).
Because phthalates are transported everywhere in the atmo-
sphere above developed countries (Choi et al. 2012;
Blanchard et al. 2013) and because they have been found in
theArctic(Xieetal.2007), a region isolated from direct an-
thropogenic influences, they appear to be widespread. To
verify this, we hypothesized that their presence in isolated
pristine Amazonian rainforests would provide strongevidence
that the planets atmosphere is thoroughly polluted by these
compounds.
Ants are present everywhere, are found in almost every part
of the food web, and constitute the most abundant animal
taxon in tropical ecosystems (Longino et al. 2014; see also
Basset et al. 2015 for tropical insect diversity).
Consequently, ants represent important bioindicators based
on the degree to which they have been contaminated by pol-
lution. So, we compared the phthalate pollution levels of ants
from isolated pristine rainforest in French Guiana, far from
any human activity, with areas having increasing levels of
anthropogenic perturbation, including urban areas, where
plastics and many products containing phthalates (e.g., deter-
gents, building materials, and furniture) are in constant use.
However, because phthalates are rapidly degraded by micro-
bial activity and abiotic processes (i.e., hydrolysis, photocata-
lytic oxidation, and photolysis) (Staples et al. 1997;Zhouetal.
2005; Yuan et al. 2010; Huang et al. 2013; Manzetti et al.
2014), the levels recorded are likely much lower than those
associated with the original source of contamination. We also
aimed to identify the various phthalates present because, due
to concerns over their safety, the most frequently used (i.e.,
DBP, diisobutyl phthalate (DiBP), and DEHP) are progres-
sively replaced by heavier molecules, which have already
been found in soft plastics produced in Asia (Barušićet al.
2015; AL, personal observation).
Materials and methods
We collected ants from various sites in French Guiana in
November 2013 (Fig. 1). The CNRS Nouragues research sta-
tion (40° 05N, 52° 40W, 121 m asl) was an important
sampling location in our study because it is situated in an
isolated, uninhabited, and protected area 90 km from the
coast and can be reached only by helicopter (or by pirogue
then a 4-h hike). We collected ants near the station, where
human activity may have served as a source of pollution
(i.e., different materials have been used to construct shelters,
and plastic has been brought in as a result of the provision of
food and research materialssee Suppl. 1). We also collected
ants in the rainforest far from the station and on the summit
(397 m) of the inselberg near the station (see Suppl. 2).
Exposed to the elements, it harbors sparse vegetation. We also
sampled ants near the Petit-Saut hydroelectric dam (4° 59N,
53° 08W) as well as in the forest of Crique Plomb, including
the dirt road which crisscrosses the forest over 10 km from the
road leading to the dam from Route N° 1, and in other forested
areas along this road. We also collected ants in and near the
cities of Sinnamary (5° 22N; 52° 57W), Kourou (5° 09N;
52° 38W), and Cayenne (4° 56N; 52° 20W).
Environ Sci Pollut Res
Ants were captured with metal forceps and placed di-
rectly into glass vials containing hexane; they were never
in contact with plastics and were left in the vials until the
analyses were run. At that point, they were removed from
the vials, and the solvent evaporated. Then, the extract
was redissolved in 10 μLofhexanetowhich2μLof
hexane containing 400 ng of eicosane (C20) was added as
an internal standard (we verified that all the hexane used
was phthalate free). We injected 2 μL of each redissolved
extract into a Perkin-Meyer gas chromatograph-mass spec-
trometer (GC-MS) functioning at 70 eV and with a source
temperature of 230 °C. The GC-MS was equipped with a
ZB-5HT column (30-m L×0.25-mmID×0.252μmdf;
5 % phenyl95 % dimethylpolysiloxane). The following
temperature program was used: 2 min at 80 °C, increased
by 10 °C/min to reach 320 °C, and a 10-min hold at
320 °C (for a total of 36 min). An external mixture of
phthalates is generally used to quantify phthalate acid es-
ters (PAEs) (Teil et al. 2006). Eicosane is frequently used
as the standard in hydrocarbon analyses, so we utilized it
here to compare this study with previous ones (Lenoir
et al. 2012,2014; Cuvillier-Hot et al. 2014). We used ion
149, typical of phthalates, as the basis for our analyses of
the phthalate peaks (Cao 2008; Valton et al. 2014; Barušić
et al. 2015). This method is less sensitive but much more
effective in differentiating phthalates from other hydrocar-
bons, particularly DEHP from 5MeC25 (Lenoir et al. 2014).
We calculated the quantity of each compound relative to the
eicosane internal standard. The threshold for DEHP
quantification is 0.20 ng, so that, for small ants, we placed
five workers in the extract vial. We analyzed a total of
243 samples.
Since the species ranged in size, the results were normal-
ized and presented in terms of nanogram per milligram of dry
weight (DW), as in Lenoir et al. (2014).
Data are presented as means ± standard errors (SE), and
statistical analyses were conducted using ANOVAs and the
Newman-Keuls post hoc test for multiple comparisons (R
software).
Results and discussion
The different phthalates recorded
Guianese ants were contaminated with the same phthalates as
their European and North African counterparts (Lenoir et al.
2012), notably DEHP, DBP, diisobutyl phthalate (DiBP), and
benzyl butyl phthalate (BBP). DEHP, ubiquitous and noted in
95 % of the samples (Table 1), was found in higher quantities
on Solenopsis (19.5 ng/mg DW vs. 0.9 for other ants) and
accounted for 97 and 61.5 % of the phthalates found on
Solenopsis saevissima workers and other ants, respectively.
DEHP is also the most prevalent phthalate in the atmosphere
in the Paris region (Teil et al. 2016).
We also found on Guianese ant cuticules two new
phthalates, di(2-ethylhexyl) terephthalate ((DEHTP) =
dioctylterephthalate (DOTP)) and diisononyl phthalate 35
Fig. 1 Main ant sampling
locations. Map created using
Google Earth. A transect was
established along the road
between the Petit-Saut Dam and
the city of Sinnamary. Other main
places are Nouragues field
station, Kourou, and Cayenne
cities
Environ Sci Pollut Res
isomers (DINP), which are recently being used instead of
DEHP (Rastogi 1998; Abe et al. 2012). DEHTP can be pas-
sively transferred by simple contact between ants and frag-
ments of plastic childrens toys (A. Lenoir, unpublished re-
sults), explaining why it occurred on urban Guianese ants.
DINP was detected in 22.7 % of Solenopsis and 31.8 % of
other ants gathered around the Nouragues research station and
in the cities of Cayenne (at the harbor), Kourou, and
Sinnamary; it was also noted at the Petit-Saut field station
and along the road to the dam. When present, DINP only
represented 1 to 2 % of the phthalates. In the Nouragues re-
search station, it was recorded in the pieces of flagging tape
tied around trees to delimit parcels. DINP is found in toys,
childcare products, PVC, flagging tape, and many soft plastics
(Barušićet al. 2015). Its metabolites have been detected in
human urine across the globe (Saravanabhavan 2012), and
although it seems to be less toxic than the more common
phthalates (Babich and Osterhout 2010), it was placed on
Californias official list of carcinogens (Tomar et al. 2013).
The plastic tubing used to delimit parcels at the Nouragues
research station contains BBP and DEHP in small quantities,
likely explaining their presence on ants. However, these com-
pounds were also noted on ants gathered far from any human
activity, such as the top of the inselberg.
Anthropogenic gradient of pollution
Classically, phthalate pollution levels increased from the
rainforest to the cities regardless of the ant taxa tested, showing
a relationship with human activity (Fig. 2). An ANOVA using
Table 1 Different phthalates
found on ants in French Guiana
for Solenopsis and all other ant
species (mean ng/mg DW ± SE,
% of samples containing
phthalates, % quantities related to
the total amount of phthalates)
Phthalates (ng/mg DW) Other species Solenopsis
Mean SE % Samples % Total Mean SE % Samples % Total
DBP 0.1 0.0 45.5 6.4 0.1 0.1 13.4 0.6
DiBP 0.04 0.0 25.5 2.9 0.01 0 12.4 0.1
BBP 0.4 0.1 39.1 27.6 0 0 0 0
DEHP 0.9 0.2 94.5 61.5 19.5 3.6 93.8 97.4
DINP 0.02 0 31.8 1.5 0.4 0.1 22.7 1.9
DEHTP 0.001 0.0 0.9 0.1 0 0 0 0
Total 1.4 100 20.0 100
n= 110 97
0
5
10
15
20
25
30
35
Forest (149) Road (16) City (64)
ng.mg-1
a
b
b
Fig. 2 Mean phthalate levels
pooled from the cuticles of the
different ant genera. Comparison
between individuals gathered
from the rainforest, along the
roads, and in the cities (mean ng/
mg DW ± SE). Statistical
comparisons: ANOVA
(F= 24.31; df 2; p< 0.0001) and
Newman-Keuls post hoc test;
different letters indicate
significant differences at
p<0.001
Environ Sci Pollut Res
0
10
20
30
40
50
60
70
80
Forest (49) Road (33) City (11)
ng.mg-1
a
b
c
Fig. 3 Mean phthalate levels for
the different ant genera in the
different areas along the road
from the Petit-Saut dam tothecity
of Sinnamary (mean ng/mg
DW ± SE). Statistical
comparisons: ANOVA (F=45.3;
df =2;p< 0.0001) and Newman-
Keuls post hoc test; different
letters indicate significant
differences at p<0.001
0
5
10
15
20
25
30
35
Gigantiops (12)
Atta (20)
Paraponera (4)
Eciton (5)
Azteca (1)
Pachycondyla (6)
Cephalotes (1)
Odontomachus (21)
Pheidole (5)
Ectatomma (13)
Dolichoderus (4)
Camponotus (73)
Dorymyrmex (10)
Solenopsis (68)
ng.mg-1
Fig. 4 Overall mean phthalate
levels for the different ant genera
(mean ng/mg DW ± SE).
Statistical comparisons: ANOVA
(F=6.576;df =14;p< 0.0001)
Environ Sci Pollut Res
the full data set revealed that phthalate levels, which
ranged from 0 to 200 ng/mg DW, differed significantly
across ant genus (F=6.57,df =14,p<001),areas
(i.e., rainforests vs. roads vs. cities, F=32.03,df =2,p<001),
but not with altitude (F=1.47,df =1,p= 0.226). Overall,
phthalate levels were significantly higher in urban areas
(p< 0.001) and there was an increase, albeit non-significant,
from road sides to cities (p= 0.45; Fig. 2). The same trend was
noted for the data from ants sampled in the rainforest of Petit-
Saut, along the road leading to the dam, and in the city of
Sinnamary (ANOVA (F=45.3;df =2;p< 0.0001); here, all
of the differences between areas were significant (Fig. 3ac).
The cuticular phthalate levels observed for urban Guianese
ants are similar to those noted for the ant L. niger in Europe
(i.e., 2 ng/ant fresh weight, corresponding to 5 ng/mg DW)
(Lenoir et al. 2012). Yet, a perfect comparison would require
using the same species.
Phthalates were ubiquitous around the Nouragues research
station, as they were found in ants from the camp, the forest,
and the top of the inselberg.The levels were low, ranging from
0.5 (the top of the inselberg) to 2 ng/mg DW, and did not differ
significantly between sites (p=0.06,butnearsignificancefor
the top of the inselberg, p= 0.055), so that human activity in
and around the station is not likely responsible for the phthal-
ate pollution noted deep in the rainforest and on the top of the
inselberg.
Therefore, our hypothesis that phthalate pollution is glob-
ally ubiquitous is likely confirmed as, in addition to their pres-
ence in the Arctic (Xie et al. 2007), we found them in other
areas isolated from direct anthropogenic influence, including
parts of the Amazonian rainforest and the top of an inselberg.
These results strongly suggest that contaminants arrive from
the atmosphere both with air particles and in gaseous form
(see Blanchard et al. 2014; Cecinato et al. 2012; Gao and
Wen 2016;Teiletal.2016; Xie et al. 2005). For example, in
the Paris region, phthalate pollution ranges from 10 to
100 ng m
3
of total air and 80 % in the gaseous phase. It is
more concentrated in urban areas compared to forest sites (Teil
et al. 2016).
Variation in phthalate levels across ant genera
The levels of phthalate contamination varied between ant gen-
era (Fig. 4), a pattern likely due to differences in cuticle com-
position (Vienne et al. 1995). S. saevissima had the highest
levels but was not found at the Nouragues research station nor
the rainforest (see Dejean etal. 2015). Yet, it did occur at all of
the other sites, including along the dirt road of Crique Plomb
which crisscrosses the rainforest at Petit-Saut. Phthalate levels
noted on workers were low in the latter case and high in the
cities with values of up to 180 ng/mg DW. Consequently, with
its anthills interconnected by galleries forming huge colonies
extending along several kilometers (Martin et al. 2011; Lenoir
et al. 2016), S. saevissima appears to be a good bioindicator
for gauging phthalate pollution in human-disturbed areas.
In conclusion, it appears that phthalates are universal con-
taminants and are probably major constituents of generalized
anthropogenic pollution, which is a leading cause of human
health problems. They may also be playing a role in the mass
extinctions of the Anthropocene, which are affecting both ver-
tebrate and, albeit less visibly, invertebrates (Dirzo et al.
2014). Phthalates are the major pollutants disseminated
throughout the world in gaseous form and on atmosphere
particles (Teil et al. 2016). Our results show that they are
found in different levels on ant cuticle based on a gradient of
urbanization, so ants can be considered good bioindicators
due to their ubiquity and ease of sampling them. It is thus
imperative to continue to study the pollution of ant popula-
tions, most particularly in tropical rainforests.
Acknowledgments Financial support for this study was provided by a
CNRS/Centre dÉtudes de la Biodiversité Amazonienne (CEBA) project
entitled BPhthalate pollution in an Amazonian rainforest^(PPAR). We are
grateful to Chloé Fasilleau and Chloé Moyse (École Polytechnique,
Université de Tours, France) for the analysis of the data, to Jessica
Pearce-Duvet and Andrea Yockey-Dejean for proofreading the manu-
script, and to Jacques H. C. Delabie (Laboratório de Mirmecologia,
CRC, Ilhéus, Bahia, Brazil) for the identification of the ants. We would
like to thank the staff of the CNRS Nouragues research station and the
Laboratoire Environnement de Petit-Saut for furnishing logistical assis-
tance.
Compliance with ethical standards
Conflict of interest The authors declare that they have no competing
interest.
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