Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons:...

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Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico Rosa María Flores-Serrano a, , Rosario Iturbe-Argüelles a , Guillermina Pérez-Casimiro a , Adriana Ramírez-González a , José Salvador Flores-Guido b , Jesús Martín Kantún-Balam b a Instituto de Ingeniería, Universidad Nacional Autónoma de México, Edicio 5, Apdo. Postal 70472, Col. Ciudad Universitaria, Delegación Coyoacán, C.P. 04510 México D.F., Mexico b Licenciatura en Biología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil Km. 15.5 Apdo. Postal 4116 Itzimná, C.P. 97100 Mérida, Yucatán, Mexico HIGHLIGHTS An ecological risk assessment was performed using the hazard quotient (HQ) method. HQs were obtained for omnivorous mammals exposed to polycyclic aromatic hydrocarbons. Risks for the oral exposure route were less than benchmarks in all cases (HQ b 1). More research must be done in Mexico aimed primarily at obtaining TRVs for mammals abstract article info Article history: Received 14 September 2013 Received in revised form 18 December 2013 Accepted 18 December 2013 Available online xxxx Keywords: Hazard quotient Omnivorous mammals Polycyclic aromatic hydrocarbons Ecological risk assessment Mexico An ecological risk assessment (ERA) was performed using the hazard quotient (HQ) method to evaluate the risks of oral exposure to polycyclic aromatic hydrocarbons (PAHs) for medium sized omnivorous mammals. This is the rst in a series of three papers. In Mexico there is little experience in performing this kind of assessment for the terrestrial compartment, in particular for birds and mammals exposed to hydrocarbons. The purpose of this paper is to perform an ERA and to establish if the omnivorous mammalian species living in the area are at risk of adverse effects. The studied site is a land that in past years had been used for the disposition of petroleum tank bottom sludges, and scrap metals. Soil and water samples were collected and analyzed, and we obtained a list of the site's wildlife species as well as samples of the specimens, which were analyzed also. HQs were calculated for the hydrocarbons identied as chemicals of potential ecological concern (COPECs) and the omnivorous mammals of the site were evaluated. Toxicity reference values (TRVs) were taken from the appropriate literature, and the doses of exposure were esti- mated considering the ingestion of water, soil, and diet. Results indicated that potential risks associated to the oral exposure route were less than benchmarks for effects (in all cases HQ b 1). The methodology is adequate in terms of the parameters considered in the calculations, but it was concluded that in order to reduce uncertainty, more research is required in Mexico. This should be primarily aimed at obtaining TRVs for mammals, and consider test species with body weights more similar to those found in the local fauna. © 2013 Elsevier B.V. All rights reserved. 1. Introduction The application of quantitative ecological risk assessment methodol- ogies, e.g., the hazard quotient (HQ) method, for terrestrial wildlife in Mexico has a short history. Ecotoxicological studies have primarily focused on the effect of metals, pesticides and, to a lesser extent, hydro- carbons in the aquatic environment; cladocerans, algae, and oysters are the most popular organisms studied (Bernal-Hernandez et al., 2010; Carvalho et al., 2009). Ecotoxicological studies focused on soil microor- ganisms and macrofauna, mainly earthworms, have been performed with certain regularity (Espinosa-Reyes et al., 2010; Hernández- Hernández et al., 2007). Most investigations address the issue of the health of organisms by measuring both effects and exposure biomarkers, or concentrations of contaminants in the tissues, but they do not indicate if the concentra- tions in the natural media pose a risk to organisms of upper trophic levels and the magnitude of the risk. Organisms in the upper trophic levels, e.g., herbivorous, carnivorous, or omnivorous vertebrates, are rarely chosen as ecological receptors for assessment and, as a conse- quence, terrestrial risk assessments are almost non-existent in Mexico. Some studies have focused on the study of biomarkers in rodents, reptiles, and birds (Ilizaliturri-Hernández et al., 2008; Tovar-Sánchez et al., 2012) or on measuring residual concentrations of contaminants in tissues, mainly organochlorine substances (Pardío et al., 2012; Science of the Total Environment 476477 (2014) 218227 Corresponding author. Tel.: +52 55 56233600x8653; fax: +52 55 56162164. E-mail address: [email protected] (R.M. Flores-Serrano). 0048-9697/$ see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scitotenv.2013.12.092 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Transcript of Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons:...

Page 1: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Science of the Total Environment 476–477 (2014) 218–227

Contents lists available at ScienceDirect

Science of the Total Environment

j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv

Ecological risk assessment for small omnivorous mammals exposed topolycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Rosa María Flores-Serrano a,⁎, Rosario Iturbe-Argüelles a, Guillermina Pérez-Casimiro a,Adriana Ramírez-González a, José Salvador Flores-Guido b, Jesús Martín Kantún-Balam b

a Instituto de Ingeniería, Universidad Nacional Autónoma de México, Edificio 5, Apdo. Postal 70–472, Col. Ciudad Universitaria, Delegación Coyoacán, C.P. 04510 México D.F., Mexicob Licenciatura en Biología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, CarreteraMérida-Xmatkuil Km. 15.5 Apdo. Postal 4–116 Itzimná, C.P. 97100Mérida,Yucatán, Mexico

H I G H L I G H T S

• An ecological risk assessment was performed using the hazard quotient (HQ) method.• HQs were obtained for omnivorous mammals exposed to polycyclic aromatic hydrocarbons.• Risks for the oral exposure route were less than benchmarks in all cases (HQ b 1).• More research must be done in Mexico aimed primarily at obtaining TRVs for mammals

⁎ Corresponding author. Tel.: +52 55 56233600x8653;E-mail address: [email protected] (R.M. Flor

0048-9697/$ – see front matter © 2013 Elsevier B.V. All rihttp://dx.doi.org/10.1016/j.scitotenv.2013.12.092

a b s t r a c t

a r t i c l e i n f o

Article history:Received 14 September 2013Received in revised form 18 December 2013Accepted 18 December 2013Available online xxxx

Keywords:Hazard quotientOmnivorous mammalsPolycyclic aromatic hydrocarbonsEcological risk assessmentMexico

An ecological risk assessment (ERA)was performed using the hazard quotient (HQ)method to evaluate the risks oforal exposure to polycyclic aromatic hydrocarbons (PAHs) formedium sized omnivorousmammals. This is the firstin a series of three papers. InMexico there is little experience in performing this kind of assessment for the terrestrialcompartment, in particular for birds andmammals exposed to hydrocarbons. Thepurpose of this paper is to performan ERA and to establish if the omnivorous mammalian species living in the area are at risk of adverse effects. Thestudied site is a land that in past years had been used for the disposition of petroleum tank bottom sludges, andscrapmetals. Soil andwater sampleswere collected and analyzed, andwe obtained a list of the site's wildlife speciesaswell as samples of the specimens, whichwere analyzed also. HQswere calculated for the hydrocarbons identifiedas chemicals of potential ecological concern (COPECs) and the omnivorous mammals of the site were evaluated.Toxicity reference values (TRVs) were taken from the appropriate literature, and the doses of exposure were esti-mated considering the ingestion of water, soil, and diet. Results indicated that potential risks associated to theoral exposure route were less than benchmarks for effects (in all cases HQ b 1). The methodology is adequate interms of the parameters considered in the calculations, but it was concluded that in order to reduce uncertainty,more research is required in Mexico. This should be primarily aimed at obtaining TRVs for mammals, and considertest species with body weights more similar to those found in the local fauna.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

The application of quantitative ecological risk assessmentmethodol-ogies, e.g., the hazard quotient (HQ) method, for terrestrial wildlife inMexico has a short history. Ecotoxicological studies have primarilyfocused on the effect of metals, pesticides and, to a lesser extent, hydro-carbons in the aquatic environment; cladocerans, algae, and oysters arethe most popular organisms studied (Bernal-Hernandez et al., 2010;Carvalho et al., 2009). Ecotoxicological studies focused on soil microor-ganisms and macrofauna, mainly earthworms, have been performed

fax: +52 55 56162164.es-Serrano).

ghts reserved.

with certain regularity (Espinosa-Reyes et al., 2010; Hernández-Hernández et al., 2007).

Most investigations address the issue of the health of organisms bymeasuring both effects and exposure biomarkers, or concentrations ofcontaminants in the tissues, but they do not indicate if the concentra-tions in the natural media pose a risk to organisms of upper trophiclevels and the magnitude of the risk. Organisms in the upper trophiclevels, e.g., herbivorous, carnivorous, or omnivorous vertebrates, arerarely chosen as ecological receptors for assessment and, as a conse-quence, terrestrial risk assessments are almost non-existent in Mexico.Some studies have focused on the study of biomarkers in rodents,reptiles, and birds (Ilizaliturri-Hernández et al., 2008; Tovar-Sánchezet al., 2012) or on measuring residual concentrations of contaminantsin tissues, mainly organochlorine substances (Pardío et al., 2012;

Page 2: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Surface waterrun-off

SHM

Surface soil

SOMHB HROB I/L

Soil solution

P

Air

Air sources (chimneys)

Petroleum tank bottom sludges, and scrap metals

CB IRIB

Fig. 1. Conceptual model. Rectangles with heavy borders represent receptors thatare assessment endpoints and dashed lines represent exposure routes present at thesite but that were not assessed. CB = Carnivorous birds, IB = Insectivorous birds, HB =Herbivorous birds, OB = Omnivorous birds, SHM = Small herbivorous mammals,SOM = Small omnivorous mammals, HR = Herbivorous reptiles, IR = Insectivorousreptiles, IL = Invertebrates/Larvae, P = Plants.

219R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

Ruelas-Inzunza et al., 2007), but in these investigations no risk values orclean-up concentrations have been proposed. Sometimes vertebratesare not considered as assessment targets since their populations fre-quently have much larger home ranges than the area of contaminatedsites, so it is expected that the effects may be diluted over the range ofthe population (Suter, 1997). Nevertheless, this is not a valid reason to ex-clude this group of organisms from assessments, since biomagnificationmay be important in food chains, leading to potentially high levels of ex-posure in wildlife that feed on organisms from lower trophic levels.

The purpose of this paper is to perform an ERA and to establish if theomnivorous mammalian species living in the area are at risk of adverseeffects. This is the first in a series of three papers. The HQ method isapplied to estimate the risk of exposure to polycyclic aromatic hydro-carbons (PAHs) formammals found in a vegetated area close to a petro-leum facility. Since no previous studies of this kind exist in Mexico, asecondary objective is to identify future lines of research that wouldneed to be strengthened to attain better results.

TheHQmethod is a technique developed for performing risk estima-tions. It is defined as the ratio of estimated level of exposure of variousenvironmental receptors to appropriate toxicity reference values(TRVs):

HQ ¼ Concentration or dose of exposureð Þ=TRV ð1Þ

In this work, only the oral pathway was considered, so the HQ isexpressed as follows:

HQ ¼ Doseoralð Þ=TRV ð2Þ

TRVs are usually derived from review of published toxicity studies,and identify concentration values or dose values that correspond to ano-observed adverse effect level (NOAEL) and/or a lowest observed ad-verse effect level (LOAEL). Each TRV is both chemical-specific andspecies-specific (USEPA, 2008).

In this study, HQs for the oral route were computed for five mediumsized omnivorous mammals to evaluate the risks from exposure toPAHs. They are present in petroleum products and they were chosenas contaminants of concern for this site because they are known tocause adverse health effects, including cancer and reproductive effectsin animals (Chung et al., 2011). They are moderately toxic and persis-tent and can accumulate to hazardous levels at locations where heavyfractions of petroleum have been deposited (Suter, 1997).

2. Material and methods

2.1. Study area

Thefieldwork for the ERAwas conducted in a vegetated area locatedwithin a petroleum facility located in northeastern Mexico. Distillationprocesses took place at this facility, producing gasoline, intermediatedistillates (turbosine and diesel), combustoleum, carbon black, avgas,LP gas, coke, sulfur, and asphalt that were stored in facility tanks. Thevegetated area, where the research was conducted, is located in thenorthwestern side of the facility covering a surface of 21 ha. For the pur-poses of this research, this area was named Study Area. Before the year2000, residual sludge from oil storage tanks was disposed directly ontothe soil, as well as in a dumping area located in the western border ofthis location. For comparison purposes, a Background Area was chosen.The Background Area was considered to be representative of sites notaffected by the disposal of residual sludges; this site had an extensionof 17 ha and was located at the East of the facility, it was verified thatno oil sludges were present and that the vegetation was similar to thatof the Study Area.

Both sites are located on alluvial sandy soil. The geology of the areaconsists of two sedimentary basins with Tertiary rocks mainly formedby shales and sandstones. The climate is warm and semi-humid with

rains in the summer. Annual mean precipitation and temperature are927.8 mm and 24.2 °C, respectively. No groundwater wells are presentin the Study Area but, according to the literature, the region has aquiferswith static levels that vary between 3 and 80 m. The groundwater gen-erally moves in the direction of the superficial streams, which run fromWest to East. The stratigraphy of the area is composed of clayey silt withlow content of organic matter (0–0.30 m), silty sand or sandy silt(0.30–2.80 m), and sand with small-sized gravel and shell fragments(2.8–22.8 m). During soil sampling activities, in some of the areasthere were sand or silty sand deposits in the first 0.40 m; this materialwas used to cover bottom tank sludges that were disposed on thesite. Soil pH was measured in the field considering a 1:1 soil:water(distilled) ratio. The measurement was made using pH paper and hada value of 6.

2.2. Problem formulation

In this stage of the assessment, site visits weremade to gather infor-mation about sources of contamination, contaminants of potential con-cern and their concentrations, and additional information used todevelop a conceptual model (e.g., biota present at the site).

2.2.1. Soil and water sampling and analysisFor soil characterization 64 samples were obtained; 32 samples

were taken from 0.00 to 0.05 m depth and 32 samples were takenfrom 0.20 to 0.40 mdepth. A grid of 100 × 100 mwas followed and po-sitions were recorded with a Garmin Etrex GPS. Due to financial re-source restrictions, only five random soil samples were gathered inthe Background Area.

Sampleswere collected in stainless steel tubes that were sealed aftercollection and preserved at 4 °C until analysis. Samples were analyzedfor TPHs, PAHs, and BTEX (benzene, toluene, ethylbenzene, and xy-lenes), as defined by the Mexican standard NOM-EM-138-ECOL-2002(DOF, 2002) that was in force at the time of the study. For PAHs,NOM-EM-138 only considers six of these compounds, but, for thisstudy, we included the 16 priority PAHs established by USEPA. For theanalysis, the following methods were used: EPA-8310 for PAHs, EPA-8260 for BTEX, and EPA-418.1 for TPHs, as indicated by the standardmentioned before. Table 1 summarizes the PAHs and TPHs contentfound at the upper soil layer.

Since the assessment endpoints were terrestrial organisms presentat the site, surface water sources were sought. Five water samples

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220 R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

were collected frompuddles locatedwithin the StudyArea, four of themwere obtained inside the dumping site and one outside of it; due to thehigh permeability of the soil, the latter was obtained right after a rainevent. Preferencewas given to the areawithin the dumping site becausemany animal tracks were found near the puddles of this area. Sampleswere collected in amber jars (4-L capacity) and frozen until their analy-sis. Hydrocarbons (PAHs) were extracted in the laboratory using highpurity hexane. The analysis was performed by column chromatography(gas chromatography, flame ionization detection for quantitation; de-tection level of 0.00001 mg/L for all PAHs). Table 1 shows the concen-trations; as observed only two PAHs among the 16 PAHs analyzedwere present inwater samples at concentrations above analytical detec-tion levels.

Table 1 summarizes the PAHs and TPHs content found at the uppersoil layer. As was expected, due to its high volatility, BTEX concen-trations were below analytical detection levels and are not shown inthis table. The statistical parameters shown in Table 1 were calculatedusing concentrations different from non-detected levels, because theusual convention of considering one half of the level of detection result-ed in very low values that were not representative of the site. Hence, forassessment purposes, the geometric mean of the sampling points withconcentrations above the analytical detection level was used; this wasthought to be a moderate posture that would be more representativeof site conditions.

2.2.2. Chemicals of potential ecological concern (COPECs)Hydrocarbons in soil were screened against ecological screening

benchmarks (ESB) for soil to determine appropriate chemicals of poten-tial ecological concern (COPECs), as established by Suter (1996) andTNRCC (2000).

Table 2 shows the geometric mean of the ESB used for this work.The information used to generate the values shown on Table 2was obtained from the following documental sources: Efroymsonet al. (1997a,b), USEPA (1999), TNRCC (2000), RAIS (2001), and EPTI(1999).

In accordancewith TNRCC (2000) recommendation, bioaccumulablesubstances with soil concentrations above the analytical detection levelwere also classified as COPECs. PAHs were classified as bioaccumulablebased on their Kow value (octanol-water partition coefficient value,6.3E+03 b Kow b1.0E+08) (TNRCC, 2000). Table 2 depicts the Kowvalues for the PAHs considered in this study, as well as the COPECsretained for their assessment.

2.2.3. Biological characterizationThe objective of the biological characterizationwas to obtain a list of

the flora and fauna species present in the Study Area and BackgroundArea, and select the appropriate assessment endpoints. During thischaracterization, biota tissues were also collected (muscles and internalorgans) to analyze the PAH content and use these concentrations in HQcalculations. Mammal, bird, and reptile species were registered at theStudy Area by means of direct and indirect methods. For the captureof small mammals, 40 Shermann traps were used (3″ × 3.5″ × 9″ fold-ing aluminum traps) in transects of 100 m length. For medium sizedmammals, three Tomahawk traps were used (40″ × 12″ × 12″ collaps-ible traps). For the capture of bats, two four-shelved mist nets wereused; the same nets were used during daytime for the collection ofbirds. Transects were also used for the capture of reptiles and amphib-ians; sampling was made by hand using snake hooks, aerial insectnets, and occasionally an air rifle. Collected specimens were identifiedby specialists, and indirect means were used also for their identification(tracks, scats, burrows, carcasses, nests, and bird's songs). Table 3 pre-sents the list of all the species (mammals, birds, and reptiles) registeredin the Study Area.

Captured specimens were killed and tissue samples were taken(muscle, stomach, and liver) and analyzed for hydrocarbons andmetals.In some cases, samples of body fat, gonads, and brain were analyzed

also. In this study, only results concerning HAPs concentrations inmuscle tissue are presented. No tissue samples were taken in theBackground Area.

In the case of invertebrates, 11 composite samples were taken inthe Study Area (one sample each of the orders Scolopendromorpha,Blattodea, Isopoda, Hemiptera, Opiliones, and Lepidoptera, two sampleseach of the orders Orthoptera and Hymenoptera, and one sample oflarvae from unidentified organisms) (see Table 4). Organisms were col-lected by hand from soil, stems, and leaves, and for flying insects, sweepnets and light traps were used. Collected insects were washed with dis-tilled water to eliminate dust and soil, and were preserved at −4 °Cuntil analysis. It is important to mention that insects were not purgedprior to analysis.

All samples were lyophilized and analyzed following the standardoperating procedures described by UNEP/IOC/IAEA/FAO (1990) andUNEP/FAO/IAEA/IOC (1991). Quantification was performed in a gaschromatograph equipped with a flame ionization detector (FID-GC).

To obtain the list of plant species and the description of the type ofvegetation present at the Study Area and the Background Area, linetransects and quadrants were used. In some cases, specimens of plantswere collected and herborized for identification.

A total of 134 plant species were recorded in the Study Area and 66species in the Background Area. Tissue samples were also collected(leaves and stems from herbaceous plants and shrubs): seven samplesfrom the Study Area and four samples from the Background Area. Anal-yses were performed as described for animal tissue; samples werewashed with distilled water prior to analysis. Table 4 presents COPEC'sconcentrations found in plant tissue from the Study Area.

2.3. Analysis

In this work, themagnitude of the exposure (dose of exposure, DOE)was restricted to the oral pathway (Doseoral), and was calculatedconsidering the appropriate input data, e.g., bodyweight, food ingestionrates, water ingestion rates, diet composition, proportion of food types,concentration of COPECs in food items, water and soil. Appropriate TRVswere estimated also in this stage of the assessment. As seen in Eq. (2),both values, Doseoral and TRV, are used to estimate the HQ.

2.3.1. Dose of exposure (DOE)The dose of exposure considered in Eq. (2) for the oral pathway

(Doseoral) was calculated as follows (TNRCC, 2000):

Doseoral ¼EMFf

XNi¼1

PFið Þ � TFIRð Þ � Cið Þf g !

þ IRw � Cw � EMFwð Þ þ IRs � Cs � EMFsð Þ" #

BW

ð3Þwhere:

Doseoral oral dose of exposure (estimated dose from the ingestion offood, water, and soil) (mg COPEC/kg body weight/day)

EMFf exposure modifying factor for food ingestion (unitless) = 1N total number of food types in the dietPFi proportion of the i food type in the diet (equal distribution for

each type of food; e.g., if diet is composed by four types offood, then the proportion of each type is 0.25)

TFIR total food ingestion rate [kg (dry weight)/day)]Ci COPEC concentration in i food type [mg COPEC/kg of food

(dry weight)]IRw ingestion rate of water (L/day)Cw COPEC concentration in water (mg/L)EMFw exposure modifying factor for water ingestion (unitless) = 1IRs ingestion rate of soil [kg (dry weight)/day)]Cs COPEC concentration in soil [mg COPEC/kg (dry weight)]EMFs exposure modifying factor for soil ingestion (unitless) = 1BW body weight of receptor (kg)

Page 4: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

ater

(mg/L)

samples

from

theStud

yArea.

Water

ntFlu

Pyr

Ban

Cry

Bkf

Bap

Ind

Bpe

TPH

Ana

Cry

34

44

45

55

NA

24

.30E

−1

1.50

E−1

5.60

E−1

1.24

E+0

1.30

E+0

7.20

E−1

4.80

E−1

5.00

E−2

8.00

E−2

7.4E

+5

1.40

E−3

1.65

E−2

.30E

−1

1.50

E−1

5.00

E−2

5.00

E−2

6.00

E−2

1.00

E−1

1.00

E−2

5.00

E−2

8.00

E−2

2.66

E+1

5.50

E−6

5.50

E−6

ANA

2.40

E−1

6.00

E−1

5.20

E−1

4.40

E−1

3.30

E−1

NA

NA

1.41

E+5

8.04

E−4

8.73

E−3

.30E

−1

1.50

E−1

2.00

E−1

6.10

E−1

6.10

E−1

4.10

E−1

50E−

15.00

E−2

8.00

E−2

3.16

E+4

4.71

E−4

9.91

E−3

.30E

−1

1.50

E−1

1.26

E−1

3.20

E−1

3.86

E−1

2.68

E−1

6.90

E−2

5.00

E−2

8.00

E−2

5.54

E+2

3.60

E−5

1.07

E−3

232

3232

3232

3232

3232

55

14

34

22

11

323

3

e=

phen

anthrene

;Ant

=an

thracene

;Flu

=fluo

ranthe

ne;P

yr=

pyrene

;Ban

=be

nzo(a)an

thracene

;Cry

=crhy

sene

;Bkf

=be

nzo(k)fluo

ranthe

ne;B

ap=

benz

o(a)py

rene

;PH

s=

totalp

etroleum

hydroc

arbo

ns;N

BR=

numbe

rof

benz

enering

s;NA=

notap

plicab

le;M

ax=

max

imum

;Min

=minim

um;S

D=

stan

dard

deviation;

Avg

=av

erag

e;=

numbe

rof

samplingpo

ints

withco

ncen

trations

abov

eno

nde

tected

(ND)leve

ls.

from

ND;C

ontaminan

tswithNDco

ncen

trations

inallsam

plingpo

ints

areno

tsh

own.

221R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

Due to the scarcity of BWdata for the species of interest in the StudyArea, this information was obtained from zoological collections ofMexican institutions. Table 5 shows BWs of all the species registeredfor the Study Area.

It was impossible to obtain in the field the TFIRs mentionedin Eq. (3), so they were estimated by means of allometric equationsdeveloped by different authors on the basis of animal bodyweight using models derived from specific taxa or groups. Table 6shows all TFIR equations considered for the analyses for all thespecies found in the site. Table 7 summarizes information regardingthe equations used for each species (all species found in the StudyArea).

For the estimation of IRw, three sources of information were con-sidered: Calder and Braun (1983), Gibson et al. (1997), and Nagy andPeterson (1988). Table 6 presents all the IRw equations consideredfor the analysis for all the species registered for the Study Area, andTable 7 summarizes the information regarding the equations foreach species. As for TFIR, several equations suited a particular species(e.g., for rabbit S. floridanus, three equations could be used) andit was decided to perform the same statistical analysis as for TFIRequations. Results of these tests are not shown but in 17 out of 24of the species considered for the analysis significant differences(p b 0.05) were observed among all the IRw estimated with theequations used.

For the selection of the IRw equations, factors like the “kind” ofwater requirements estimated by the equations were taken intoaccount (free water, metabolic water, and preformed water), aswell as the range of body weights used in the regressions by theauthors consulted. The Nagy and Peterson equations are referredto the total flux of water (free, metabolic, and preformed water),and the Calder and Braun equations only consider free water,which is more suitable for the objectives of the present study. Therange of weights of the eutherian mammals, herbivorous eutherianmammals, and birds (general) used by Nagy and Peterson (1988)in their regressions was much larger than the average weights ofthe species of interest (11.5–429,000 g versus 41.5–5246.6 g forthe species of interest; for eutherian mammals the maximumweight used in the regressions was 81 times larger and 9 timeslarger for birds).

Regarding to soil ingestion rates (IRs), theywere estimated using theconservative values proposed by Gibson et al. (1997) as percentage ofTFIR for different groups of animals. Table 8 shows IRs for all the speciesfound in the Study Area.

With the information described above, oral doses of exposure(Doseoral) for the species of interest were calculated. Estimated valuesfor each of the five omnivorous mammals of interest are shown inTable 9 (numerator of the ratios Doseoral/TRVs presented in each rowof omnivorous mammals).

Table1

Conc

entrations

ofhy

drocarbo

nsin

soil(0

to0.05

m,m

g/kg

)an

dw

Parameter

Soil

Ace

Fen

Phe

A

NBR

22

33

Max

2.12

E+0

2.07

E+0

5.23

E+0

4Min

2.12

E+0

6.20

E−1

4.00

E−2

4SD

NA

1.03

E+0

1.94

E+0

NAvg

2.12

E+0

1.35

E+0

1.30

E+0

4GM

2.12

E+0

1.13

E+0

3.62

E−1

4NSP

3232

323

NSP

C1

27

1

Ace

=acen

aphthe

ne;A

na=

acen

aphtylen

e;Fen=

fluo

rene

;Ph

Ind=

inde

ne(1

,2,3,c,d)p

erylen

e;Bp

e=

benz

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rylene

;TGM

=ge

ometricmean;

NSP

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mbe

rof

samplingpo

ints;N

SPC

Note:

parameterswerecalculated

cons

ideringtheva

lues

diffe

rent

2.3.2. Toxicity reference values (TRVs)No observed adverse effect level (NOAEL)-based TRVs for the oral

route were used in this study. Specific NOAEL values for the Mexicanmammalian and avian wildlife species present at the Study Area arenot available; thus, for the wildlife species of interest it was necessaryto extrapolate NOAELs from laboratory test species. These extrapola-tions were achieved through the application of the equation proposedby Sample et al. (1996), which is based on body size of both testand wildlife species, as well as the allometric scaling factor (3/4 formammals).

TRVs for reproductive or lethal endpoints were preferred, in theabsence of this kind of endpoints, systemic effects that may reduce thesurvival of the species were used (e.g., hepatic effects). In cases wherechronic NOAELs for a specific chemical were not available for the labo-ratory species, uncertainty factors were used as indicated by Sampleet al. (1996).

Page 5: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Table 2ESB, Kow and soil concentrations of the contaminants found in the Study Area.

Contaminant ESB(mg/kg)

Concentrationin soil (mg/kg)

Kow(dimensionless)

Contaminant retainedfor further assessment?

Naphthalene 4.790 0.004a 2.36E+03 NoAcenaphtylene NF 0.003a 1.18E+04 NoAcenaphthene 20.000 2.120b 9.22E+03 YesFluorene 30.000 1.133b 1.47E+04 YesPhenanthrene 6.300 0.362b 3.55E+04 YesAnthracene 0.100 0.430c 2.95E+04 YesFluorantene 0.100 0.150c 1.21E+05 YesPyrene 10.000 0.126b 1.00 E+05 YesBenzo(a)anthracene 1.320 0.320b 4.77E+05 YesChrysene 0.170 0.386c 5.48E+05 YesBenzo(b)fluoranthene 1.320 0.003a 1.59E+06 NoBenzo(k)fluoranthene 1.320 0.268b 1.56E+06 YesBenzo(a)pyrene 0.270 0.069b 1.35E+06 YesIndene(1,2,3,c,d)pyrene 1.320 0.050b 8.22E+06 YesDibenzo(ah)anthracene 1.320 0.003a 3.53E+06 NoBenzo(g,h,i)perylene NF 0.080b 3.08E+06 YesTPHs NF 554.172d NF No

ESB = ecological screening benchmark (geometric mean); Kow = octanol-water partition coefficient [obtained from USEPA (1999) except for acenaphtylene, whichwas obtained fromMontgomery and Welkom (1990)]; TPHs = total petroleum hydrocarbons; NF = not found.

a Not considered for further assessment since concentration in soil is below the analytical detection level (DL/2).b Retained for further assessment since it is expected to be a bioaccumulative compound based on its Kow value.c Retained for further assessment since concentration in soil N ESB.d TPHs were not considered for further assessment since no ESB, Kow and TRV (Toxicity Reference Value) were found in the literature for Mexican mixtures of TPHs.

222 R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

3. Results and discussion

The information gathered during the analysis and problem formula-tion steps was used in Eq. (2). Table 9 presents the ratios Doseoral/TRVthat define the estimated risk values (HQ) for the mammal omnivorousspecies of interest; in all cases these ratios were below one, indicatingthat the acceptable thresholds were not exceeded and therefore there isno risk for these species. Due to the evidence of contamination found inthe Study Area and the lipophilicity of the hydrocarbons it was expectedto find high levels of risk, but this was not the case, at least for the expo-sure to PAHs. The results obtained may be due in part to the low concen-trations of PAHs (compared to TPHs) and low proportion of samplingpoints with concentrations above analytical detection levels.

Table 3Fauna species found in the Study Area.

Taxonomic Scientific name

ClassMammalia (mammals) Artibeus intermediusa

Artibeus jamaicensisa

Dasypus novemcinctusDidelphis virginianaa

Mephitis macrouraa

Procyon lotorSpilogale putoriusa

Sylvilagus floridanusAves (birds) Amazilia yucatanensisa

Columbina passerinaa

Coragyps atratusCrotophaga sulcirostrisDendrocygna autumnalisHirundo rusticaIcterus sp.a

Melanerpes aurifronsa

Myiozetetes similisPandion haliaetusPasser domesticusQuiscalus mexicanusa

Tyrannus melancholicusa

Zenaida macrouraReptilia (reptiles) Cnemidophorus gularisa

Ctenosaura pectinataa

Iguana iguanaa

Sceloporus variabilisa

a Species captured in the field, all others were identified by sight, sound or other indirect m

On the other hand, the extrapolation of TRVs from laboratory towildlife speciesmay have underestimated the toxicity of the substances.In the present study, extrapolation from laboratory test animals towild-life species was made by means of allometric equations based on bodyweights, considering that responses to toxic chemicals is best expressedin terms of body weight raised to the 3/4 power (Travis and White,1988; USEPA, 2011). This means that, for mammals, metabolism isinversely proportional to their bodyweight and their sensitivity to con-taminants depicts the same behavior, in other words: smalleranimals have higher metabolic rates and usually are more resistant totoxic chemicals because of more rapid rates of detoxification, havinglower TRV (Sample et al., 1996). Mammals used to estimate TRVsshown on Table 9 have average body weights of 0.03 kg (mouse) and

Common name (English) Common name (Spanish)

Bat MurciélagoMexican fruit bat Murciélago zapoteroNine-banded armadillo Armadillo de nueve bandasVirginia opossum TlacuacheHooded skunk Zorrillo rayadoRaccoon MapacheSpotted skunk Zorrillo pigmeoEastern cotton tail rabbit Conejo de monteBuff bellied hummingbird Colibrí yucateco, chupaflorCommon ground dove Tortolita, coquita, mucuyBlack Vulture Zopilote, zamuro negroGroove-billed ani Garrapatero, pijulBlackbellied whistling duck Pichichi, PijijeBarn swallow GolondrinaOriole CalandriaWoodpecker golden fronted Pájaro carpintero, ChequeSocial flycatcher Mosquero, luisilloOsprey Águila pescadoraHouse sparrow Gorrión domésticoGreat tailed grackle ZanateTropical wild kingbird Mosquero tropicalMourning dove Paloma de alas blancasTexas spotted whiptail Lagartija llaneraMexican spiny-tailed iguana Iguana negra, garroboGreen iguana Iguana verdeRosebelly lizard Lagartija

eans.

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223R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

0.35 kg (rats). All wildlifemammals addressed in this study, except batsand spotted skunk, presented weights between 0.83 kg and 4.9 kg (seeTable 5).

Considering the aforementioned, it is possible that the big differ-ences in weights, two orders of magnitude in some cases, betweentest and wildlife species could lead to an overestimation of theNOAEL doses, producing lower HQs and, in consequence, higher al-lowable concentrations of contaminants in the medium. This overes-timation, whatever its magnitude, may be reduced if specific TRVswere obtained for the fauna species present at the site. Since, inMexico, this is not possible most of the time, because of the highcosts of the studies in the laboratory, it is recommended to developTRV values for test species more similar to the prevailing Mexicanwildlife species.

Body weights of Mexican mammals vary from a few grams, e.g.,some species of shrews, bats and rodents, to over 100 kg, e.g. tapir(Tapirus bairdii), wild boar (Sus scrofa) and the American black bear(Ursus americanus) (Álvarez-Romero and Medellín, 2005). Betweenthese two extreme values, there is a wide variety of small to mediumsized mammals like opossums, raccoons, wildcats, and armadillos,whose weights range from 1 to 10 kg, followed by bigger mammalswith weights between 10 and 100 kg (e.g., howler monkeys, coyotes,bighorn sheep, and jaguars). According to Sarukhán et al. (2009) andRamírez-Pulido (2008) in Mexico there are between 477 and 488 spe-cies of mammals; 78% to 80% of these species are small sized animalslike shrews and moles (order Insectivora), rodents (order Rodentia),and bats (order Chiroptera) (López-Rojas, 2004). This fact has beencorroborated by field studies performed by Ceballos et al., 2009, in theState of Mexico, and Cruz-Lara et al., 2004, in the state of Chiapas; inthese investigations the orders with the largest number of recordswere Chiroptera and Rodentia. It is important to note that with the ex-ception of some species like Agouti paca (Rodentia), which may reach13 kg of bodyweight (Sánchez et al., 1998), weights of bats and rodentsare less than 1 kg. On the other hand, body weights of test species usedin the laboratory to obtain TRVs (rats and mice) are very similar to theweights of the 80% of Mexican mammals, therefore, it can be assumedthat the estimated values of HQ for that 80% of species, may be accurate.However, to achieve a better performance of the HQ methodology, it isrecommended to perform toxicological tests with species having bodyweights more similar to the remaining 20% of the Mexican mammals;especially those with body weights between 1 and 10 kg that are verycommon.

Table 4Concentrations (mg/kg dry weight) of COPECs found in the biota tissues collected in the Study

Contaminant Mammalsa Birdsb

Acenaphthene 7.10E−03 5.50E−03Fluorene 5.00E−03f 7.30E−03Phenanthrene 1.41E−02 1.13E−02Anthracene 5.00E−03f 7.10E−03Fluoranthene 1.00E−02 9.60E−03Pyrene 5.00E−03f 5.00E−03f

Benzo(a)anthracene 5.00E−03f 5.00E−03f

Chrysene 1.00E−02 5.50E−03Benzo(k)fluoranthene 2.80E−01 6.99E−02Benzo(a)pyrene 6.71E−02 1.74E−02Indene(1,2,3,c,d)pyrene 5.00E−03f 5.00E−03f

Benzo(g,h,i)perylene 1.00E−02 5.90E−03

a Geometric mean of muscular tissue from the herbivorous mammals captured in the studyb Geometric mean of muscular tissue from the birds captured in the study area that feed on v

M. similis, and T. melancholicus (2 samples).c Geometricmean ofmuscular tissue from the reptiles captured in the study area that feed on

S. variabilis (2 samples).d Geometric mean of composite samples: orders Scolopendromorpha, Blattodea, Isopoda, H

non identified larvae.e Geometric mean of plant tissue collected in the study area (seven samples): Caesalpinia m

Cynodon dactylon (leaves), Senna occidentalis (leaves), and Psidium guajava (leaves).f Below detection level (DL) = DL/2.

Other aspects that need to be consideredwhenperforming an ERA inMexico are: a) using contaminants that are more frequently found inMexican contaminated sites by hydrocarbons, e.g. 16 priority hydrocar-bons proposed by theUSEPA,MTBE, andmixtures of substances, like thefractions of hydrocarbons determined in theMexican standard that is inforce at the present time (light, medium and heavy fractions; NOM-138-SEMARNAT/SSA1-2012; DOF, 2012), b) aging and weathering ofcontaminants in the soil, and c) the organisms adaptation capacity tocontamination (the possibility of using previously exposed organismsin laboratory toxicity tests should be assessed). These actions are ex-pected to reduce errorswhen extrapolating TRV values from test speciesto wildlife species.

In this study, the assessment was performed considering singlechemicals separately, but in the real world organisms are exposed tomixtures of substances acting at the same time. One of the most fre-quently used methods to approach this problem is the hazard index(HI), which is the sum of the hazard quotients of different substances.This method requires similarity in target organ (ORD, 2000; SCHER-SCCS-SCENIHR, 2012), so care must be taken in order to group sub-stances in an appropriate manner. In the present study most PAHswere assessed considering reproductive effects, but this was becausethe effect for benzo(a)pyrene was used as surrogate (due to the lackof specific information). The use of surrogate TRVs for this indexmay in-crease its uncertainty.

Considering the above, a better approachmay be to test themixturesdirectly on biological systems in order to obtain specific TRVs. Neverthe-less, to obtain TRVs for the principal mixtures of hydrocarbons inMexico, it should be highlighted that for the heavy fraction (N C18),the analytical method established in the Mexican standard (NOM-138-SEMARNAT/SSA1-2012; DOF, 2012) is not specific since there isan overlap with the medium fraction (C10–C28) and, on the otherhand, the composition of theMexican crudes varies, so it may be neces-sary to perform specific tests on a case-by-case basis.

4. Conclusions

The risk to the omnivorous mammals exposed to PAHs in this studyis acceptable (HQ b 1 for all contaminants and mammal speciesassessed). Themethodology is adequate in terms of the types of param-eters considered in the calculations, but it was concluded that to reduceuncertainty, more research is needed in Mexico. This should be primar-ily aimed at obtaining TRVs for mammals, considering test species with

Area.

Reptilesc Invertebratesd Plantse

7.60E−03 5.00E−03f 6.90E−031.86E−02 5.00E−03f 1.67E−023.90E−02 5.00E−03f 8.00E−031.54E−02 1.00E−02 9.35E−031.57E−02 5.00E−03f 9.42E−038.20E−03 5.00E−03f 5.00E−03f

7.90E−03 5.00E−03f 6.46E−031.18E−02 5.00E−03f 1.95E−021.00E−02 5.00E−03f 8.80E−022.16E−02 5.00E−03f 4.00E−015.70E−03 5.00E−03f 2.51E−025.70E−03 5.00E−03f 2.37E−02

area (two specimens: A. intermedius and A. jamaicensis).egetable material and invertebrates (six specimens): C. passerina (2 samples),M. aurifrons,

vegetablematerial and invertebrates (five specimens):C. gularis, C. pectinata, I. iguana, and

emiptera, Orthoptera (2 samples), Opiliones, Hymenoptera (2 samples), Lepidoptera, and

exicana (stems and leaves), Indigofera suffructicosa (leaves), Panicum maximum (leaves),

Page 7: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Table 6Total food ingestion rate (TFIR) and water ingestion rate (IRw) equations found in the literature for the species found in the Study Area.

Identification Code Intake equations(TFIR and IRw)

Type of organism

Eq1 0.323(BW)0.744a Mammals in generalEq2 0.299(BW)0.767a Eutherian mammalsEq3 0.859(BW)0.628a Herbivorous mammalsEq4 0.365(BW)0.671a Mammals from the Order ChiropteraEq5 0.432(BW)0.678a Omnivorous mammalsEq6 0.483(BW)0.666a Marsupial mammalsEq7 0.638(BW)0.685a Birds in generalEq8 0.344(BW)1.216a Birds from the Order ApodiformesEq9 0.670(BW)0.627a Omnivorous birdsEq10 0.301(BW)0.751b Non-passerine birdsEq11 0.849(BW)0.663a Carnivorous birdsEq12 0.540(BW)0.705a Insectivorous birdsEq13 0.630(BW)0.683a Passerine birdsEq14 0.0111(BW)0.920a Reptiles in generalEq15 0.0109(BW)0.914a Insectivorous reptilesEq16 0.0109(BW)0.944a LizardsEq17 0.0334(BW)0.717a Herbivorous reptilesEq18 0.0141(BW)0.884a Lizards from the Infraorder IguaniaEq19 0.0291(BW)0.782a Reptiles from the Family IguanidaeEq20 0.019(BW)0.841b Herbivorous reptiles from the Family IguanidaeEq21 0.0252(BW)0.542a Lizards from the Family PhrynosomatidaeEq22 0.099(BW)0.90c Mammals in generalEq23 0.326(BW)0.818d Eutherian mammalsEq24 0.708(BW)0.795d Herbivorous mammalsEq25 0.059(BW)0.67c Birds in generalEq26 1.369(BW)0.694d Birds in generalEq27 0.981(BW)0.746d Carnivorous birdsEq28 1.180(BW)0.874d Passerine birdsEq29 0.065(BW)0.726e Reptiles in general

BW = body weight.a TFIR equation (g dry weight/d) from Nagy (2001), BW in g (fresh weight).b TFIR equation (g dry weight/d) from Nagy (1987), BW in g (fresh weight).c IRw equation (L/d) from Calder and Braun (1983), BW in kg (fresh weight).d IRw equation (mL/d) from Nagy and Peterson (1988), BW in g (fresh weight).e IRw equation (mL/d) from Gibson et al. (1997), BW in g (fresh weight).

Table 5Body weight data (BW, kg) for the fauna species found in the Study Area.

Species N Max Min SD Avg GMa

MammalsA. intermedius 98 0.031 0.090 0.0099 0.0569 0.0561A. jamaicensis 158 0.026 0.056 0.0051 0.0415 0.0412D. novemcinctus 12 0.678 3.950 1.2871 2.1898 1.7778D. virginiana 52 0.176 6.322 1.1238 1.6820 1.3625M. macroura 11 0.589 1.500 0.3059 1.0377 0.9965P. lotor 3 3.003 7.500 2.2483 5.2466 4.9042S. putorius 8 0.199 0.830 0.2476 0.3940 0.3406S. floridanus 37 0.334 1.517 0.3574 0.9058 0.8334

BirdsA. yucatanensis 24 0.003 0.005 0.0007 0.0042 0.0041C. passerina 57 0.030 0.046 0.0038 0.0376 0.0374C. atratus 3 0.885 1.750 0.4583 1.4050 1.3476C. sulcirostris 60 0.0555 0.13 0.0122 0.0785 0.0776D. autumnalis 7 0.606 0.799 0.0739 0.6926 0.6893H. rustica 29 0.008 0.040 0.0070 0.0172 0.0162M. aurifrons 28 0.058 0.091 0.0096 0.0757 0.0751M. similis 55 0.024 0.039 0.0033 0.0315 0.0314P. haliaetus 2 1.300 1.316 0.0113 1.3080 1.3070P. domesticus 22 0.019 0.030 0.0025 0.0266 0.0265Q. mexicanus 40 0.077 0.360 0.0637 0.1736 0.1628T. melancholicus 41 0.030 0.049 0.0048 0.0385 0.0382Z. macroura 14 0.083 0.128 0.0127 0.1067 0.1060

ReptilesC. gularis NA NA NA NA NA NAC. pectinata 68 0.222 1.773 0.3704 0.7078 0.6168I. iguana 11 0.113 2.237 0.7486 0.7330 0.4267S. variabilis 141 0.002 0.024 0.0040 0.0094 0.0085

N = number of specimens found in the zoological collections; Max = maximum; Min = minimum; SD = standard deviation; Avg = average; GM = geometric mean; NA = notavailable.Note: Weights of the different specimens were gathered from the Zoological Museum “Alfonso L. Herrera”, Faculty of Sciences, Universidad Nacional Autónoma de México (UNAM); and,Collections of birds, mammals, and reptiles of the National School of Biology, Instituto Politécnico Nacional (IPN).

a BW values used in Eq. (3).

224 R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

Page 8: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Table 7Total food ingestion rate (TFIR, g dry weight/d) and water ingestion rate (IRw, L/d, mL/d) equations per fauna species (all species found in the Study Area).

Species N Applicable TFIR equations a Applicable IRw equations a

MammalsA. intermedius 98 Eq1,Eq2,Eq3,Eq4⁎ Eq22⁎,Eq23,Eq24A. jamaicensis 158 Eq1,Eq2,Eq3,Eq4⁎ Eq22⁎,Eq23,Eq24D. novemcinctus 12 Eq1,Eq2,Eq5⁎ Eq22⁎,Eq23D. virginiana 52 Eq1,Eq5⁎,Eq6 Eq22⁎M. macroura 11 Eq1,Eq2,Eq5⁎ Eq22⁎,Eq23P. lotor 3 Eq1,Eq2,Eq5⁎ Eq22⁎,Eq23S. putorius 8 Eq1,Eq2,Eq5⁎ Eq22⁎,Eq23S. floridanus 37 Eq1,Eq2,Eq3⁎ Eq22⁎,Eq23,Eq24

BirdsA. yucatanensis 24 Eq7,Eq8⁎,Eq9, Eq10 Eq25⁎,Eq26C. passerina 57 Eq7,Eq10⁎ Eq25⁎,Eq26C. atratus 3 Eq7,Eq10,Eq11⁎ Eq25⁎,Eq26,Eq27C. sulcirostris 60 Eq7,Eq10,Eq12⁎ Eq25⁎,Eq26D. autumnalis 7 Eq7,Eq9,Eq10⁎ Eq25⁎,Eq26H. rustica 29 Eq7,Eq12, Eq13⁎ Eq25⁎,Eq26,Eq28M. aurifrons 28 Eq7,Eq9,Eq10⁎ Eq25⁎,Eq26,M. similis 55 Eq7,Eq9,Eq13⁎ Eq25⁎,Eq26,Eq28P. haliaetus 2 Eq7, Eq10, Eq11⁎ Eq25⁎,Eq26,Eq27P. domesticus 22 Eq7,Eq9,Eq13⁎ Eq25⁎,Eq26,Eq28Q. mexicanus 40 Eq7,Eq9,Eq13⁎ Eq25⁎,Eq26,Eq28T. melancholicus 41 Eq7,Eq12,Eq13⁎ Eq25⁎,Eq26,Eq28Z. macroura 14 Eq7,Eq10⁎ Eq25⁎,Eq26

ReptilesC. gularis 0b Eq14,Eq15,Eq16 Eq29C. pectinata 68 Eq14,Eq16,Eq17,Eq18. Eq19⁎,Eq20 Eq29⁎I. iguana ◊ 11 Eq14,Eq16,Eq17,Eq18, Eq19⁎,Eq20 Eq29⁎S. variabilis 141 Eq14,Eq15,Eq16,Eq21⁎,Eq18 Eq29⁎

N = number of specimen's body weights used for the application of TFIR and IRw equations.a Equations corresponding to these codes are described on Table 6.b There was no information regarding body weights for this species and no calculations could be made with the equations shown.⁎ Selected equation for the estimation of TFIR for each species.

Table 8Summary of the values of total food ingestion rate (TFIR, kg dryweight/d), water ingestion rate (IRw, L/d), soil ingestion rate (IRs, kg dryweight/d), and diet composition used in this studyfor all the species found in the Study Area.

Species TFIRa IRwa IRsb Diet composition

MammalsA. intermedius 0.00544 0.00741 5.44E−06 (0.1%) VA. jamaicensis 0.00443 0.00561 4.43E−06 (0.1%) VD. novemcinctus 0.06901 0.16616 1.17E−02 (17.0%) V,I,M,B,RD. virginiana 0.05762 0.13078 2.88E−03 (5.0%) V,I,M,B,RM. macroura 0.04661 0.098699 7.92E−03 (17.0%) V,I,MP. lotor 0.13730 0.414129 1.24E−02 (9.0%) V,I,M,BS. putorius 0.02251 0.03755 3.83E−03 (17.0%) V,I,MS. floridanus 0.05868 0.08407 1.17E−03 (2.0%) V

BirdsA. yucatanensis 0.00192 0.00150 1.92E−06 (0.1%) V,IC. passerina 0.00457 0.00653 9.14E−05 (2.0%) VC. atratus 0.10371 0.07203 4.15E−03 (4.0%) M,BC. sulcirostris 0.01161 0.01064 1.97E−03 (17.0%) ID. autumnalis 0.04076 0.06671 8.15E−04 (2.0%) V,IH. rustica 0.00422 0.00373 4.22E−06 (0.1%) IM. aurifrons 0.00771 0.01041 1.54E−04 (2.0%) V,IM. similis 0.00663 0.00580 6.63E−06 (0.1%) V,IP. haliaetus 0.09886 0.07059 9.89E−05 (0.1%) FP. domesticus 0.00591 0.00518 1.18E−04 (2.0%) V,IQ. mexicanus 0.01632 0.01748 3.26E−04 (2.0%) V,I,RT. melancholicus 0.00759 0.00663 7.59E−06 (0.1%) V,IZ. macroura 0.00999 0.01312 2.00E−04 (2.0%) V

ReptilesC. gularis NA NA NA (17.0%) IC. pectinata 0.00442 0.00690 4.42E−06 (0.1%) V,I, pI. iguana 0.00332 0.00527 3.32E−06 (0.1%) V,I, pS. variabilis 0.00008 0.00031 1.36E−05 (17.0%) I

V = vegetable material; I = invertebrates; M = mammals; B = birds; R = reptiles; F = diet based on fish; not considered in this study because in this case only the terrestrialenvironment was evaluated; p = diet based on plants (vegetables) for juveniles.

a Geometric mean of the values obtained for all specimens using equations selected in Table 7 (marked with *).b % of dry weight TFIR, numbers in parenthesis indicate the % of TFIR considered in each case according to Gibson et al. (1997) recommendations.

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Page 9: Ecological risk assessment for small omnivorous mammals exposed to polycyclic aromatic hydrocarbons: A case study in northeastern Mexico

Table 9Oral dose (Doseoral, mg/kg/d), toxicity reference values (TRVs, mg/kg/d), and effects of the contaminants on the small omnivorousmammals of interest and laboratory test species used inthe extrapolation.

Contaminant TRV for test species Doseoral/TRVa for wildlife species

NOAEL (chronic) Test species Effect D. novemcinctus D. virginiana M. macroura P. lotor S. putorius

Acenaphthene 1b Mouse R 1.42E−02/0.36 4.75E−03/0.39 1.71E−02/0.42 5.53E−03/0.28 2.43E−02/0.54Fluorene 1b Mouse R 7.84E−03/0.36 2.84E−03/0.39 9.42E−03/0.42 3.10E−03/0.28 1.33E−02/0.54Phenanthrene 1b Mouse R 2.98E−03/0.36 1.42E−03/0.39 3.30E−03/0.42 1.18E−03/0.28 4.67E−03/0.54Anthracene 100 (A) c Mouse S 3.19E−03/36.04 1.31E−03/38.52 3.80E−03/41.65 1.31E−03/27.97 5.37E−03/54.48Fluoranthene 125 (B)d Mouse L,K 1.37E−03/45.05 7.39E−04/48.15 1.57E−03/52.07 6.18E−04/34.96 2.22E−03/68.1Pyrene 75 (C)d Mouse L,K 1.07E−03/27.03 5.14E−04/28.89 1.27E−03/31.24 4.69E−04/20.98 1.79E−03/40.86Benzo(a)anthracene 15 (D)c Rat L,K,G 2.33E−03/9.99 9.25E−04/10.68 2.80E−03/11.55 9.60E−04/7.75 3.96E−03/15.1Chysene 1b Mouse R 3.09E−03/0.36 1.39E−03/0.39 3.78E−03/0.42 1.37E/03/0.28 5.32E−03/0.54Benzo(k)fluoranthene 1b Mouse R 5.29E−03/0.36 4.40E−03/0.39 7.95E−03/0.42 3.78E−03/0.28 1.12E−02/0.54Benzo(a)pyrene 1 (E)e Mouse R 4.43E−03/0.36 4.47E−03/0.39 7.90E−03/0.42 3.60E−03/0.28 1.12E−02/0.54Indene(1,2,3,c,d)pyrene 1b Mouse R 6.85E−04/0.36 4.93E−04/0.39 9.44E−03/0.42 4.07E−04/0.28 1.33E−03/0.54Benzo(g,h,i)perylene 1b Mouse R 9.18E−04/0.36 5.96E−04/0.39 1.24E−03/0.42 5.15E−04/0.28 1.75E−03/0.54

NOAEL = No observed adverse effect level (mg/kg/d); LOAEL = Lowest observed adverse effect level (mg/kg/d); R = Reproductive; S = Sistemic; L = Liver; K = Kidney;G = Gastrointestinal.Sources: (A) USEPA (1989); (B) USEPA (1988); (C) TRL (1989); (D) Nousiainen et al. (1984); (E) Mackenzie and Angevine (1981).Note: HQ is defined by the Doseoral/TRV rate described in the right side of the table (HQ b 1 in all cases).

a TRV obtained from equation proposed by Sample et al. (1996).b No specific TRVs were found, information for benzo(a)pyrene was used as surrogate data.c Extrapolation from NOAELsubchronic to NOAELchronic was needed.d No extrapolation was needed.e Extrapolation from LOAELsubchronic (during pregnancy) to LOAELchronic and from LOAELchronic to NOAELchronic was needed.

226 R.M. Flores-Serrano et al. / Science of the Total Environment 476–477 (2014) 218–227

BWs more similar to the ones found in the local fauna, especially thosewith body weights between 1 and 10 kgwhich are very common.Moreresearch is also needed in order to report local fauna characteristics suchas body weights, diet composition, and total food, water and soil inges-tion rates.

Acknowledgments

Authors gratefully acknowledge Ángel A. Vega López (biologicalcharacterization, fauna), Pilar Gabriela Ibáñez Hernández (birds identi-fication), Edmundo Pérez Ramos (reptiles identification), Carlos FloresTorres and Jesús Flores Torres (soil sampling), Livia León Paniagua andthe Zoological Museum “Alfonso L. Herrera”, Universidad NacionalAutónoma de México (UNAM), for providing traps and nets used forthe biological characterization, Roberto Carlos Barrientos Medina forhis help in the statistical analysis, the Undergraduate Scholarship Pro-gramof UNAM, and Instituto de Ingeniería, UNAM for the funds providedfor this research.

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