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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.48 no.5 Valparaíso Nov. 2020

http://dx.doi.org/10.3856/vol48-issue5-fulltext-2461 

Review

Review of the biomonitoring of persistent, bioaccumulative, and toxic substances in aquatic ecosystems of Mexico: 2001-2016

Eduardo Ramírez-Ayala1 

Miguel A. Arguello-Pérez1 

Adrián Tintos-Gómez1  2 

Rebeca Y. Pérez-Rodríguez3 

Juan A. Díaz-Gómez2 

Imelda Borja-Gómez4 

César Antonio Sepúlveda-Quiroz5 

Manuel Patiño-Barragán4 

Carlos Lezama-Cervantes4 

Joel Salomé-Baylón2 

1Doctorate Program in Sciences in Biosystematics, Ecology and Management of Natural and Agricultural Resources (BEMARENA), Department of Studies for the Development of the Coastal Zone University of Guadalajara, Cihuatlán, Jalisco, Mexico

2Renewable Energy Research Center, Technical Secretariat of the Academic Area Technological University of Manzanillo, Manzanillo, Colima, Mexico

3Department of Chemistry, Division of Natural and Exact Sciences University of Guanajuato, Mexico

4Faculty of Marine Sciences, University of Colima, Manzanillo, Colima, Mexico

5Laboratory of Tropical Aquaculture, Academic Division of Biological Sciences (DACBiol) Juárez Autonomous University of Tabasco, Villahermosa, Tabasco, México

ABSTRACT

Mexico is responsible for the protection and management of a large number and variety of aquatic bodies of national and international importance. Environmental pollution by so-called persistent and bioaccumulative toxic substances (PBTS) poses significant risks for all of the world's aquatic ecosystems, especially in countries with emerging economies, where environmental regulations are often poorly implemented. In Mexico, the development of industrial projects and the deficient application of environmental regulations, together with the rapid increase in population and the inefficient disposal of urban waste, have generated a severe problem of water pollution in the country. National environmental protection programs have not included the monitoring of PBTS, even though researchers have been monitoring the main aquatic ecosystems of the country for nearly three decades, generating valuable information that could help improve the protection and exploitation of these ecosystems. The present work reviewed a large portion of the available literature (∼150 articles) on aquatic biomonitoring of the main PBTS (Hg, Cd, Pb, POCs, and PCBs) in Mexico. This work aims to collect, synthesize, and facilitate the management and interpretation of the reported data to improve the country's aquatic ecosystems' protection and management.

Keywords: PBTS; pollution; heavy metals; pesticides; biomonitoring; management; Mexico

INTRODUCTION

The chemical pollution of aquatic ecosystems, especially that caused by persistent and bioaccumulative toxic substances (PBTS), is one of the most critical problems facing modern society, both because of the important contribution to the overall degradation of aquatic ecosystems and the loss of biodiversity, but also because of the immediate risk posed for public health and food safety (Reyes et al., 2016). Creates a growing and multidimensional problem because aquatic ecosystems are the final destination of most PBTS derived from industrial, agricultural, and domestic activities, and this problem is expected to get more complicated by population and urban growth, as well as the accelerated growth of industrial activity around the world, especially in countries with emerging economies. Due to these countries' need for economic-industrial development, their governments often make important concessions to industrial sectors, sometimes at the expense of the integrity of their aquatic ecosystems and natural resources in general. Some of these countries also have great ecological wealth, belonging to the group of countries considered megadiverse (11 countries that, together, harbor about 70% of Earth's biodiversity), including China, India, Brazil, Mexico, and Indonesia. Mexico, a leading member of this group, has many aquatic ecosystems of both national and international importance, being the second country with the highest number of wetlands included in the RAMSAR agreement (RAMSAR, 2019). It is also the eleventh most populous country on the planet, and even though its industrial development has lagged behind that of other emerging economies, several of the country's industrial sectors have been developed intensively, as is the case of the mining industry, the oil industry, the textile industry, and the agricultural industry.

Due to the complicated balance between economic development and ecological protection, several international conventions and treaties, laws, regulations, national policies, and monitoring programs (including the National Monitoring Network of National Waters Quality restructured in 1995; CONAGUA, 2017) have been implemented to promote the protection and conservation of the country's aquatic ecosystems. However, the complex contamination scenarios involving much of the country's aquatic ecosystems (CONAGUA, 2017) require other competent authorities (McCulligh, 2014). It has become clear that pollutant monitoring programs of aquatic ecosystems are essential to ensure compliance with national and international commitments (e.g., Minamata Treaty or Stockholm Convention, ratified by Mexico in 2003 and 2015, respectively) regarding the protection and responsible exploitation of these natural assets.

In Mexico, there is enough information about the short-term effects of aquatic pollutants on wild organisms, but there is very little information on their effects on human health, particularly of those effects that are associated with impacted ecosystems (Álvarez-Moya & Reinoso-Silva, 2015; Gómez-Meda et al., 2017). However, researchers have spent nearly three decades monitoring the concentration of the most important PBTS in various environmental matrices (water, sediment, air, and biota) of the country's aquatic ecosystems, generating valuable information that can serve as the basis for decision-making in environmental and public health matters, and help improve the protection and responsible management of aquatic ecosystems. This work aims to review the available studies on the biomonitoring of PBTS (mainly heavy metals, organochlorine pesticides, and polyaromatic hydrocarbons) in the various aquatic ecosystems of Mexico between 2001 and 2016, presenting both the different concentrations of the main PBTS (Hg, Cd, Pb, POC) presented as well as the organisms most commonly used in their monitoring.

Selection of bibliographic material

The selection of scientific publications was made through a search in different academic databases and search engines (Elsevier-Scopus, SCIELO, CONRICyT, and Google Scholar) of monitoring studies of PBTS in aquatic ecosystems in Mexico. The search was delimited using several combinations of keywords such as: “Mexico”, “aquatic ecosystems”, “lagoon”, “estuary”, “bay”, “lake”, “river”, “wetland”, “swamp”, “pollution”, “pollutant”, “COPs”, “heavy metals”, “PCBs”, “biota”, “aquatic organisms”, “fish”, “bivalves”, “clams”, “crustaceans”, “aquatic birds”, among others, both in Spanish and in English. The search was carried out for the period from 2001 to 2016. For the selection of publications, only the articles and chapters of scientific books that met the following requirements were considered: 1) studies conducted in aquatic ecosystems of the Mexican territory, 2) studies on the concentration of heavy metals (Hg, Cd, and Pb), organochlorine pesticides, polychlorinated biphenyls, and polyaromatic hydrocarbons, and 3) studies conducted in biota tissue (muscle, liver, blood, eggs).

Selected studies

Based on these criteria, 150 publications were selected. The number of studies selected in the present study is consistent with Páez-Osuna et al. (2017), who found 382 publications on general pollution for the Gulf of California area in the last 45 years. For practicality, we divided the country's aquatic ecosystems into four regions (Fig. 1): Gulf of California, Gulf of Mexican Caribbean, Mexican Pacific, and inland ecosystems (rivers and lakes-reservoirs). The average concentration obtained by each study in the calendar year of sampling was considered the annual average concentration to simplify the visualization and interpretation of the concentrations of PBTS in the present work. In the cases in which the authors did not indicate a single annual average for the calendar year in which the sampling was carried out, as, in the case of seasonal sampling (rain and dry season, or spring, summer, autumn, and winter), the data corresponding to that calendar year were selected and averaged using the following expression:

Annual average=1ix1n1+x2n2++xinin1+n2++ni (1)

Figure 1 Mexican territory and political division. 1 Aguascalientes, 2 Baja California, 3 Baja California Sur, 4 Campeche, 5 Chiapas, 6 Chihuahua, 7 Coahuila, 8 Colima, 9 México Distrito Federal, 10 Durango, 11 Estado de México, 12 Guanajuato, 13 Guerrero, 14 Hidalgo, 15 Jalisco, 16 Michoacán, 17 Morelos, 18 Nayarit, 19 Nuevo León, 20 Oaxaca, 21 Puebla, 22 Querétaro, 23 Quintana Roo, 24 San Luis Potosí, 25 Sinaloa, 26 Sonora, 27 Tabasco, 28 Tamaulipas, 29 Tlaxcala, 30 Veracruz, 31 Yucatán, 32 Zacatecas. 

where x1, x2, … xi are average concentrations within the corresponding calendar year, and n1, n2, …, ni are the sample sizes of the respective average. In the case in which authors reported average concentrations for each sampling site within their study area, Equation 1 was used but taking x1, x2, …, xi as the averages of each sampling site and. n1, n2, …, ni as the sample sizes of the respective averages. Concerning persistent organic pesticides (POPs), which are found in the form X = x1 + x2, …, xn where X is the group of POPs and x are the metabolites, derivatives, or related compounds of X, the total annual concentration was obtained using the following expression:

X=1ix1n1+x2n2++xinin1+n2++nik (2)

where x1, x2, …, xi are the averages of each of the derivatives, n1, n2, …, ni are the sample sizes of the respective averages, and k is the number of derivatives of each group. When the authors presented more than one total annual concentration, Equation 1 was applied, substituting x for X, and n for k, applying the same temporal and spatial distribution criteria.

Persistent pollutants in aquatic organisms

Contamination of aquatic ecosystems with PBTS is one of the most critical environmental problems caused by direct human action (Saaristo et al., 2018) due to the great negative impact on wildlife. The adverse effects of pollution with PBTS can occur both in the short term (acute effects) and in the long term (chronic effects), including transgenerational effects. The effects of several of these pollutants (heavy metals and POPs mainly) at the sub-organism and organism level have been extensively studied for several decades and have been thoroughly described. PBTS are currently found in virtually all aquatic ecosystems in the world and, in most cases, below the probable effect concentrations established by environmental protection agencies, even below detection limits. Thus, aquatic organisms are continuously exposed to a wide variety of concentrations and mixtures of these substances throughout their life cycle, and the real effects of this exposure cannot be appreciated in the short term or at basic levels of biological organization (Schwarzenbach et al., 2006). Nevertheless, the effects of chronic long-term exposure to low concentration levels are equally harmful; they are just less obvious (Saaristo et al., 2018). These effects may occur at the genetic, epigenetic, or behavioral level, affecting present or future gene-rations, compromising long-term survival and repro-duction, and decimating and damaging existing populations.

Since a large part of the world's population depends on the consumption of fishery products (marine and freshwater, animal and vegetable) as an essential part of their daily diet and due to this fact, the ability of PBTS to bioaccumulate and biomagnify in the trophic networks of aquatic ecosystems pose a serious public health problem, mainly in developing countries (FAO, 2018). The consumption of fishery products is considered the primary source of exposure to PBTS in humans (Dórea, 2008). Although the effects of poisoning with food contaminated with PBTSs have been well established, while the long-term effects of the consumption of fishery products contaminated with low concentrations of PBTS are still being studied. These effects may include neurological, cardiovascular, endocrine, or immunological alterations, but further studies are required (Dórea, 2008). The biomonitoring of PBTS in aquatic ecosystems is thus a vital tool for protecting wildlife and public health, providing valuable information on these substances' bioavailability and the spatial and temporal variation of these substances' bioavailable fraction pollutants. For an organism to have potential as a biomonitor, it must possess a series of desirable attributes (both ecological and logistical) to facilitate its application. A wide variety of organisms are currently used as biomonitors of aquatic pollution, including fish, bivalves, crustaceans, macroalgae, birds, or mammals.

Heavy metals in biota

The presence, bioaccumulation, and biomagnification of heavy metals in aquatic ecosystems have been widely studied in recent decades because the presence and bioaccumulation of some of these metals in trophic networks can pose a serious risk to human health (Mendoza-Carranza et al., 2016). The potential for bioaccumulation and biomagnification of heavy metals is high, and such a process can be complex and difficult to understand. It is not yet clear how some metals biomagnify the trophic networks of aquatic ecosystems, while the biomagnification of Hg and Se is an easy process to elucidate; other cases, such as Cd and Pb, are still under discussion (Schneider et al., 2018). Bioaccumulation and bioconcentration processes are influenced by the exposure routes and by intraspecific and interspecific differences; thus, it is recommended that biomonitoring studies use several different species to make a better estimation of the behavior of pollutants in ecosystems (Jara-Marini et al., 2013). In general, monitoring the concentration of metals in aquatic organisms can make evident the pollution status of an ecosystem and help understand the potential risk to consumers (Wang et al., 2013).

Different organisms were used for monitoring the concentration of Hg, Cd, and Pb in different aquatic ecosystems in Mexico (Tables 12). Based on the information obtained in the present review, coastal ecosystems have been the most studied in this regard, mainly the coastal ecosystems of the Gulf of California. The organisms used as biomonitors include various groups, such as macroalgae, bivalve mollusks, fish, sharks, rays, birds, and turtles. Bivalves and fish were the most frequently used, maybe because bivalves are frequently used as biomonitors throughout the world (Páez-Osuna & Osuna-Martínez, 2011). They have various desirable qualities for aquatic biomonitoring, such as resistance to handling (which means they can be used for both in situ and ex situ studies), simple eating habits, they are efficient accumulators, sedentary, abundant, and cosmopolitan. However, even though they are found virtually on all Mexican coastal sites, their use as biomonitors has been limited to the Gulf of California area, mainly the States of Sonora and Sinaloa coasts. Furthermore, in some areas of the central Mexican Pacific (Jalisco-Colima-Michoacán), the northern part of the Gulf of Mexico (Tamaulipas), and the Mexican Caribbean, the number of studies using bivalves within the reviewed period are significantly scarce. Regarding the bivalve species used, the genus Crassostrea was the most common, probably due to its commercial importance, given that these species are extensively cultivated in coastal lagoons of the Gulf of California, which would have simplified many logistical issues during the sampling campaigns.

Table 1 Average concentration of Hg (in μg g−1 dw) in different tissues of organisms from various aquatic ecosystems of Mexico. 

Species Place Hg Reference
Primary producers
Fitoplankton UR (SIN) 0.02D (2006) Jara-Marini et al. (2012)
Gracilaria sp. UR (SIN) 0.02D (2006) Jara-Marini et al. (2012)
Gracilaria subsecuentata BGY (SON) 0.09 (1998) Green-Ruiz et al. (2005)
Chaetomorpha linum UR (SIN) 0.04D (2006) Jara-Marini et al. (2012)
Caulerpa serticularioides UR (SIN) 0.02D (2006) Jara-Marini et al. (2012)
Ulva Lactuca BGY (SON) 0.05D (1998) Green-Ruiz et al. (2005)
Mollusks
Crassostrea corteziensis BBP (SON) 0.04W (2004) ST García-Rico et al. (2010)
0.03W (2005) ST García-Rico et al. (2010)
UR (SIN) 0.05D (2006) ST Jara-Marini et al. (2012)
0.17D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
BCT (SIN) 0.37D (N/E) ST Osuna-Martínez et al. (2010)
0.57D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
LTB (SON) 0.43D (2009) ST Jara-Marini et al. (2013)
LCL (SIN) 0.54D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
SMOT (SIN) 0.18D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
INM (SIN) 0.39D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
SMR (SIN) 0.30D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
AEP (SIN) 0.52D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
ERY (SIN) 0.29D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
UR (SIN) 0.05D (2006) ST Jara-Marini et al. (2008)
Crassostrea gigas BGY (SON) 0.23 (1998) ST Green-Ruiz et al. (2005)
LTB (SON) 0.39D (2009) Jara-Marini et al. (2013)
LCL (SIN) 0.93D (N/E) ST Osuna-Martínez et al. (2010)
BCT (SIN) 0.46D (N/E) ST Osuna-Martínez et al. (2010)
SMR (SIN) 0.24D (N/E) ST Osuna-Martínez et al. (2010)
AEP (SIN) 0.23D (N/E) ST Osuna-Martínez et al. (2010)
CSNR (SON) 0.03W (1997) ST Garcia-Rico & Ramos-Ruiz (2001)
Crassostrea virginica LTM (CAM) 0.0001 (2011) ST Benítez et al. (2012)
RPL (CAM) 0.5 (N/E) ST Aguilar et al. (2012)
RCHP (CAM) 0.7 (N/E) ST Aguilar et al. (2012)
RCDLR (CAM) 1.1 (N/E) ST Aguilar et al. (2012)
Crassostrea sp. BCHC (SON) 0.17D (2010-2011) ST Delgado-Álvarez et al. (2015b)
SBRB (SON) 0.25D (2010-2011) ST Delgado-Álvarez et al. (2015b)
LTB (SON) 0.14D (2010-2011) ST Delgado-Álvarez et al. (2015b)
BAP (SON) 0.17D (2010-2011) ST Delgado-Álvarez et al. (2015b)
SMR (SIN) 0.19D (2010-2011) ST Delgado-Álvarez et al. (2015b)
BCMCH (NAY) 0.19D (2010-2011) ST Delgado-Álvarez et al. (2015b)
CGC (N/A) 0.17D (2010-2011) ST Delgado-Álvarez et al. (2015b)
Megapitaria squalida BKK (SON) 0.001 (2003) ST García-Hernández et al. (2005)
Mytella strigata UR (SIN) 0.06D (2006) ST Jara-Marini et al. (2012)
UR (SIN) 0.06D (2006) ST Jara-Marini et al. (2008)
Chione fluctifraga LTB (SON) 0.28D (2009) ST Jara-Marini et al. (2013)
Chione gnidia LTB (SON) 0.47D (2009) ST Jara-Marini et al. (2013)
Chione californiensis BKK (SON) 0.001W (2003) ST García-Hernández et al. (2005)
Chione subrugosa BGY (SON) 0.06 (1998) ST Green-Ruiz et al. (2005)
Chione sp. DRC (SON) 0.04D (1998-2000) ST García-Hernández et al. (2001)
Anadara tuberculosa LTB (SON) 0.20D (2009) ST Jara-Marini et al. (2013)
Corbicula sp. RCL (SON) 0.04D (1998-2000) ST García-Hernández et al. (2001)
Corbicula fluminea RCZ (VER) 0.09D 2005) ST Ruelas-Inzunza et al. (2009a)
Polymesoda caroliniana RCZ (VER) 0.155D (2005) ST Ruelas-Inzunza et al. (2009a)
Polymesoda caroliniana RCZ (VER) 0.115D (2006) ST Ruelas-Inzunza et al. (2009a)
Pinna rugosa BKK (SON) 0.022W (2003) ST García-Hernández et al. (2005)
Hexaplex erythrostomus BKK (SON) 0.05W (2003) ST García-Hernández et al. (2005)
Mytilopsis sallei BCHM (ROO) 1.09 (2002) ST Díaz-López et al. (2006)
Crustaceans
Penaeus vannamei AEP (SIN) 0.20D (1998-1999) M Ruelas-Inzunza et al. (2004)
UR (SIN) 0.03D (2006) T Jara-Marini et al. (2012)
AEP (SIN) 0.06W (1998-1999) M Ruelas-Inzunza et al. (2011a)
GSNR (SON) 0.19 (2010) M Delgado-Álvarez et al. (2015a)
GSNL (SIN) 0.31 (2010) M Delgado-Álvarez et al. (2015a)
GNYR (NAY) 0.45 (2010) M Delgado-Álvarez et al. (2015a)
Litopenaeus stylirostris AEP (SIN) 0.30D (1998-1999) M Ruelas-Inzunza et al. (2004)
AEP (SIN) 0.09W (1998-1999) M Ruelas-Inzunza et al. (2011a)
Litopenaeus setiferus LTM (CAM) ND (2011) M Benítez et al. (2012)
Penaeus aztecus LAV (VER) 0.008 (2003) M Guentzel et al. (2007)
LAV (VER) 0.03W (2005) M Guentzel et al. (2007)
Farfantepenaeus AEP (SIN) 0.06W (1998-1999) M Ruelas-Inzunza et al. (2011a)
brevirostris AEP (SIN) 0.21D (1998-1999) M Ruelas-Inzunza et al. (2004)
Farfantepenaeus AEP (SIN) 0.04W (1998-1999) M Ruelas-Inzunza et al. (2011a)
californiensis AEP (SIN) 0.13D (1998-1999) M Ruelas-Inzunza et al. (2004)
Xiphopenaeus kroyeri AEP (SIN) 0.04W (1998-1999) M Ruelas-Inzunza et al. (2011a)
AEP (SIN) 0.13D (1998-1999) M Ruelas-Inzunza et al. (2004)
Palaemonetes BBCN (SON) 0.40D (1998-2000) T García-Hernández et al. (2001)
Paludosus CSC (SON) 0.60D (1998-2000) T García-Hernández et al. (2001)
Callinectes arcuatus UR (SIN) 0.13D (2006) T Jara-Marini et al. (2012)
Callinectes rathbunae LAV (VER) 0.02W (2012) M Guentzel et al. (2007)
Callinectes bellicosus BCY (SON) 0.20W (2012) M García-Hernández et al. (2015)
BST (SON) 0.26W (2012) M García-Hernández et al. (2015)
BKK (SON) 0.15W (2012) M García-Hernández et al. (2015)
GYEMP (SON) 0.08W (2012) M García-Hernández et al. (2015)
BGMS (SON) 0.09W (2012) M García-Hernández et al. (2015)
BLB (SON) 0.05W (2012) M García-Hernández et al. (2015)
LTB (SON) 0.10W (2012) M García-Hernández et al. (2015)
BYV (SON) 0.12W (2012) M García-Hernández et al. (2015)
BAP (SON) 0.19W (2012) M García-Hernández et al. (2015)
INM (SIN) 0.20W (2012) M García-Hernández et al. (2015)
BOH (SIN) 0.14W (2012) M García-Hernández et al. (2015)
SMR (SIN) 0.09W (2012) M García-Hernández et al. (2015)
AEP (SIN) 0.13W (2012) M García-Hernández et al. (2015)
Procambarus clarkii RMYR (SON) 0.05D (1998-200) T García-Hernández et al. (2001)
Fish
Opisthonema libertate BGY (SON) 0.20D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
BGY (SON) 0.06W (1998) M Ruelas-Inzunza et al. (2011a)
Paralichthys woolmani BTBP (SON) 0.68W (2004) M Ruelas-Inzunza et al. (2008)
BTBP (SON) 0.21W (2004) M Ruelas-Inzunza et al. (2011a)
Cyclopsetta querna CGRR (GRO) 0.21D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 0.39D (2011) M Ruelas-Inzunza et al. (2012)
Ancylopsetta dendritica CGRR (GRO) 0.26D (2011) M Spanopoulos-Zarco et al. (2014)
Achirus mazatlanus LBN (JAL) 0.29D (2014) M Aguilar-Betancourt et al. (2016)
Bagre marina LAV (VER) 0.29W (2005) M Guentzel et al. (2007)
Cathorops fuerthii BGY (SON) 0.45D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
Cathorops fuerthii BGY (SON) 0.14W (1998) M Ruelas-Inzunza et al. (2011a)
Galeichthys peruvianus AEP (SIN) 1.58D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
Arius platypogon BTBP (SON) 0.29W (2004) M Ruelas-Inzunza et al. (2011a)
Sciades guatemalensis LBN (JAL) 1.43D (2014) M Aguilar-Betancourt et al. (2016)
Arius felis LAV (VER) 0.27W (2000-2003) M Elliott et al. (2015)
Arius sp. ESBL (NAY) 0.20W (2000-2003) M Elliott et al. (2015)
Ictalurus furcatus PLL (CHH) 0.08W (2001-2012) M Luna-Porres et al. (2014)
Pterygoplichthys pardalis RUSMT (TAB) 0.45D (N/E) M Maldonado-Enríquez et al. (2015)
Eugerris plumeri LAV (VER) 0.35W (2002) M Guentzel et al. (2007)
LAV (VER) 0.30W (2005) M Guentzel et al. (2007)
Eugerris axillaris UR (SIN) 0.70D (2012) M Frías-Espericueta et al. (2016)
UR (SIN) 0.48D (2013) M Frías-Espericueta et al. (2016)
Gerres cinereus UR (SIN) 0.15D (2006) M Jara-Marini et al. (2012)
TCPN (SIN) 0.29W (2005) M Ruelas-Inzunza et al. (2011a)
ERCZ (VER) 0.09W (2005) M Ruelas-Inzunza et al. (2011a)
ERCZ (VER) 0.19D (2005) M Ruelas-Inzunza et al. (2009a)
Diapterus peruvianus BTBP (SON) 0.16W (2004) M Ruelas-Inzunza et al. (2011a)
CGRR (GRO) 0.53D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 2.55D (2011) M Ruelas-Inzunza et al. (2012)
Diapterus brevirostris LBN (JAL) 0.36D (2014) M Aguilar-Betancourt et al. (2016)
Cyprinus carpio LCHP (JAL) 0.39W (2010) M Stong et al. (2013)
LCHP (JAL) 0.35W (2011) M Torres et al. (2014)
LCHP (JAL) 0.10W (2012) M Torres et al. (2014)
PVM (MEX) NDW (2013) M Morachis-Valdez et al. (2015)
PLL (CHH) 0.008W (2011-2012) M Luna-Porres et al. (2014)
Criprynus sp. LCHP (JAL) 0.83W (2007) M Trasande et al. (2010)
Chirostoma sp. LCHP (JAL) 0.11W (2007) M Trasande et al. (2010)
LCHP (JAL) 0.15W (2011) M Torres et al. (2014)
LCHP (JAL) 0.07W (2012) M Torres et al. (2014)
Gambusia affinis RCL (SON) 0.63D (1998-2000) T García-Hernández et al. (2001)
RHD (SON) 0.32D (1998-2000) T García-Hernández et al. (2001)
RMYR (SON) 0.89D (1998-2000) T García-Hernández et al. (2001)
Poecilia latipinna CSC (SON) 0.12D (1998-2000) T García-Hernández et al. (2001)
Mugil cephalus CCP (SON) 0.04D (1998-2000) T García-Hernández et al. (2001)
BGY (SON) 0.02D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
AEP (SIN) 0.13D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
UR (SIN) 0.06D (2006) T Jara-Marini et al. (2012)
BGY (SON) NDD (1998) M Ruelas-Inzunza et al. (2011a)
BTBP (SON) 0.01W (2004) M Ruelas-Inzunza et al. (2011a)
AEP (SIN) 0.04W (1998-1999) M Ruelas-Inzunza et al. (2011a)
AEP (SIN) 0.03W (2004) M Ruelas-Inzunza et al. (2011a)
Mugil curema UR (SIN) 0.02W (2003) M Ruelas-Inzunza et al. (2011a)
SMR (SIN) 0.03W (2003) M Ruelas-Inzunza et al. (2011a)
LAV (VER) 0.57W (2003) M Guentzel et al. (2007)
LCTC (VER) 0.02W (2000-2003) M Elliott et al. (2015)
MTTN (VER) 0.14W (2000-2003) M Elliott et al. (2015)
LAV (VER) 0.03W (2000-2003) M Elliott et al. (2015)
LBN (JAL) 0.03D (2014) M Aguilar-Betancourt et al. (2016)
LCTC (VER) 0.02W (2000-2003) M Elliott et al. (2015)
Mugil sp. RSTG (NAY) 0.04W (2000-2003) M Elliott et al. (2015)
LBN (JAL) 0.02W (2000-2003) M Elliott et al. (2015)
UR (SIN) 0.18D (2012) M Frías-Espericueta et al. (2016)
UR (SIN) 0.15D (2013) M Frías-Espericueta et al. (2016)
Cichlasoma sp. LBN (JAL) 0.05W (2000-2003) M Elliott et al. (2015)
Oreochromis sp. LCHP (JAL) 0.04W (2007) M Trasande et al. (2010)
LCHP (JAL) 0.03W (2011) M Torres et al. (2014)
LCHP (JAL) 0.03W (2012) M Torres et al. (2014)
CSDR (CHP) 0.05W (2000-2003) M Elliott et al. (2015)
Oreochromis sp. RCZ (VER) 0.05D (2005) M Ruelas-Inzunza et al. (2009a)
Oreochromis niloticus LCTC (VER) 0.01W (2000-2003) M Elliott et al. (2015)
LAV (VER) 0.02W (2000-2003) M Elliott et al. (2015)
Lepomis macrochirus RHD (SON) 0.65W (2010) M García-Hernández et al. (2013)
CSC (SON) 0.69D (1998-2000) T García-Hernández et al. (2013)
Lepomis cyanellus PLL (CHH) 0.07W (2011-2012) M Luna-Porres et al. (2014)
Archosargus probatocephalus LAV (VER) 0.09W (2002) M Guentzel et al. (2007)
Gobiomorus polylepis RCZ (VER) 0.86D (2006) M Ruelas-Inzunza et al. (2009a)
Centropomus parallelus LAV (VER) 0.15W (2002) M Guentzel et al. (2007)
LAV (VER) 0.18W (2000-2003) M Elliott et al. (2015)
MTTN (VER) 0.29W (2000-2003) M Elliott et al. (2015)
TLCP (VER) 0.13W (2000-2003) M Elliott et al. (2015)
Centropomus viridis ERCZ (VER) 0.26W (2005) M Ruelas-Inzunza et al. (2011a)
ERCZ (VER) 0.68D (2005) M Ruelas-Inzunza et al. (2009a)
ERCZ (VER) 0.48D (2006) M Ruelas-Inzunza et al. (2009a)
Centropomus nigrescens BTBP (SON) 0.56D (2004) M Ruelas-Inzunza et al. (2008)
BTBP (SON) 0.17W (2004) M Ruelas-Inzunza et al. (2011a)
Centropomus armatus BTBP (SON) 1.51D (2004) M Ruelas-Inzunza et al. (2008)
BTBP (SON) 0.44W (2004) M Ruelas-Inzunza et al. (2011a)
Centropomus medius SMR (SIN) 0.82D (2003) M Ruelas-Inzunza et al. (2008)
Centropomus ensiferus LAV (VER) 0.18W (2005) M Guentzel et al. (2007)
Centropomus sp. MTCL (NAY) 0.30W (2000-2003) M Elliott et al. (2015)
Cynoscion xanthulus AEP (SIN) 0.1D (1998-1999) M García-Hernández et al. (2005)
Micropogonias ectenes CGRR (GRO) 0.54D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 0.65D (2011) M Ruelas-Inzunza et al. (2012)
Haemulopsis axillaris CGRR (GRO) 0.51D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 1.69D (2011) M Ruelas-Inzunza et al. (2012)
Umbrina xanti CGRR (GRO) 0.40D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 0.58D (2011) M Ruelas-Inzunza et al. (2012)
Pomadasys panamensis CGRR (GRO) 0.12D (2011) M Spanopoulos-Zarco et al. (2014)
Pseudupeneus grandisquamis CGRR (GRO) 0.38D (2011) M Spanopoulos-Zarco et al. (2014)
Hemicaranx leucurus CGRR (GRO) 0.13D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 0.58D (2011) M Ruelas-Inzunza et al. (2011)
Lutjanus colorado AEP (SIN) 0.89D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
URTCP (SIN) 0.53D (2003-2004) M Ruelas-Inzunza et al. (2008)
UR (SIN) 0.10W (2003) M Ruelas-Inzunza et al. (2011a)
AEP (SIN) 0.26W (1998-1999) M Ruelas-Inzunza et al. (2011a)
UR (SIN) 0.18W (2003) M Ruelas-Inzunza et al. (2011b)
Lutjanus argentiventris UR (SIN) 0.19D (2006) T Jara-Marini et al. (2012)
Caranx caninus BTBP (SON) 3.32D (2004) M Ruelas-Inzunza et al. (2008)
BTBP (SON) 1.0W (2004) M Ruelas-Inzunza et al. (2011a)
BTBP (SON) 0.2W (2004) M Ruelas-Inzunza et al. (2011b)
Polydactylus approximans CSNL (SIN) 1.72D (2011) M Ruelas-Inzunza et al. (2012)
Scorpaena sp. CSNL (SIN) 1.72D (2011) M Ruelas-Inzunza et al. (2012)
Oligoplites saurus BTBP (SON) 1.74D (2004) M Ruelas-Inzunza et al. (2008)
Isopisthus remifer CSNL (SIN) 1.77D (2011) M Ruelas-Inzunza et al. (2012)
Trachinotus kennedyi CGRR (GRO) 0.11D (2011) M Spanopoulos-Zarco et al. (2014)
CSNL (SIN) 0.10D (2011) M Ruelas-Inzunza et al. (2012)
Seriola lalandei BGY (SON) 0.76D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
GCFR (N/A) 0.07W (2003-2004) M García-Hernández et al. (2007)
BGY (SON) 0.23W (1998) M Ruelas-Inzunza et al. (2011a)
Thunnus albacares GCFR (N/A) 0.03W (2003-2004) M García-Hernández et al. (2007)
Coryphaena hippurus GCFR (N/A) 0.05W (2003-2004) M García-Hernández et al. (2007)
Makaira mazara GCFR (N/A) 0.36W (2003-2004) M García-Hernández et al. (2007)
Istiophorus platypterus GCFR (N/A) 0.40W (2003-2004) M García-Hernández et al. (2007)
Acanthocybium solandri GCFR (N/A) 0.15W (2003-2004) M García-Hernández et al. (2007)
Tetrapturus audax GCFR (N/A) 0.14W (2003-2004) M García-Hernández et al. (2007)
Sharks and rays
Carcharhinus limbatus PVCZ (VER) 3.33W (1994-1995) M Núñez-Noriega (2005)
GCFR (N/A) 0.51W (2003-2004) M García-Hernández et al. (2007)
Carcharhinus leucas AEP (SIN) 0.20D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
AEP (SIN) 0.62W (2003) M Ruelas-Inzunza et al. (2011b)
Carcharhinus falciformis GCFR (N/A) 0.30W (2003-2004) M García-Hernández et al. (2007)
PDBC (BCS) 3.40D (2001-2005) M Maz-Courrau et al. (2012)
Sphyrna lewini AEP (SIN) 0.49D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2005)
GCFR (N/A) 1.08W (2003-2004) M García-Hernández et al. (2007)
CSPT (SIN) 0.81W (2009-2010) M Hurtado-Banda et al. (2012)
TCPN (SIN) 0.63W (2011-2012) M Bergés-Tiznado et al. (2015)
Sphyrna zygaena GCFR (N/A) 8.25W (2003-2004) M García-Hernández et al. (2007)
PDBC (BCS) 0.98D (2001-2005) M Maz-Courrau et al. (2012)
Prionace glauca CBCF (BSC) 1.39W (2005-2006) Escobar-Sánchez et al. (2011)
PDBC (BCS) 1.96D (2001-2005) M Maz-Courrau et al. (2012)
PBLCH (BCS) 1.03W (2011) M Barrera-García et al. (2012)
Isurus oxyrinchus PDBC (BCS) 1.05D (2001-2005) M Maz-Courrau et al. (2012)
IMGD (BCS) 0.39w (2008) M Vélez-Alavez et al. (2013)
Squatina californica PPG (BCS) 0.24W (2012-2013) M Escobar-Sánchez et al. (2016)
Rhizoprionodon terraenove PVCZ (VER) 0.76W (1994-1995) M Núñez-Noriega (2005)
Rhizoprionodon longurio GCFR (N/A) 1.3W (2003-2004) M García-Hernández et al. (2007)
BKN (SON) 0.91W (2009-2010) M Hurtado-Banda et al. (2012)
Nasolamia velox GCFR (N/A) 1.02W (2003-2004) M García-Hernández et al. (2007)
Triakis semifasciata GCFR (N/A) 0.08W (2003-2004) M García-Hernández et al. (2007)
Dasyatis dipterura BCHY (SON) 0.946D (2012) M Ruelas-Inzunza et al. (2013)
PRY (NAY) 2.84D (2012) M Ruelas-Inzunza et al. (2013)
Dasyatis longus GCFR (N/A) 0.71W (2003-2004) M García-Hernández et al. (2007)
Dasyatis brevis GCFR (N/A) 0.45W (2003-2004) M García-Hernández et al. (2007)
Dasyatis longa PRY (NAY) 4.465D (2012) M Ruelas-Inzunza et al. (2013)
Rhinobatos productus GCFR (N/A) 0.31W (2003-2004) M García-Hernández et al. (2007)
PPG (BCS) 0.89D (2012) M Ruelas-Inzunza et al. (2013)
Rhinoptera steindachnerii GCFR (N/A) 0.43W (2003-2004) M García-Hernández et al. (2007)
DTLL (SIN) 0.37W (2012) M Escobar-Sánchez et al. (2014)
Narcine entemedor PPG (BCS) 0.101D (2012) M Ruelas-Inzunza et al. (2013)
PCHL (BCS) 1.053D (2012) M Ruelas-Inzunza et al. (2013)
GCFR (N/A) 0.12W (2003-2004) M García-Hernández et al. (2007)
Zapteryx exasperata GCFR (N/A) 0.11W (2003-2004) M García-Hernández et al. (2007)
PCHL (BCS) 0.898D (2012) M Ruelas-Inzunza et al. (2013)
Gymnura marmorata GCFR (N/A) 0.14W (2003-2004) M García-Hernández et al. (2007)
DTLL (SIN) 0.706D (2012) M Ruelas-Inzunza et al. (2013)
Myliobatis californica GCFR (N/A) 0.05W (2003-2004) M García-Hernández et al. (2007)
Mustelus albipinnis BKN (SON) 0.33W (2009-2010) M Hurtado-Banda et al. (2012)
Urolophus halleri PPG (BCS) 1.37D (2012) M Ruelas-Inzunza et al. (2013)
PRY (NAY) 2.33D (2012) M Ruelas-Inzunza et al. (2013)
Urolophus spp. PRY (NAY) 3.713D (2012) M Ruelas-Inzunza et al. (2013)
Mobula thurstoni DTLL (SIN) 0.09W (2012) M Escobar-Sánchez et al. (2014)
SBRB (SON) 0.20W (2012) M Escobar-Sánchez et al. (2014)
Mobula munkiana SBRB (SON) 0.19W (2012) M Escobar-Sánchez et al. (2014)
Mobula japanica SBRB (SON) 0.14W (2012) M Escobar-Sánchez et al. (2014)
DTLL (SIN) 0.01W (2012) M Escobar-Sánchez et al. (2014)
Urotrygon chilensis PCHL (BCS) 0.52D (2012) M Ruelas-Inzunza et al. (2013)
Raja velezi PPG (BCS) 1.127D (2012) M Ruelas-Inzunza et al. (2013)
Turtles
Chelonia mydas PDBC (BCS) 0.021 (N/E) M Kampalath et al. (2006)
LTM (CAM) 0.37 (2009) H Benítez et al. (2012)
Caretta caretta PDBC (BCS) 0.026 (N/E) M Kampalath et al. (2006)
Lepidochelys olivacea PDBC (BCS) 0.05 (N/E) M Kampalath et al. (2006)
PEPA (OAX) 0.0006 (2005-2006) S Páez-Osuna et al. (2011)
PEPA (OAX) 0.001 (2005-2006) H Páez-Osuna et al. (2011)
Eretmochelys imbrincata LTM (CAM) 0.37 (2009) H Benítez et al. (2012)
Birds
Phalacrocorax CSNL (SIN) 1.49D (2002) M Ruelas-Inzunza et al. (2009b)
Brasilianus UR (SIN) 1.01 D (2006) M Jara-Marini et al. (2012)
Pelecanus occidentalis CSNL (SIN) 2.85 D (2002) M Ruelas-Inzunza et al. (2009b)
Anas clypeata CSNL (SIN) 0.47 D (2002) M Ruelas-Inzunza et al. (2009b)
Anas discors CSNL (SIN) 0.77 D (2002) M Ruelas-Inzunza et al. (2009b)
Aythya affinis CSNL (SIN) 1.06 D (2002) M Ruelas-Inzunza et al. (2009b)
Sula leucogaster SMR (SIN) 1.12 (2010-2012) S Lerma et al. (2016)
Crocodiles
Crocodylus moreletti RCHPT (CAM) 3.1 (2012) B Trillanes et al. (2014)
LPNCLT (ROO) 4.3 (2012) B Trillanes et al. (2014)
RHND (ROO) 20 (2012-2013) S Buenfil-Rojas et al. (2015)
RHND (ROO) 0.33 (2012-2013) B Buenfil-Rojas et al. (2015)
Mammals
Tursiops truncatus LTM (CAMP) ND (2011) B Benítez et al. (2012)
Stenella longirostris GCFR (N/A) 1.2 (1993) M Ruelas-Inzunza et al. (2003)
Trichechus manatus LTM (CAMP) ND (2011) B Benítez et al. (2012)
Eschrichtius robustus GCFR (N/A) 0.14 (1999) M Ruelas-Inzunza et al. (2003)
Baleanoptera musculus GCFR (N/A) 0.06 (2012) B Ruelas-Inzunza et al. (2014)

EU: Estero Urías; AEP: Altata-Ensenada del Pabellón; BGY: Bahía Guaymas; GCFR: Golfo de California; GSNR: Granjas-Sonora; GSNL: Granjas Sinaloa; GNYR: Granjas Nayarit; BBP: Bahía de Bacochibampo; BCT: Bahía de Cueta; BBCN: Bocana; GYEMP: Guaymas-Empalme LTM: Laguna de Términos; LTB: Laguna El Tobari; LCL: El Colorado; ERY: Estero El Rey; SMOT: Santa María-Ohurias-Topolobampo; SMR: Santa María- LA Reforma; LCHP: Lago de Chapala; BKK: Bahía de Kuu Kaak; BGMS: Bahía Las Guácimas; LAV: Laguna Alvarado; CSNR: Costa de Sonora; BTBP: Bahía de Topolobampo; BAP: Laguna Agiabampo; BCHC: Bachoco; CSC: Ciénega Santa Clara; LBN: Laguna Barra de Navidad; SBRB: Santa Bárbara; RPL: Río Palizada; RCHP: Río Chumpán; BTPB: Bahía de Topolobampo; BCMCH: Boca Camichín; BCHM: Bahía Chetumal; PLL: Presa Luis León; CSDR: Cañón del sumidero; MTCL: Mercado de Tecuala; RCL: Río Colorado; RCDLR: Río Candelaria; BCY: Bahía La Choya; ESBL: Estero de San Blas; LCTC: Lago de Catemaco; BLB: Bahía de Lobos; RMYR: El Mayor; RUSMT: Río Usumacinta; TCPN: Teacapán; PVM: Presa Viejo Mandín; CCP: Cucapa; MTTN: Minatitlán; RSTG: Río Santiago; TLCP: Tlacotalpan; URTCP: Urías-Teacapán; PVCZ: Puerto de Veracruz; CSPT: Cospita; CBCF: Baja California; PBLCH: Punta Belcher; IMGD: Isla Magdalena; PPG: El Portugués; BCHY: El Choyudo; PRY: Playa del Rey; DTLL: Dautillos; PCHL: Puerto Chale; RCHPT: Río Champotón; LPNCLT: Los Petenes-Celestún; RHND: Río Hondo; CGRR: Costa de Guerrero; CSNL: Costa de Sinaloa; PDBC: Península de Baja California; PEPA: Playa la Escobilla-Puerto Escondido-Puerto Ángel. SON: Sonora; SIN: Sinaloa; NAY: Nayarit; JAL: Jalisco; COL: Colima; MIC: Michoacán; GRO: Guerrero; OAX: Oaxaca; CHP: Chiapas; CAM: Campeche; ROO: Quintana Roo; YUC: Yucatán; TAB: Tabasco; VER: Veracruz; TAM: Tamaulipas; BCS: Baja California Sur; BCN: Baja California Norte; AGU: Aguascalientes; MEX: México; CMX: Ciudad de México. N/E: not specified; ND: not detect; -: not analized;

Ddry weight;

Wwet weight;

M: muscle; ST: soft tissue; T: whole body; S: blood; B: biopsy; H: eggs.

Table 2 Average concentration of Cd and Pb (μg g−1 dw, D or ww, W) in different tissues of organisms from various aquatic ecosystems of Mexico. 

Species Place Cd Pb References
Primary producers
Plankton PAA (MEX) 8W (1998-1999) Rodríguez et al. (2001)
Phytoplankton AEP (SIN) 0.27D(1998-1999) 23D (1998-1999) Ruelas-Inzunza & Páez-Osuna (2006)
Ulva lactuca INM (SIN) 1.9D (2002) 174.8D (2002) Orduña-Rojas & Longoria-Espinoza (2006)
BGY (SON) 0.54D(1998-1999) 0.35D (1998-1999) Ruelas-Inzunza & Páez-Osuna (2006)
LCHT (SIN) 3D (2002-2003) Soto-Jiménez et al. (2008)
UR (SIN) 3D (2002-2003) Soto-Jiménez et al. (2008)
Gracilaria textorii BMGD (BCS) 3.65D(2004-2005) 0.83D (2004-2005) Talavera-Sáenz et al. (2007)
EBNT (BCS) 3.16D(2004-2005) 0.9D (2004-2005) Riosmena-Rodríguez et al. (2010)
Gracilaria subsecundata AEP (SIN) 0.18D (1998-1999) 0.19D (1998-1999) Ruelas-Inzunza & Páez-Osuna (2006)
Gracilaria vermiculophylla BMGD (BCS) 1.40D (2004-2005) 0.84D (2004-2005) Talavera-Sáenz et al. (2007)
EBNT (BCS) 1.36D (2004-2005) 0.8D (2004-2005) Riosmena-Rodríguez et al. (2010)
UR (SIN) 3.9D (2002-2003) Soto-Jiménez et al. (2008)
LCHT (SIN) 5D (2002-2003) Soto-Jiménez et al. (2008)
Gracilaria sp. AEP (SIN) 0.23D (1998-1999) 4.9D (1998-1999) Ruelas-Inzunza & Páez-Osuna (2006)
AEP (SIN) 0.23D (1999-2000) 4.9D (1999-2000) Ruelas-Inzunza & Páez-Osuna 2008
Zostera marina LSI (BCS) 6.2D (2000) 8.8D (2000) Macías-Zamora et al. (2008)
LOL (BCS) 1.6D (2000) 14.9D (2000) Macías-Zamora et al. (2008)
BMGD (BCS) 1.09D (2004-2005) 1.23D (2004-2005) Talavera-Sáenz et al. (2007)
Ruppia maritima EBNT (BCS) 4.5D (2004-2005) 2.15D (2004-2005) Riosmena-Rodríguez et al. (2010)
BMGD (BCS) 4.52D (2004-2005) 2.12D (2004-2005) Talavera-Sáenz et al. (2007)
Caulerpa sertularioides UR (SIN) 0.14D (2006) 2.45D (2006) Jara-Marini et al. (2008)
Echhornia crassipes RLM (MEX) 4.32D (2006) Tejeda et al. (2010)
Hydrocoyle ranunculoides CARL (MEX) 5.27D (2010) Zarazúa et al. (2013)
Thalassia testudinum LYLH (YUC) 0.72D (2005-2006) Avelar et al. (2013)
Polysiphonia AEP (SIN) 0.87D (1998-1999) 3.1D (1998-1999) Ruelas-Inzunza & Páez-Osuna (2006)
Bivalves
Crassostrea corteziensis UR (SIN) 0.27D (2006) ST 1.14D (2006) ST Jara-Marini et al. (2008)
UR (SIN) 2.6D (2003-2004) ST 11.5D (2003-2004) ST Frías-Espericueta et al. (2005)
AEP (SIN) 6.4D (2004-2005) ST 8.36D (2004-2006) Frías-Espericueta et al. (2008)
UR (SIN) 4.9D (2002-2003) M Soto-Jiménez et al. (2008)
AEP (SIN) 6.47D (2008) ST 2.11D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
BBP (SON) 3.2W (2004-2005) ST 0.5W (2004-2005) ST García-Rico et al. (2010)
LTB (SON) 0.42D (2009) ST 3.18D (2009) ST Jara-Marini et al. (2013)
LCL (SIN) 7.65D (2008) ST 0.74D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
INM (SIN) 3.72D (1996) ST Páez-Osuna et al. (2002)
SMR (SIN) 9.02D (2008) ST 1.64D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
BCT (SIN) 7.11D (1996) S Páez-Osuna et al. (2002)
BCT (SIN) 4.27D (2008) ST 0.96D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
AEP (SIN) 7.2D (1999-2000) ST 3.4D (1999-2000) ST Ruelas-Inzunza & Páez-Osuna 2008
UR (SIN) 1.45D (2008) ST 1.36D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
SMOT (SIN) 5.56D (2008) ST 0.3D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
BYV (SON) 2.50D (1996) ST Páez-Osuna et al. (2002)
BAP (SON) 6.82D (1996) ST Páez-Osuna et al. (2002)
BOH (SIN) 2.50D (1996) ST Páez-Osuna et al. (2002)
SMR (SIN) 5.32D (1996) ST Páez-Osuna et al. (2002)
AEP (SIN) 7.62D (1996) ST Páez-Osuna et al. (2002)
PMZ (SIN) 7.42D (1996) ST Páez-Osuna et al. (2002)
LHCM (SIN) 5.22D (1996) ST Páez-Osuna et al. (2002)
TPAB (NAY) 3.63D (1996) ST Páez-Osuna et al. (2002)
LMXT (NAY) 5.10D (1996) ST Páez-Osuna et al. (2002)
LSCL (NAY) 2.33D (1996) ST Páez-Osuna et al. (2002)
NVT (JAL) 4.72D (1996) ST Páez-Osuna et al. (2002)
LBN (JAL) 4.83D (1996) ST Páez-Osuna et al. (2002)
INM (SIN) 6.4D (2006-2007) ST 4.8D (2006-2007) ST Frías-Espericueta et al. (2009)
SMR (SIN) 5.8D (2006-2007) ST 5.3D (2006-2007) ST Frías-Espericueta et al. (2009)
AEP (SIN) 5.01D (2006-2007) 5.7D (2006-2007) ST Frías-Espericueta et al. (2009)
BCT (SIN) 6.9D (2006-2007) ST 8.1D (2006-2007) ST Frías-Espericueta et al. (2009)
UR (SIN) 1.5D (2006-2007) ST 6.5D (2006-2007) ST Frías-Espericueta et al. (2009)
LHCM (SIN) 5.9D (2006-2007) ST 4.2D (2006-2007) ST Frías-Espericueta et al. (2009)
INM (SIN) 8.39D (2008) ST 0.65D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
ERY (SIN) 0.64D (2008) ST 1.51D (2008) ST Páez-Osuna & Osuna-Martínez (2015)
TPBA (SIN) 3.6D (2006-2007) ST 9.4D (2006-2007) ST Frías-Espericueta et al. (2009)
BCT (SIN) 5D (N/E) ST 0.46D (N/E) ST Osuna-Martínez et al. (2011)
Crassostrea gigas LCL (SIN) 5.1D (N/E) ST 1.85D (N/E) ST Osuna-Martínez et al. (2011)
CSNR (SON) 0.76W (1997) ST 0.5W(1997) ST García-Rico & Ramos-Ruiz (2001)
LTB (SON) 0.38D (2009) ST 2.35D (2009) ST Jara-Marini et al. (2013)
AEP (SIN) 12.1D (N/E) ST 1.42D (N/E) ST Osuna-Martínez et al. (2011)
BCT (SIN) 8.6D (N/E) ST 1.11D (N/E) ST Osuna-Martínez et al. (2011)
SMR (SIN) 11.55D (N/E) ST 0.92D (N/E) ST Osuna-Martínez et al. (2011)
CSNR (SON) 5.5D (N/E) ST 1.3D (N/E) ST Vázquez-Boucard et al. (2014)
CSNL (SIN) 3.4D (N/E) ST 2.2D (N/E) ST Vázquez-Boucard et al. (2014)
Crassostrea virginica LSA (TAM) 2.27D (2000) ST 0.802D (2000) ST Vázquez-Sauceda et al. (2005)
LTM (CAM) 2.55D (2002) ST Gold-Bouchot et al. (2007)
LMDG (VER) 2.2D (2003-2004) ST 5.84D (2003-2004) ST Guzmán-García et al. (2009)
LTMH (VER) 11.8D (2004) ST 0.5D (2004) ST Lango-Reynoso et al. (2010)
LSA (TAM) 2.27D (2000) ST 0.802D (2000) ST Vázquez-Sauceda et al. (2011)
LTM (CAM) 0.0295W (N/E) ST 0.1445W (N/E) ST Aguilar-Ucán et al. (2014)
LMCN (TAB) 42.23D (2007) ST 189.78D (2007) ST Castañeda-Chávez et al. (2014)
RPJ (TAB) 2.33D (2011) ST 0.8D (2011) ST Castañeda-Chávez et al. (2014)
RPL (CAM) 3D (N/E) ST Aguilar et al. (2012)
RCHP (CAM) 3.2D N/E) ST Aguilar et al. (2012)
Crassostrea iridescens PMZ (SIN) 2.3D (1995-1996) ST 2.3D (1995-1996) ST Soto-Jiménez et al. (2001)
Megapitaria squalida BKK (SON) 0.4W (2003) ST 0.001W (2003) ST García-Hernández et al. (2005)
BPZ (BCS) 5.57D (2003) ST 2.5D (2003) ST Méndez et al. (2006)
AEP (SIN) 3.2D (2004-2005) ST 7.7D (2004-2005) ST Frías-Espericueta et al. (2008)
BPZ (BCS) 7D (N/E) ST 4.02D (N/E) ST Cantu-Medellin et al. (2009)
BLRT (BCS) 4.66D (2004) ST 0.03D (2004) ST Cadena-Cárdenas et al. (2009)
BPZ (BCS) 0.93W (N/E) ST Escobedo-Fregoso et al. (2010)
Mytilus edulis LSLQ (BCS) 2.42D (2004) ST 0.27D (2004) ST Cadena-Cárdenas et al. (2009)
LSRL (BCS) 4.05D (2004) ST 5.8D (2004) ST Cadena-Cárdenas et al. (2009)
Mytella strigata AEP (SIN) 6.3D (2004-2005) ST 5.22D (2004-2005) ST Frías-Espericueta et al. (2008)
UR (SIN) 0.22D (2006) ST 1.72D (2006) ST Jara-Marini et al. (2008)
UR (SIN) 3.1D (2002-2003) M Soto-Jiménez et al. (2008)
INM (SIN) 1.91D (1996) ST 13.18D (1996) ST Osuna-López et al. (2009)
AEP (SIN) 1.75D (1996) ST 17.42D (1996) ST Osuna-López et al. (2009)
UR (SIN) 0.73D (1996) ST 11.11D (1996) ST Osuna-López et al. (2009)
BCT (BCT) 0.82D (1996) ST 9.39D (1996) ST Osuna-López et al. (2009)
LMXT (NAY) 0.75D (1996) ST 11.21D (1996) ST Osuna-López et al. (2009)
LSCL (NAY) 0.72D (1996) ST 8.58D (1996) ST Osuna-López et al. (2009)
Mytilus californianus ICND (BCN) 9.86D (1989-1990) M Segovia-Zavala et al. (2004)
PBND (BCN) 17D (1989-1990) ST Segovia-Zavala et al. (2004)
Chione californiensis BKK (SON) 0.4W (2003) ST 0.001W (2003) ST García - Hernández et al. (2005)
GSC (SON) 0.42D (2006) ST 9.2D (2006) ST Cadena-Cárdenas et al. (2009)
Chione fluctifraga LTB (SON) 0.54D (2009) ST 2.17D (2009) ST Jara-Marini et al. (2013)
Chione gnidia LTB (SON) 0.52D (2009) ST 3.27D (2009) ST Jara-Marini et al. (2013)
BGY (SON) 2.29D (N/E) ST 0.85D (N/E) ST Méndez et al. (2002)
Chione sp. PAGC (SON) 0.8D (1998-2000) ST 1.6D (1998-2000) ST García - Hernández et al. (2001)
Pinna rugosa BKK (SON) 2.44W (2003) ST 0.001W (2003) ST García - Hernández et al. (2005)
Anadara multicostata BKK (SON) 8.16W(2003) ST 0.001W (2003) ST García - Hernández et al. (2005)
Corbicula sp. CLSNR (SON) 0.4D (1998-2000) ST ND (1998-2000) ST García - Hernández et al. (2001)
RCL (SON) 0.4D (1998-2000) ST 2D (1998-2000) ST García - Hernández et al. (2001)
Hexaplex erythrostomus BKK (SON) 5.15W (2003) ST 0.48W (2003) ST García-Hernández et al. (2005)
Corbicula fluminea ECZ (VER) 0.1D (2005) ST Ruelas-Inzunza et al. (2007)
Mytilopsis sallei BCHM (ROO) 0.86D (2002) ST 1.24D (2002) ST Díaz López et al. (2006)
Argopecten ventricosus PCHG (BCS) 1.7D (1998-2000) ST 3.34D (1998-2000) ST Sobrino-Figueroa et al. (2007)
Fistulobalanus dentivarians LTB (SON) 0.72D (2009) ST 2.97D (2009) ST Jara-Marini et al. (2013)
Lampsilis tampicoensis LTJ (TAB) 0.18W (2008) ST 4.96W (2008) ST Pérez-Cruz et al. (2013)
RSPT (TAB) 0.25W (2008) ST N/D (2008) STT Pérez-Cruz et al. (2013)
Potamilus alata LGM (TAB) 0.33W (2008) ST N/D (2008) ST Pérez-Cruz et al. (2013)
Polymesoda caroliniana ECZ (VER) 1.15D (2005) ST Ruelas-Inzunza et al. (2007)
ECZ (VER) 0.6D (2006) ST Ruelas-Inzunza et al. (2007)
Polymesoda arctata RSPSP (TAB) 0.5W (2008) ST 2.06W (2008) ST Pérez-Cruz et al. (2013)
Lampsilis tampicoensis RNJ (TAB) 0.16W (2008) ST 2.58W (2008) ST Pérez-Cruz et al. (2013)
RPJ (TAB) 0.44W (2008) ST 0.76W (2008) ST Pérez-Cruz et al. (2013)
Crustaceans
Penaeus vannamei AEP (SIN) 3.48D (1998-1999) M 0.74D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2004a)
AEP (SIN) 3.1D (1999-2000) M 0.5D (1999-2000) M Ruelas-Inzunza & Páez (2008)
AEP (SIN) 0.36D (2006) M 4.89D (2006) M Frías-Espericueta et al. (2009)
LVCH (SIN) 0.66D (2003) M 2.3D (2003) M Frías-Espericueta et al. (2005)
LLRL (NAY) 0.59D (2003) M 1.4D (2003) M Frías-Espericueta et al. (2005)
PPCD (NAY) 0.65D (2003) M 2D (2003) M Frías-Espericueta et al. (2005)
LMXT (NAY) 0.62D (2003) M 1.5D (2003) M Frías-Espericueta et al. (2005)
LHCM (SIN) 0.7D (2003) M 2.4D (2003) M Frías-Espericueta et al. (2005)
LHCM (SIN) 0.39D (2006) M 4.21D (2006) M Frías-Espericueta et al. (2009)
SMR (SIN) 0.44D (2006) M 5.18D (2006) M Frías-Espericueta et al. (2009)
AEP (SIN) 0.4D (2006) M 5.52D (2006) M Frías-Espericueta et al. (2009)
INM (SIN) 0.40D (2006) M 5.62D (2006) M Frías-Espericueta et al. (2009)
TPAB (SIN) 0.7D (1998-1999) M 6.93D (1998-1999) M Frías-Espericueta et al. (2009)
AEP (SIN) 0.45D (1998-1999) M 0.40D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2004a)
AEP (SIN) 0.89D (2003) M 4.5D (2003) M Frías-Espericueta et al. (2005)
AEP (SIN) 0.5D (1999-2000) M 0.9D (1999-2000) M Ruelas-Inzunza & Páez (2008)
Penaeus setiferus CCMP (CAM) 3.64D (1997) M 4.22D (1997) M Vázquez et al. (2001)
LAV (VER) 0.05D (200) M 0.5D (200) M Lango-Reynoso et al. (2013)
Litopenaeus setiferus LTM (CAM) ND (N/E) ND (N/E) Aguilar-Ucán et al. (2014)
Farfantepenaeus californiensis AEP (SIN) 4.94D (1998-1999) M 0.54D (1998-1999) M Ruelas-Inzunza & Páez-Ozuna (2004a)
Farfantepenaeus aztecus LTMH (VER) 0.032D (2004) M 0.12D (2004) M Palomarez-García et al. (2009)
LTMH (VER) 0.04D (200) M 0.05D (200) M Lango-Reynoso et al. (2013)
Paleomonetes paludosus BBCN (SON) 0.4D (1998-2000) T ND (1998-2000) T García - Hernández et al. (2001)
Callinectes similis LSPT (TAB) 0.12D (2009) M Mendoza-Carranza et al. (2016)
Callinectes arcuatus UR (SIN) 23D (2002-2003) M Soto-Jiménez et al. (2008)
Callinectes sapidus LTM (CAM) 0.05W (N/E) 0.34W (N/E) Aguilar-Ucán et al. (2014)
Macrobrachium acanthurus LSPT (TAB) 0.72D (2009) M Mendoza-Carranza et al. (2016)
Panulirus gracilis PMZ (SIN) 0.4D (1995-1996) M 1.55D (1995-1996) M Morales-Hernández et al. (2004)
Procambarus clarkii CSC (SON) 0.2D (1998-2000) T 1.8D (1998-2000) T Gracia-Hernández et al. (2001)
Fish
Pterygoplichthys pardalis RUSMT (TAB) 0.31D (N/E)M Maldonado-Enríquez et al. (2015)
Cyprinus carpio CSC (SON) ND (1998-2000) T 1.1D (1998-2000) T García-Hernández et al. (2001)
Achirus mazatlanus LBN (JAL) 0.08D (2014) M 0.7D (2014) M Aguilar-Betancourt et al. (2016)
Sciades guatemalensis LBN (JAL) 0.08D (2014) M 0.7D (2014) M Aguilar-Betancourt et al. (2016)
Syacium gunteri CCMP (CAM) 0.001D (1997) M 1.66D (1997) M Vázquez et al. (2001)
Ariopsis guatemalensis LTPL (GRO) 2.25D (2011) M 5.27D (2011) M Rodríguez-Amador et al. (2014)
LTPL (GRO) 1.28D (2012) M 6.58D (2012) M Rodríguez-Amador et al. (2014)
Ariopsis assimilis BCHM (ROO) ND (1999) M 0.90D (1999) M García-Ríos & Gold-Bouchot (2002)
BCHM (ROO) ND (2000) M ND (2000) M García-Ríos & Gold-Bouchot (2002)
Ictalurus punctatus ECZ (VER) 0.001D (2006) M Ruelas-Inzunza et al. (2007)
Gerres cinereus LSTN (VER) 0.2D (2005) M Ruelas-Inzunza et al. (2007)
ECZ (VER) 1.88D (2005) M Ruelas-Inzunza et al. (2007)
Dormitators latifrons LTPL (GRO) 9.6D (2011) M Rodríguez et al. (2012)
Oreochromis aureus PSLT (SIN) 0.28D (2004-2005) M 2.12D (2004-2005) M Frías-Espericueta et al. (2010)
Oreochromis sp. ECZ (VER) 2.24D (2005) M Ruelas-Inzunza et al. (2007)
Diapterus sp. PMZ (SIN) 0.32D (2004-2005) M 2.8D (2004-2005) M Frías-Espericueta et al. (2010)
Gambusia affinis RLC (SON) ND (1998-2000) T 1.4D (1998-2000) T García-Hernández et al. (2001)
CSC (SON) ND (1998-2000) T ND (1998-2000) T García-Hernández et al. (2001)
CDOC (SON) 0.2D (1998-2000) T 0.3D (1998-2000) T García-Hernández et al. (2001)
RHD (SON) ND (1998-2000) T 0.90D (1998-2000) T García-Hernández et al. (2001)
Poecilia lapitina CSC (SON) 0.1D (1998-2000) T 1.3D (1998-2000) T García-Hernández et al. (2001)
Mugil cephalus CCP (SON) ND (1998-2000) T 1.9D (1998-2000) T García-Hernández et al. (2001)
AEP (SIN) 0.3D (1999-2000) M 1D (1999-2000) M Ruelas-Inzunza & Páez (2008)
UR (SIN) 3.3D (2002-2003) M Soto-Jiménez et al. (2008)
PMZ (SIN) 0.31D (2004-2005) M 2.62D (2004-2005) M Frías-Espericueta et al. (2010)
INM (SIN) 0.23D (2006) M 1.95D (2006) M Frías-Espericueta et al. (2011)
SMLR (SIN) 0.13D (20069 M 1.66D (2006) M Frías-Espericueta et al. (2011)
AEP (SIN) 0.14D (2006) M 2.1D (2006) M Frías-Espericueta et al. (2011)
BCT (SIN) 0.17D (2006) M 1.53D (2006) M Frías-Espericueta et al. (2011)
UR (SIN) 0.16D (2006) M 1.24D (2006) M Frías-Espericueta et al. (2011)
LHCM (SIN) 0.16D (2006) M 1.38D (2006) M Frías-Espericueta et al. (2011)
TPAB (SIN) 1.7D (2006) M 1.58D (2006) M Frías-Espericueta et al. (2011)
Mugil curema LBN (JAL) 0.08D (2014) M 0.7D (2014) M Aguilar-Betancourt et al. (2016)
ECZ (VER) 2.1D (2006) M Ruelas-Inzunza et al. (2007)
Centropomus viridis LSTN (VER) 1.8D (2005) M Ruelas-Inzunza et al. (2007)
ECZ (VER) 2.5D (2005) M Ruelas-Inzunza et al. (2007)
ECZ (VER) 0.001D (2006) M Ruelas-Inzunza et al. (2007)
Lutjanus analis CCMP (CAM) 0.001D (1997) M 4.68D (1997) M Vázquez et al. (2001)
Lutjanus colorado AEP (SIN) 0.2D (1999-2000) M 1.3D (1999-2000) M Ruelas-Inzunza & Páez (2008)
Cynoscion xanthulus AEP (SIN) 0.9D (1999-2000) M 2.6D (1999-2000) M Ruelas-Inzunza & Páez (2008)
Thrichurus nitens ECZ (VER) 3.7D (2005) M Ruelas-Inzunza et al. (2007)
Scomberomorus sierra PMZ (SIN) 0.27D (2004-2005) M 2.33D (2004-2005) M Frías-Espericueta et al. (2010)
Paraneetroplus synspilus LSPT (TAB) 0.14D (2009) M Mendoza-Carranza et al. (2016)
Paraneetroplus bifasciatus LSPT (TAB) 0.41D (2009) M Mendoza-Carranza et al. (2016)
Amphilophus robertsoni LSPT (TAB) 0.26D (2009) M 0.28D (2009) M Mendoza-Carranza et al. (2016)
Rocio octofasciata LSPT (TAB) 0.55D (2009) M Mendoza-Carranza et al. (2016)
Cichlasoma salvini LSPT (TAB) 0.28D (2009) M 0.68D (2009) M Mendoza-Carranza et al. (2016)
Sharks and rays
Carcharhinus limbatus PVCZ (VER) 0.35W (1994-1995) M 2.51W (1994-1995) M Núñez-Noriega (2005)
Carcharhinus falciformis BTS (SON) 0.37W (2014) M Terrazas-López et al. (2016)
Prionace glauca PBLCH (BCS) 0.2W (2011) M 0.07W (2011) M Barrera-García et al. (2012)
Isurus oxyrinchus IMGD (BCS) 0.0001D (2008) M 0.16D (2008) M Vélez-Alvares et al. (2013)
Rhizoprionodon terraenovae PVCZ (VER) 0.34W (1994-1995) M 3.31W (1994-1995) M Núñez-Noriega (2005)
Turtles
Chelonia mydas PDBC (BCS) 0.06W (2005-2007) S Labrada-Martagón et al. (2011)
CBCF (BCS) 0.01D (N/E) M 0.01D (N/E) M Gardner et al. (2006)
BMGD (BCS) 0.03W (2005-2007) S Labrada-Martagón et al. (2011)
CFN (SON) 0.99D (2008) S Ley-Quiñonez et al. (2013)
Caretta caretta CBCF (BS) 0.10D (N/E) M 0.01D (N/E) M Gardner et al. (2006)
PLM (BCS) 1.8W (N/E) S Ley-Quiñonez et al. (2011)
Lepidochelys olivacea BCT (SON) 2.6D (2005) M 8.9D (2005) M Frías-Espericueta et al. (2006)
CBCF (BCS) 0.48D (N/E) M ND (N/E) M Gardner et al. (2006)
PSCLL (OAX) 0.24D (2005-2006) H Páez-Osuna et al. (2010a)
PSCLL (OAX) 0.45D (2005-2006) S Páez-Osuna et al. (2010a)
PSCLL (OAX) 1.08D (2005-2006) E Páez-Osuna et al. (2010b)
PSCLL (OAX) 0.95D (2005-2006) S Páez-Osuna et al. (2010b)
PSCLL (OAX) 1.16W (2012) S 0.02W (2012) S Cortez-Gómez et al. (2014)
BGSB (SIN) 1.33W (2011) S ND Zavala-Norzagaray et al. (2014)
Eretmochelys imbrincata CBCF (BCS) 1.02D (N/E) M 0.38D (N/E) M Gardner et al. (2006)
Birds
Phalacrocorax brasilianus AEP (SIN) 1.2D (1999-2000) M 1.7D (1999-2000) M Ruelas-Inzunza & Páez (2008)
Pelecanus occidentalis AEP (SIN) 0.7D (2000) M 4.2D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
CBCF (BCS) 0.20W (2012-2013) H Ceyca et al. (2016)
AEP (SIN) 0.7D (1999-2000) M 4.2D (1999-2000) M Ruelas-Inzunza & Páez (2008)
Phalacrocorax olivaceus AEP (SIN) 1.2D (2000) M 1.7D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Fulica americana AEP (SIN) 1.4D (2000) M 4.1D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Recurvirostra americana AEP (SIN) 1.2D (2000) M 4.8D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Dendrocygna autumnalis AEP (SIN) 1.3D (2000) M 1.8D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Anas cyanoptera AEP (SIN) 1.3D (2000) M 1.4D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Sula nebouxii CBCF (BCS) 0.26W (2012-2013) H Ceyca et al. (2016)
Sula leucogaster CBCF (BCS) 0.32W (2012-2013) H Ceyca et al. (2016)
Phalacrocorax auritus CBCF (BCS) 0.33W (2012-2013) H Ceyca et al. (2016)
Aythia affinis AEP (SIN) 1.2D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Dendrocygna bicolor AEP (SIN) 0.2D (2000) M 2.8D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Plagadis chihi AEP (SIN) 1.3D (2000) M 2.5D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Charadrius vociferus AEP (SIN) 1.6D (2000) M 5.7D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Casmerodius albus AEP (SIN) 1.4D (2000) M 0.9D (2000) M Ruelas-Inzunza & Páez-Osuna (2004b)
Zenaida macroura DRC (SON) 0.44D (N/E) H 0.20D (N/E) H García - Hernández et al. (2006)
Athene cunicularia DRC (SON) 0.13D (N/E) H 0.06D (N/E) H García - Hernández et al. (2007)
Cistothorus palustris DRC (SON) 0.78D (N/E) H 0.07D (N/E) H García - Hernández et al. (2008)
Sula leucogaster SMR (SIN) 0.05D (2010-2012) S 0.3D (2010-2012) S Lerma et al. (2016)
Crocodiles
Crocodylus moreletti RCHPT (CAM) 63.8D (2011) B Trillanes et al. (2014)
LPNCLT (CAM) 64.8D (2012) B Trillanes et al. (2014)
RHND (ROO) 16.04W (2012) B Buenfil-Rojas et al. (2015)
RHND (ROO) 7.85W (2012) S Buenfil-Rojas et al. (2015)

EU: Estero Urías; AEP: Altata-Ensenada del Pabellón; BTS: Bahía Todos Santos; BGY: Bahía Guaymas; EBNT: Estero Banderitas; CSNR: Costa de Sonora; CSNL: Costa de Sinaloa; GNYR: Granjas Nayarit; BBP: Bahía de Bacochibampo; INM: Laguna San Ignacio-Navachiste-Macapule; BCT: Bahía de Cueta; PAGC: Parte alta del Golfo de California; PCHG: Pichiligue; BBCN: Bocana; BLRT: Bahía de Loreto; GYEMP: Guaymas-Empalme LTM: Laguna de Términos; LTB: Laguna El Tobari; LSLQ: San Luquitas; SMR: Santa María- La Reforma; LCL: El Colorado; ERY: Estero El Rey; LCHP: Lago de Chapala; GSC: Golfo de Santa Clara; LHCM: Laguna Huizache-Caimanero; LGM: Laguna Guasimo; LSI: Laguna de San Ignacio; BKK: Bahía de Kuu Kaak; LOL: Laguna Ojo de Liebre; BGMS: Bahía Las Guácimas; LAV: Laguna Alvarado; LYLH: Laguna Yalahau; BBP: Bacochibampo; BTBP: Bahía de Topolobampo; BAP: Laguna Agiabampo; BOH: Bahía de Ohuria; PPCD: Pescadero; BCHC: Bachoco; CSC: Ciénega Santa Clara; BMGD: Bahía Magdalena; LLRL: Los Laureles; CLSNR: Canal Sonora; PLM: Puerto López Mateos; DRC: Delta del Río Colorado; LBN: Laguna Barra de Navidad; SBRB: Santa Bárbara; RPL: Río Palizada; RCHP: Río Chumpán; BTPB: Bahía de Topolobampo; BYV: Laguna de Yavaros; BCMCH: Boca Camichín; BCHM: Bahía Chetumal; BPZ: Bahía La Paz; PLL: Presa Luis León; LSPT: Laguna de San Pedrito; CSDR: Cañón del sumidero; MTCL: Mercado de Tecuala; RCL: Río Colorado; PSLT: Presa el Salto; RCDLR: Río Candelaria; BCY: Bahía La Choya; BGSB: Guasabe; ESBL: Estero de San Blas; LCTC: Lago de Catemaco; ICND: Islas Coronado; BLB: Bahía de Lobos; RMYR: El Mayor; RUSMT: Río Usumacinta; TCPN: Teacapán; PVM: Presa Viejo Mandín; CCP: Cucapa; LSTN: Laguna Ostión; MTTN: Minatitlán; RSTG: Río Santiago; LMCN: Lago Mecoacán; TLCP: Tlacotalpan; URTCP: Urías-Teacapán; PVCZ: Puerto de Veracruz; LTJ: Laguna Tasajera; CSPT: Cospita; CBCF: Baja California; LTMH: Laguna de Tamiahua; PSCLL: Playa La Escobilla; PBLCH: Punta Belcher; NVT: Nuevo Vallarta; PBND: Punta Banda; LSRL: Laguna de Santa Rosalía; LVCH: Verde Camacho; LMXT: Laguna de Mexcaltitlán; PMZ: Puerto de Mazatlán; DTLL: Dautillos; CDOC: El Doctor; RNJ: Río Naranjos; PCHL: Puerto Chale; CARL: Curso Alto de Río Lerma; RCHPT: Río Champotón; CCMP: Costa de Campeche; LPNCLT: Los Petenes-Celestún; RSPSP: Río San Pedro y San Pablo RSPT: Río San Pedrito; RHND: Río Hondo; PAA: Presa Antonio Alzate; CFN: Infiernillo; RLM: Río Lerma; RPJ: Río Pantoja; LSA: Laguna de San Andrés; LTPL: Laguna Tres Palos; LMDG: Laguna Mandinga. SON: Sonora; SIN: Sinaloa; NAY: Nayarit; JAL: Jalisco; COL: Colima; MIC: Michoacán; GRO: Guerrero; OAX: Oaxaca; CHP: Chiapas; CAM: Campeche; ROO: Quintana Roo; YUC: Yucatán; TAB: Tabasco; VER: Veracruz; TAM: Tamaulipas; BCS: Baja California Sur; BCN: Baja California Norte; AGU: Aguascalientes; MEX: México; CMX: Ciudad de México. N/E: not specified; ND: not detect; -: not analized;

Ddry weight;

Wwet weight;

M: muscle; ST: soft tissue; T: whole body; S: blood; B: biopsy; H: eggs.

The use of teleost fish as biomonitors of aquatic pollution is also of great importance. These fish are found in virtually all aquatic ecosystems throughout the world, and many species can be considered integrators of ecological conditions, especially those closest to the highest levels of the food chain. Since they perform the function of transferring energy from the low to the high levels of the trophic networks of aquatic ecosystems (Van der Oost et al., 2003), they are a good mirror of the health of the ecosystem (Sedeño-Díaz & López-López, 2012). Fish are the organisms most frequently consumed by humans, especially those in high trophic levels and by bioaccumulating heavy metals (such as Cd, Pb Hg), they passed them on to consumers and can cause both acute (poisoning) and chronic diseases, most of which are not yet fully understood. Unlike bivalves, fish as biomonitors of aquatic pollution is more widespread throughout the Mexican territory, including coastal and inland ecosystems. The present review shows that pollution monitoring studies have used different species of fish belonging to different trophic levels and with different eating habits, including planktivorous fish (sardines), detritivorous fish (lizas), omnivorous fish (catfish), carnivorous-piscivorous fish (mojarras, snooks, snappers), carnivorous-benthic fish and major pelagic fish. The most used species were the lizas (Mugilidae), probably due to their commercial importance in Mexico (Frías-Espiricueta et al., 2011). This genus of fish is one of the most used around the world in aquatic monitoring studies (Waltham et al., 2013), since they are directly associated with sediments, allowing to evaluate the transfer of pollutants from this environmental matrix to the first levels of the trophic chain. Other commercially important fish that have been used in Mexico are snooks, mojarras, and snappers. Other organisms belonging to different trophic levels have also been used for biomonitoring purposes, including crustaceans, sharks, rays, macroalgae (which also have a high commercial value), sea turtles, birds, crocodiles, and mammals.

Mercury in biota

Table 1 shows the average concentrations of Hg found in various tissues of aquatic organisms in Mexico. The average values of Hg in macrophytes were 0.02-0.09 μg g−1 dw (dry weight) for Gracilaria sp., and 0.05 μg g−1 dw for Ulva lactuca, both cases in the Gulf area of California. No references for the presence of Hg in macrophytes were found in other areas of the country. Similar concentrations have been reported in other areas around the world. Qiu & Wang (2016) reported concentrations of 0.04 μg g−1 dw in U. fasciata in Daya Bay in southern China. Pereira et al. (2008) reported average Hg values of 0.04-0.34 μg g−1 dw in Gracilaria sp. in Ria de Aveiro, Portugal. Akcali & Kucuksezgin (2011) reported a much higher average Hg (53-72 μg g−1 dw) in Ulva sp. found in Turkey's Aegean coast.

Regarding mollusks, its use has increased in the Gulf of California area. We found 15 studies focused on important ecosystems on the Gulf of California's coastal area during 1997-2011 (sampling year) that used the genus Crassostrea species. These studies reported average values of Hg of 0.05-0.9 μg g−1 dw, EL Colorado Lagoon being the site with the highest concentrations (0.54 μg g−1 dw in 2008 and 0.93 μg g−1 dw in an undetermined date), and the Urías Lagoon with the lowest concentrations (0.05 μg g−1 dw in 2006 and 0.17 μg g−1 dw in 2008). It is known that there are difficulties when comparing the levels of metals in mollusks of different species or different geographical areas since the concentrations can vary depending on the metabolism, age, gonadal stage, habitat (freshwater, marine; lagoons, estuaries, mangroves), sampling season, among others. Thus, the comparison of pollution levels between different mollusk species must be made with reservations (Ruelas-Inzunza et al., 2014).

There is little information on the content of Hg in Crassostrea in other areas of the country. Benítez et al. (2012) reported concentrations <0.001 μg g−1 dw in Crassostrea virginica collected in the Terminos Lagoon, in Campeche. Aguilar et al. (2012) reported concentrations of 0.5, 0.7, and 1.1 μg g−1 dw in C. virginica collected in the Palizada, Candelaria, and Chumpán rivers, in the state of Campeche, respectively. No other studies with Crassostrea were found in other areas of the country during the review period. However, Hicks et al. (1976), in Villanueva & Botello (1992), reported concentrations of 0.05 μg g−1 dw in C. virginica collected in the Terminos Lagoon. Chione bivalves were also used to assess the concentration of Hg in coastal areas of the Gulf of California, Kuu Kaak Bay, in the state of Sonora, was where the lowest concentration was found (<0.001 μg g−1 dw; 2003), while the highest concentration was found in El Tobari lagoon (0.47 μg g−1 dw; 2009). Studies conducted on Mytilopsis sallei in Chetumal Bay, in Quintana Roo, reported values of 1.09 μg g−1 dw (2002), the highest reported values in Mexico during the review period. The only studies on Hg's concentration in bivalves of inland ecosystems were made with the genus Corbicula. One study was conducted in the Colorado River, in Sonora, and another in the Coatzacoalcos River, in Veracruz. The values reported were <0.04 and 0.09 μg g−1 dw, respectively. Hg's concentration values reported in Mexico's bivalves are similar to those reported by other authors in other parts of the world. For example, Astudillo et al. (2005), in Ruelas-Inzunza et al. (2013a), reported Hg values of 0.04 μg g−1 dw in Crassostrea sp. collected in the Gulf of Paria, Venezuela. Vaisman et al. (2005), in Ruelas-Inzunza et al. (2014), reported values of 0.04, 0.05, 0.08, and 0.15 μg g−1 dw in Crassostrea rhizophorae collected in the Pacoti estuary, the Coco estuary, and Ceara estuary in Brazil, respectively. Zorita et al. (2007), in Ruelas-Inzunza et al. (2013a) reported values of 0.23 μg g−1 dw in Mytilus galloprovincialis collected in the northeast of the Mediterranean Sea. Concerning inland ecosystems, Neufeld (2010), and Faria et al. (2010), in Ruelas-Inzunza et al. (2014), reported Hg values of 1.89 and 2.3 μg g−1 dw in Corbicula fluminea collected in the Norte river in the USA and the Ebro river in Spain, respectively.

The content of Hg in crustaceans was evaluated mainly in marine organisms. Concerning inland ecosystems, the only cases found were those of Procambarus clarkii and Palaemonetes paludosus, collected in the state of Sonora, in the Colorado River, the Bocana Lagoon, and the Santa Clara swamp, with values of 0.40, 0.05, and 0.69 μg g−1 dw in the whole organism, respectively. These values are similar to others reported worldwide; for example, Li et al. (2015) reported Hg concentrations in Macrobrachium nipponense of 0.03, 0.04, and 0.03 μg g−1 dw in three reservoirs located in the central part of China. These values, however, are lower than concentrations found in other freshwater crustaceans collected in contaminated areas. For example, Higueras et al. (2006) reported values of Hg > 9.06 μg g−1 dw in the muscle of P. clarkii collected in an area impacted by mining activities in central Spain (Almaden), and Suárez-Serrano et al. (2010) reported Hg concentrations of 1.5 μg g−1 dw in P. clarkii collected in an area impacted by industrial waste in the Ebro river, Spain. Concerning marine crustaceans, Delgado-Álvarez et al. (2015a) monitored Hg's concentration in muscle tissue of Penaeus vannamei grown in aquaculture farms in the states of Sonora, Sinaloa, and Nayarit. They found concentration levels of 0.19, 0.31, and 0.45 μg g−1 dw respectively, similar to those found in P. vannamei by Ruelas-Inzunza et al. (2004) (0.2 μg g−1 dw) and Ruelas-Inzunza et al. (2011a) (0.42 μg g−1 dw) in the Altata-Ensenada del Pabellón Lagoon complex in the state of Sinaloa. Similar concentrations have been reported in other species of penaeids in this lagoon complex (Table 1), which suggests that these organisms have similar responses to Hg exposure. García-Hernández et al. (2015) conducted a monitoring study of Hg's concentration in crustaceans from thirteen coastal ecosystems in Sonora. Sinaloa's states focused on the Callinectes bellicosus crab, in which they found concentrations ranging from 0.07 up to 1.8 μg g−1 dw in muscle tissue. The highest concentrations were found in crabs from Santo Tomas Bay, with 1.82 μg g−1 dw. The mercury concentration in these ecosystems' sediments, determined in the same study, was <0.001 μg g−1, while the concentration in water (total fraction) was 5.2 μg L−1. The authors indicate the importance of the water matrix in the content of Hg in C. bellicosus; however, the highest concentrations of Hg in the water were found in the Guaymas-Empalme Bay, with 6.3 μg g−1, while the Hg concentrations in C. bellicosus were the lowest, with 0.56 μg g−1 dw. On the other hand, the highest Hg concentration in sediment was found in Las Guásimas Bay, with 1.23 μg g−1 dw, while the concentration in C. bellicosus was 0.63 μg g−1 dw showing the complex interaction between organisms and environmental pollutants.

Teleost fish are the most heterogeneous group of organisms used as biomonitors of aquatic pollution in Mexico. Marine and freshwater fish from different ecosystems (rivers, lakes, lagoons, estuaries, bays) and different eating habits (planktivorous, detritivorous, omnivorous, and carnivorous) have been used for this purpose. The present review shows that Hg concentration in fish may vary depending on the type of ecosystem, geographical location (anthropogenic or geological influence), eating habits (trophic level), and species. In the case of rivers, the highest concentration of Hg was found in muscle tissue of Lepomis macrochirus, in the Hardy river, with 3.2 μg g−1 dw, followed by Gobomorius polylepis in the Coatzacoalcos river, with 0.86 μg g−1 dw, then Pterygoplichthys pardalis in the Usumacinta River, with 0.45 μg g−1 dw, and Mugil sp., in the Santiago River, with 0.20 μg g−1 dw. Concerning lakes and other reservoirs, the highest concentrations of Hg were found in Lake Chapala in muscle tissue of Cyprinus sp., with 4.15 μg g−1 dw in 2007, 1.95 μg g−1 dw in 2010, 1.75 μg g−1 dw in 2011, and 0.5 μg g−1 dw in 2012. In other sites, such as the Luis León Dam, the concentration was 0.04 μg g−1 dw in 2011-2012, and not detected (ND) in the Viejo Mandin Dam in 2013.

Coastal ecosystems have a greater diversity of fish communities, harboring different trophic levels through which energy (and pollutants) is transferred within the same community. It is possible to observe an increase in the Hg levels in muscle from the lower trophic levels to higher levels. In the Urias Lagoon, for example, the concentration of Hg in muscle tissue increased from 0.1-0.18 μg g−1 dw in Mugil sp. to 0.7 μg g−1 dw in Eugerris axillaris and 0.9 μg g−1 dw in Lutjanus colorado; the latter two have a predator-prey relationship with Mugil sp., at least in their earlier stages (Jara-Marini et al., 2012). The same trend can be observed in other places, such as Altata-Ensenada del Pabellón, where Hg's concentration went from 0.13-0.20 μg g−1 dw in muscle tissue of M. cephalus to 0.89 μg g−1 dw in the muscle of L. colorado. In Santa Maria- La Reforma, the Hg concentration went from 0.13 μg g−1 dw in muscle tissue of M. curema to 0.82 μg g−1 dw in C. medius's muscle. In Topolobampo, the concentration Hg in muscle tissue of M. cephalus was 0.03 μg g−1 dw, increasing to 3.32 μg g−1 dw in the muscle of C. caninus. Other cases in which the level of mercury increased from lower to higher trophic levels were found in Guaymas (Sonora), Barra de Navidad Lagoon (Jalisco), and the estuary of the Coatzacoalcos River (Veracruz) (Table 1). There were also cases where the trend mentioned above was not clearly seen. In the Alvarado lagoon, for example, in Veracruz's state, the concentration of Hg in muscle tissue of M. curema was 2.85 μg g−1 dw (2003), while the concentration of Hg in C. parallelus was 0.75-0.9 μg g−1 dw (2000-2003). In general, top predators such as the great amberjack (Seriola lalandi), the striped marlin (Tetrapturus audax), the wahoo (Acanthocybium solandri), the blue marlin (Makaira mazara), and the Indo-Pacific sailfish (Istiophorus platypterus) had higher concentrations of mercury.

In coastal ecosystems, elasmobranchs are considered top predators, making them susceptible to pollutants' biomagnification such as mercury (Ruelas-Inzunza et al., 2013b). Most of the studies analyzed in this review focused on rays and sharks were conducted in the Gulf of California region. Among sharks, Sphyrna zygaena showed the highest average Hg concentration, with 33 μg g−1 dw in muscle for 2003-2004; however, other studies reported concentrations of 0.98 μg g−1 dw of Hg in muscle tissue of the same species in 2001-2005 (Table 1). Other species such as S. lewini, Prionace glauca, C. leucas, C. falciformis, and Rhizoprionodon longurio showed average concentrations of 0.49-4.32, 1.96-5.56, 0.2-2.48, 1.2-3.4, and 3.6-5.2 μg g−1 dw of Hg in muscle tissue, respectively. Regarding the other regions of Mexico, only one study was found for the Gulf of Mexico region; Núñez-Noriega (2005) analyzed the concentrations of Hg in muscle tissue of C. limbatus sampled in the port of Veracruz, finding average concentrations of 13.32 μg g−1 dw, higher than those found in C. limbatus from the Gulf of California (2.04 μg g−1 dw in muscle). Núñez-Noriega (2005) also analyzed the concentration of mercury in R. terraenovae, obtaining average values of 3.04 μg g−1 dw, which were lower than those found in similar species from the Gulf of California, such as R. longurio (5.2 μg g−1 dw of Hg in muscle).

The average concentration of mercury in the muscle tissue of the batoids (rays and torpedoes) was lower than the concentration found in sharks (approximately 1.23 and 4.01 μg g−1 dw of Hg, respectively), probably because sharks belong to a level highest trophic. Sharks feed mainly on fish, and batoids feed on organisms with lower trophic levels, such as crustaceans and mollusks and, to a lesser extent, on fish (Ruelas-Inzunza et al., 2013b), which could explain the differences in Hg levels. The highest concentrations were found in Dasyatis longa, with 2.84 μg g−1 dw, in 2003-2004, and 4.46 μg g−1 dw in 2012. Urolophus spp. batoid's muscle had concentrations of Hg in the muscle of 1.37-3.71 μg g−1 dw in 2012. The lowest concentrations were found in Mobula japanica in 2012, with 0.04-0.56 μg g−1 dw.

Other groups of aquatic animals that have also been used as biomonitors of aquatic pollution in Mexico include sea turtles, aquatic birds, crocodiles, and marine mammals. Table 1 shows the average mercury concentrations reported in sea turtles, aquatic birds, crocodiles, and marine mammals. Regarding aquatic birds, piscivorous species such as Pelecanus occidentalis and Phalacrocorax brasilianus had higher concentrations than non-piscivorous birds such as Anas discors and A. clypeata (Table 1). In Mexico, studies with aquatic reptiles such as sea turtles and crocodiles are very scarce. Only two studies with crocodiles were found, by Trillanes et al. (2014) and Buenfil-Rojas et al. (2015), who reported mercury concentrations of 3.1-4.3 μg g−1 dw in Crocodylus moreletti in the Champotón-Petenes-Celestún River, and of 0.33 μg g−1 ww in the Hondo River, respectively. Only three studies with sea turtles were found, one for the Gulf of California area (Chelonia mydas, C. caretta, and Lepidochelys olivacea), another for the Central Pacific area (L. olivacea), and another for the Gulf of Mexico area (C. mydas and Eretmochelys imbricata). Different tissues (muscle, egg, and blood) were used in these studies to evaluate the concentration of pollutants, which could serve as the basis for future research.

Cadmium and lead in biota

Table 2 shows the concentrations of Cd and Pb in aquatic organisms. As in the case of macrophytes, most of the studies about the presence of Cd and Pb in biota focused on the Gulf of California area, but a higher number of biomonitoring studies focused on Cd and Pb. Several sites along the Gulf of California coast were monitored using macrophytes, finding average concentrations of Cd of 0.14-6.2 μg g−1 dw, and 0.19-8.8 μg g−1 dw of Pb. The highest average concentrations of Cd were found in Rupia maritima (6.2 μg g−1 dw) collected in the San Ignacio Lagoon (Baja California Sur), while the lowest concentrations were found in Caulerpa sertularioides (0.14 μg g−1 dw) collected in the Urías Lagoon (Sinaloa). In Pb's case, the lowest average concentrations were found in Gracilaria subsecundata (0.19 μg g−1 dw) in Altata-Ensenada del Pabellón, while the highest concentrations were found in R. maritima (8.8 μg g−1 dw) collected in the San Ignacio Lagoon. There were also cases, such as those reported by Orduña-Rojas & Longoria-Espinoza (2006), in which average Pb concentrations of 174 μg g−1 dw was found in U. lactuca collected in the Ignacio-Navachiste Lagoon (Sinaloa), suggesting the possible influence of the small fishing boats used in the region. Of the sites evaluated in the coastal area of the Gulf of California, the ones with the lowest concentrations of Cd and Pb, simultaneously, were the Guaymas bay with 0.54 and 0.35 μg g−1 dw, and Altata-Ensenada del Pabellón with 0.18 and 0.19 μg g−1 dw in G. subsecundata and U. lactuca, respectively, both species collected in the period 1998-1999. In general, the concentration of Cd and Pb varied from one species to another. For example, Riosmena-Rodríguez et al. (2010) reported concentrations of 3.16, 1.36, and 4.5 μg g−1 dw for Cd and 0.9, 0.8, and 2.15 μg g−1 dw for Pb in G. textorii, G. vermiculophylla, and R. maritima, respectively, collected in the Banderitas Estuary (Baja California Sur) in 2004-2005. Ruelas-Inzunza & Páez-Osuna (2006) reported concentrations of 0.18, 0.23, and 0.87 μg g−1 dw for Cd and 0.19, 4.9, and 3.1 μg g−1 dw for Pb in G. subsecundata, Gracilaria sp., and Polysiphonia sp., respectively, collected in Altata-Ensenada del Pabellón (Sinaloa) in 2004-2005. There were only a few other studies that used macrophytes in other areas of the country. Avelar et al. (2013) reported Cd concentrations of 0.72 μg g−1 dw in T. testudinum in the Yalahau Lagoon, an area with relatively little contamination in the Mexican Caribbean; however, the authors reported maximum concentrations of Cd higher than 5 μg g−1 dw in leaves of Thalassia testudinum, suggesting how important underground infiltration of contaminants is in this type of sites. It is thought that macrophytes reflect greater accuracy in the amount of contamination in the fraction dissolved in the water column (Orduña-Rojas & Longoria-Espinoza, 2006). Natural sources such as upwellings and hydrothermal chimneys (Riosmena-Rodríguez et al., 2010), or anthropic sources such as gasoline in fishing vessels (Soto-Jiménez et al., 2008), can significantly alter the content of metals in macrophytes.

Studies of the content of Cd and Pb in bivalves were the most abundant. Close to 30 sites on the Gulf of California's coastal area were studied using bivalves as biomonitors. The average concentrations of Cd and Pb were 0.22-17.23 and 0.001-17.4 μg g−1 dw, respectively; countrywide, the highest concentrations of both Cd and Pb were found in this area. The typically high Cd concentrations present in the Gulf of California area sites were mainly associated with upwelling events that occurred in the winter season. Phosphorus pesticides and fertilizers, used for more than 50 years in intensive agriculture in this area, have generated large quantities of residues rich in Cd and other metals, which have been deposited in the continental slope's sediments, and reintroduced to the coastal zone during upwelling events. The sites with the highest average Cd concentrations were Bacochibampo Bay and Kuu Kaak Bay, 22.54, and 57.12 μg g−1 dw, respectively; these two sites are frequently affected by upwelling events. As we have seen before, the ability to accumulate pollutants varies from one species to another; for example, García-Hernández et al. (2005) found Cd levels of 0.4, 0.4, 2.44, and 8.16 μg g−1 dw in Megapitaria squalida, Chione californiensis, Pinna rugosa and Anadara multicostata collected in the Kuu Kaak Bay (Sonora), respectively. The highest average concentrations of Pb in bivalves living on the coastal area of the Gulf of California were found mostly in sites with intense fishing activity, mainly in the Sinaloa coast, where the highest concentrations were associated with the fuel used by small fishing boats. Other studies that used bivalves were conducted in areas outside the Gulf of California. For example, Segovia-Zavala et al. (2004) reported concentrations of 17.23 μg g−1 dw of Cd in Mytilus californianus transplanted to Punta Banda (Baja California Norte), an area affected by upwelling events. Castañeda-Chavez et al. (2014) reported concentrations of 42 and 189 μg g−1 dw of Cd and Pb, respectively, in C. virginica collected in the Mecoacán Lagoon in the state of Veracruz, in an area historically impacted by the Petrochemical industry. Nearly 80% of the cases showed average concentrations of 0.2-6.9 μg g−1 dw for Cd and 0.001-6.8 μg g−1 dw for Pb, similar to values reported worldwide. For example, Lino et al. (2016) reported Cd concentrations of 0.15 and 0.6 μg g−1 dw in Perna perna from Sepitaba Bay and Cabo do Arraial, and 1.2 and 0.8 μg g−1 dw of Cd in Nodipecten nodosus from Ilha Grande Bay and Cabo do Arraial, in southern Brazil. Liu et al. (2017) reported average concentrations of 5.9-7.8 μg g−1 dw for Cd and 0.4-0.5 μg g−1 dw for Pb in muscle tissue of Mactra veneriformis in the Laizhou Bay in China. It is worth remembering that China and Brazil are countries with emerging economies and intense industrial activity. About 10% of the cases showed high concentrations of Pb and Cd: 10-34 μg g−1 dw and 10-57 μg g−1 dw for Cd, respectively. These atypically high concentrations were influenced by upwelling events, fishing activities, or contaminated urban or industrial effluents.

Average Cd and Pb levels in crustaceans are shown in Table 2. There were very few studies on the concentration of Cd and Pb in freshwater crustaceans. Mendoza-Carranza et al. (2016) evaluated Cd's concentration in muscle tissue of Macrobrachium acanthurus, finding values of 0.72 μg g−1 dw in the San Pedrito Lagoon, Tabasco, in the year 2009. Similarly, García-Hernández et al. (2001) found average whole-body concentrations of 0.2 and 0.4 μg g−1 dw for Cd and 0.001 and 1.8 μg g−1 dw for Pb in Procambarus clarkii and Palaemonetes paludosus. These values were lower than other values reported in other areas of the world for freshwater crustaceans. For example, Rabiul-Islam et al. (2017) reported values of 2.38 and 4.64 μg g−1 dw of Cd and Pb, respectively, in muscle tissue of M. rosenbergii collected in the Satkhira Basin in southern Bangladesh. In coastal ecosystems, the only studies found in this review focused on the Gulf of California and Mexico's Gulf. Lango-Reynoso et al. (2013) found concentrations of 0.05 and 0.4 μg g−1 dw for Cd and 0.5 and 0.5 μg g−1 dw for Pb in muscle tissue of Penaeus setiferus and Farfantepenaeus aztecus, respectively, in the Alvarado Lagoon (Veracruz). Vázquez et al., 2001 found concentrations of Cd and Pb of 3.64 and 4.22 μg g−1 dw, respectively, in muscle tissue of F. aztecus collected on the coast of Campeche. Aguilar-Ucán et al. (2014) reported concentrations of Cd and Pb of 0.25 and 1.7 μg g−1 dw, respectively, in muscle tissue of Callinectes sapidus collected in the Terminos Lagoon (Campeche). Soto-Jiménez et al. (2008) reported concentrations of Pb of 23 μg g−1 dw in muscle tissue of C. arcuatus collected in the Urías Lagoon (Sinaloa). No other studies were found for other blue crab species; however, several studies were conducted throughout Sinaloa and Nayarit using shrimp as biomonitors, with average muscle concentrations of 0.36-4.94 μg g−1 dw for Cd and 0.4-6.39 μg g−1 dw for Pb. In general, the concentration of Cd and Pb varied between different tissues. For example, Frías-Espericueta et al. (2009) reported values of 0.36-0.76 μg g−1 dw for Cd and 4.21-6.93 μg g−1 dw for Pb in muscle tissue of P. vannamei collected in six lagoons in the coastal zone of Sinaloa and Nayarit, while in hepatopancreas, they reported values of 1.10-7.97 μg g−1 dw for Cd and 5.45-18.84 μg g−1 dw for Pb. Similarly, Vázquez et al. (2001) reported values of 3.6 and 4.2 μg g−1 dw for Pb and Cd respectively in muscle tissue of P. setiferus, and 15.03 and 11.6 μg g−1 dw for Cd and Pb respectively in hepatopancreas, results that indicate the high capacity of this organ to bioaccumulate metals.

Table 2 shows the concentrations of Cd and Pb in fish. In general, the number of Cd and Pb biomonitoring studies in fish was considerably lower than Hg's biomonitoring studies. In the case of freshwater fish, the average concentrations of Cd in muscle tissue were 0.28-2.24 μg g−1 dw; for Pb, the average concentrations were <0.001-0.55 μg g−1 dw in ecosystems located in southeastern Mexico. The highest Pb concentrations were 9.6 μg g−1 dw in muscle tissue of Dormitator latifrons collected in the Tres Palos Lagoon, in state of Veracruz. Average levels of Cd and Pb of 0.28 and 2.12 μg g−1 dw, respectively, were also found in the muscle tissue of Oreochromis aureus collected in the Salto Dam (Sinaloa). Cd and Pb concentrations in marine fish's muscle tissue belonging to the lower trophic levels were lower than those found in crustaceans collected in the same areas. For example, Frías-Espiricueta et al. (2011) evaluated Cd and Pb's concentration in muscle tissue of Mugil cephalus collected in seven coastal lagoons located in the state of Sinaloa and found values of 0.13-0.26 and 1.38-2.10 μg g−1 dw, respectively. In the same sites, Frías-Espiricueta et al. (2009) reported levels of 0.36-0.76 and 4.21-6.93 μg g−1 dw for Cd and Pb, respectively, in muscle tissue of P. vannamei. Concerning predatory fish, Vázquez et al. (2001) reported values of <0.001 and 1.6 μg g−1 dw for Cd and Pb, respectively, in muscle tissue of Syacium gunteri. In muscle tissue of P. zetiferus, the same authors reported values of 3.6 and 4.2 μg g−1 dw; however, in the case of Lutjanus analis, the reported concentrations were <0.001 for Cd and 4.68 for Pb μg g−1 dw. Similarly, Ruelas-Inzunza & Páez-Osuna (2008) reported values of 3.1 and 0.5 μg g−1 dw for Cd and Pb in muscle tissue of P. vannamei, respectively, and 0.5 and 0.9 μg g−1 dw in P. stylirostris. In L. colorado and Cynoscion xanthulus, the reported Cd levels were 0.2 and 0.9 μg g−1 dw, while the values of and Pb were 1.3 and 2.6 μg g−1 dw, respectively. These results are consistent with the low transfer efficiency from lower to higher trophic levels, and even with the predator-prey ratio, at least in the case of fish.

The number of biomonitoring studies focused on Cd and Pb's concentration in elasmobranchs was considerably lower than the number of studies focused on mercury and other biomonitors. In the Gulf of California, the reported levels of Cd and Pb were <0.001-1.48 μg g−1 dw for Cd and 0.16-0.28 μg g−1 dw for Pb. In the Gulf of Mexico, the reported levels were 1.4-1.48 μg g−1 dw for Cd and 10.04-13.24 μg g−1 dw for Pb; it is worth noting that the latter value of Pb was approximately 40 times higher than the value found in the Gulf of California. As in other fish, the concentrations of Cd and Pb in the muscle tissue of sharks were not higher than the concentrations found in organisms of lower trophic levels. The tendency to bioaccumulate higher Cd and Pb concentrations in the liver than in muscle was also observed in sharks. Barrera-Garcia et al. (2013), for example, reported concentrations of Cd in the liver nearly 140 times higher than the concentrations reported in muscle by Barrera-Garcia et al. (2012). Terrazas-López et al. (2016) also reported Cd >900 times higher in the liver, probably due to the high content of lipids in the liver and to its ability to synthesize metallothioneins (rich in cysteine), which are present in lower quantities in the muscles. In general, Cd and Pb tended to bioconcentrate in the liver and to biodilute in muscle.

The concentration of Cd and Pb in sea turtles, waterfowl, and crocodiles is shown in Table 2. The average concentration of Cd in muscle tissue of sea turtles sampled in the Gulf of California ranged from 0.01 to 2.6 μg g−1 dw, while the average concentration of Pb ranged from not detect to 8.9 μg g−1 dw. In blood, Cd levels were ranged between 0.15 and 6.65 μg g−1 dw. In the central area of the Mexican Pacific, Cd levels ranged from 0.45 to 0.85 μg g−1 dw. The transfer of contaminants between mother and offspring is a current subject of study, but relatively little is known about the effect that mother-transmitted contaminants have on the offspring's development. Páez-Osuna et al. (2010a) found in Lepidochelys olivacea, that the maternal transfer of Cd was 0.20% of the Cd content in the whole body (for a spawn of 200 eggs). García-Hernández et al. (2006) evaluated the concentration of Cd and Pb in eggs and embryos (in different stages) of aquatic birds living in the Colorado River Delta (Sonora) and found concentrations of 0.13-0.78 and 0.06-0.20 μg g−1 dw for Cd and Pb respectively. Similarly, Ceyca et al. (2016) reported values of 1-1.6 μg g−1 dw for Cd in seabird eggs in the coastal zone of Sinaloa, similar values to those found in the muscle tissue of several seabirds collected in the Altata-Ensenada de Pabellón Lagoon (Sinaloa), with concentrations of 0.2-1.6 μg g−1 dw, which suggests that a high percentage of this contaminant is transferred via the mother.

Organochlorine pesticides (POCs) in aquatic organisms

The results of the average concentration of POCs in different aquatic organisms in Mexico are shown (Table 3). The number of biomonitoring studies of POCs was considerably lower than the number of heavy metals' biomonitoring studies. The most studied compound was ∑DDTs. In the case of marine mollusks, the highest concentrations (282 ng g−1 dw) were found in the soft tissue of Moluchia strigata collected in the San Ignacio-Navachiste-Macapule lagoon complex. The lowest concentrations (<0.01 ng g−1 dw) were found in C. californiensis collected in the lagoons Altata-Ensenada del Pabellon and Santa María-La Reforma.

Table 3 Average concentration of POCs (ng g−1 dw, D or ww, W or LW, L) in different tissues of organisms from various aquatic ecosystems in Mexico. 

Species Place DDTs HCHs Drines Endosulfanes Heptacloros Cite
Primary producers
Ruppia sp. LTSC (CAM) 59.6D (1988-89) 4.8D (1988-89) 51.3D (1988-89) ND (1988-89) 2D (1988-89) DG05
Nimphaea sp. LTSC (CAM) 19.7D (1988-89) 30D (1988-89) 313D (1988-89) ND (1988-89) 90D (1988-89) DG05
Halodule sp. LTSC (CAM) 193D (1988-89) 88D (1988-89) 1009D (1988-89) 129D (1988-89) 18D (1988-89) DG05
Mollusks
Mytella strigata AEP (SIN) 32.4D (1989) ST 2.9D (1989) ST 13.6D (1989) ST 0.07D (1989) ST C02
INM (SIN) 282D (1996) ST OL09
AEP SIN) 99D (1996) ST OL09
BCT SON) 147D (1996) ST OL09
UR (SIN) 12D (1996) ST OL09
LMXT (NAY) 4.8D (1996) ST OL09
LSCL (NAY) 69D (1996) ST OL09
Crassostrea virginica LTM (CAM) 9.1D (2002) ST 16.3D (2002) ST 22.4D (2002) ST GB07
LTMH (VER) 114L (2005) ST CC11
LVT (VER) 103L (2005) ST CC11
LAV (VER) 53L (2001-02) ST CC11
LMCH VER) 99L (2001-02) ST CC11
LMD (TAM) 22L (2008) ST 63L (2008) ST 355L (2008) ST 13L (2008) ST LR13
LMDG (VER) 89L (2008) ST 1614L (2008) ST 347L (2008) ST 136L (2008) ST LR13
LMCN (TAB) 20L (2009) ST 23L (2008) ST 57L (2008) ST 14L (2008) ST LR13
Crassostrea gigas AEP (SIN) 29D (1989) ST 0.7D (1989) ST 18.9D (1989) ST C02
GSNR (SON) 3D (N/E) ST 72D (N/E) ST VB14
GSNL (SIN) 1.1D (N/E) ST 44D (N/E) ST VB14
Crassostrea sp. LTM (CAM) 5.8D (N/E) ST 1.4D (N/E) ST 0.2D (N/E) ST 0.38D (N/E) ST 0.08D (N/E) ST C09
Chione sp. PNGC (SON) ND (1998-00) ST GH01
Corbicula sp. RCL (SON) 350D (1998-00) ST GH01
Corbicula sp. CLSNR (SON) 1050D (1998-00) ST GH01
Chione californiensis BYV (SON) 73D (2009) ST ND (2009) ST 33D (2009) ST ND (2009) ST 63D (2009) ST VG16
Chione californiensis AEP (SIN) ND (2009) ST ND (2009) ST 7D (2009) ST ND (2009) ST 8.19D (2009) ST VG16
Chione californiensis SMR (SIN) ND (2009) ST ND (2009) ST ND (2009) ST ND (2009) ST ND (2009) ST VG16
Chione subrogosa AEP (SIN) 2.3D (1989) ST 1.2D (1989) ST 7.5D (1989) ST 32.2D (1989) ST ND (1989) ST C02
Pomacea patula LCTC (VER) ND (1993) M ND (1993) M 96.5D (1993) M CV01
Crustaceans
Penaeus vannamei AEP (SIN) 1.1D (1989) M ND (1989) M 1.1D (1989) M 3D (1989) M ND (1989) M C02
Penaeus stylirostri AEP (SIN) 6.6D (1991) M 1.3D (1991) M 1D (1991) M 0.7D (1991) M C02
Penaeus sp. BOH (SIN) 0.02D (1995-96) M 0.17D (1995-96) M 1.06D (1995-96) M 0.14D (1995-96) M OF-R02
Litopenaeus sp. EPR (NAY) 26D (1996-97) M 21D (1996-97) M 28D (1996-97) M 25D (1996-97) M 18D (1996-97) M RM06
Litopenaeus sp. LCSL (NAY) 26D (1996-97) M 42D (1996-97) M 4.6D (1996-97) M 45D (1996-97) M 0.01D (1996-97) M RM06
Callinectes sp. ERCZ (VER) 2.5D (2006) M 15D (2006) M ER12
Callinectes bellicosus BYV (SON) ND (2012) M 355D (2012) M 405D (2012) M 340D (2012) M ND (2012) M GH15
BAP (SON) 180D (2012) M ND (2012) M 425D (2012) M 855D (2012) M 130D (2012) M GH15
BLB (SON) ND (2012) M 195D (2012) M ND (2012) M ND (2012) M 310D (2012) M GH15
BOH (SIN) ND (2012) M 41D (2012) M ND (2012) M 1035D (2012) M 100D (2012) M GH15
Callinectes rathbunae LGVT (VER) 267L (2008) M LR13
Procambarus clarki RMYR (SON) 135D (1998-00) T GH01
CCP (SON 300D (1998-00) T GH01
CSC (SON) 50D (1998-00) T GH01
Paleomonetes paludosus BBCN (SON) ND (1998-00) T GH01
Fishes
Mugil cephalus AEP (SIN) 20D (1991) M 3.5D (1991) M 1.4D (1991) M 4.6D (1991) M ND (1991) M C02
ERCZ (VER) 0.98D (2006) M 1.6D (2006) M GM10
ERCZ (VER) 1D (2006) M 2.5D (2006) M ER12
INM (SIN) 155D (2010-11) M 1015D (2010-11) M 625D (2010-11) M 215D (2010-11) M 75D (2010-11) M RM13
CSC (SON) 250D (1998-00) T GH01
Arius melanopus LTSC (CAM) 116D (1999) M 26D (1999) M 509D (1999) M 49D (1999) M 300D (1999) M DG05
Lepisosteus tropicus LTM (CAM) 15D (N/E) M C09
Cyprinus carpio PAL (NAY) 1.9D (2004) M ND (2004) M 7.1D (2004) M 1.5D (2004) M ND (2004) M AZ11
CSC (SON) 275D (1998-00) T GH01
PVG (CHH) 1245D (2004) M 27D (2004) M ND (2004) M UM08
Eugerris axillaris ERCZ (VER) 0.5D (2006) M 11D (2006) M ER12
ERCZ (VER) 0.49D (2006) M 12.8D (2006) M GM10
Oreochromis aureus PAL (NAY) 0.5D (2004) M ND (2004) M 3D (2004) M 4.3D (2004) M ND (2004) M AZ11
Oreochromis niloticus XNH (CAM) 16739L (2011) M 335L (2011) M 473L (2011) M 376L (2011) M HG16
PVG (CHH) 155D (2004) M 30.5D (2004) M ND (2004) M UM08
Oreochromis sp. ERCZ (VER) 1D (2006) M 1.5D (2006) M ER12
ERCZ (VER) 0.99D (2006) M 2D (2006) M GM10
LMTT (HID) 4D (2001) M 20D (2001) M 0.5D (2001) M 6D (2001) M 1.5D (2001) M FB08
LMTT (HID) 4D (2002) M 1.2D (2002) M 1.5D (2002) M 1.5D (2002) M 43D (2002) M FB08
Centropomus parallelus ERCZ (VER) 0.5D (2006) M 6.5D (2006) M ER12
ERCZ (VER) 0.5D (2006) M 7.5D (2006) M GM10
Arius felis ERCZ (VER) 1D (2006) M 2D (2006) M ER12
ERCZ (VER) 0.99D (2006) M 1.9D (2006) M GM10
Poecilia latipinna RCL (SON) 1300D (1998-00) T GH01
CSC (SON) 1350D (1998-00) T GH01
Ictalurus punctatus RHD (SON) 100D (1998-00) T GH01
CCP (SON) 875D (1998-00) T GH01
PVG (CHH) 1060D (2004) M 16.5D (2004) M ND (2004) M UM08
PAL (NAY) ND (2004) M 3.8D (2004) M 7.6D (2004) M 0.18D (2004) M ND (2004) M AZ11
Micropterus salmoides PAL (NAY) ND (2004) M 0.1D (2004) M 3.6D (2004) M 3.5D (2004) M 0.5D (2004) M AZ11
PVG (CHH) 865D (2004) M 22.5D (2004) M 60D (2004) M UM08
Gambusia affinis RMYR (SON) 1600D (1998-00) T GH01
CSC (SON) 300D (1998-00) T GH01
CDOC (SON) 850D (1998-00) T GH01
Dorosoma petenense LCTC (VER) 6.5D (1993) M ND (1993) M 33.5D (1993) M CV01
Cichlasoma urophthalmus MCU (CAM) 19047L (2011) M 442L (2011) M 521L (2011) M 405L (2011) M HG16
Lepomis macrochirus RHD (SON) 310D (2010) M DL (2010) M 60D (2010) M ND (2010) M ND (2010) M GH13
Lutjanus argentiventris INM (SIN) 40D (2012-13) M 120D (2012-13) M 15D (2013-13) M 50D (2013-13) M 40D (2013−13) M GG15
Lutjanus novemfasciatus INM (SIN) ND (2012-13) M 190D (2012-13) M 15D (2013-13) M 45D (2013-13) M 30D (2013-13) M GG15
Lutjanus colorado INM (SIN) 50D (2012-13) M 115D (2012-13) M 20D (2013-13) M 75D (2013-13) M 40D (2013-13) M GG15
Euthynnus lineatus ZCO (OAX) 31D (2010-11) M 16.5D (2010-11) M 18D (2010-11) M 43D (2010-11) M 15D (2010-11) M MV14
Thunnus albacares ZCO (OAX) 22.5D (2010-11) M 7.5D (2010-11) M ND (2010-11) M 30.5D (2010-11) M 14D (2010-11) M MV14
Sarda orientalis ZCO (OAX) 6D (2010-11) M ND (2010-11) M 9.5D (2010-11) M ND (2010-2011) M 12.5D (2010-11) M MV14
Coryphaena hippurus ZCO (OAX) 60D (2010-11) M ND (2010-11) M 18D (2010-11) M 55D (2010-11) M 14D (2010-11) M MV14
Sharks
Sphyrna lewini ZCO (OAX) 4.4D (2010-11) M 5.6D (2010-11) M 5.6D (2010-11) M ND (2010-11) M 16D (2010-11) M MV14
Carcharhinus leucas ZCO (OAX) 9.6D (2010-11) M 8.4D (2010-11) M 4.5D (2010-11) M ND (2010-11) M 6D (2010-11) M MV14
Turtles
Chelonia mydas BPZ (BCS) 7W (N/E) M 4.8W (N/E) M 2W (N/E) M 3.8W (N/E) M G02
PAO (BCS) 0.7W (2005-07) S 2.8W (2005-07) S 3.4W (2005-07) S ND (2005-07) S 8.6W (2005-07) S LM11
BMGD (BCS) ND (2005-07) S 11W (2005-07) S 10W (2005-07) S ND (2005-07) S 4.5W (2005-07) S LM11
PXN (CAM) 14L (N/E) S 4.3L (N/E) S 17L (N/E) S 12L (N/E) S 2L (N/E) S GB14
PXN (CAM) 729L (N/E) H 335L (N/E) H 1470L (N/E) H 672L (N/E) H 78L (N/E) H GB14
Lepidochelys olivacea BPZ (BCS) 8.6W (N/E) M 14W (N/E) M 3W (N/E) M 14W (N/E) M G02
Caretta caretta BPZ BS) 3W (N/E) M 3W (N/E) M 3W (N/E) M 3W (N/E) M G02
Eretmochelys imbricata SCY (CAM) 25L (N/E) S 6.6L (N/E) S 17L (N/E) S 9L (N/E) S 19L (N/E) S GB14
Eretmochelys imbricata SCY (CAM) 8066L (N/E) H 665L (N/E) H 4818L (N/E) H 1132L (N/E) H 1284L (N/E) H GB14
Birds
Athene cunicularia DRC (SON) 48W (N/E) H 14W (N/E) H 0.5W (N/E) H 8.26W (N/E) H GH06
Zenaida macroura DRC (SON) 61W (N/E) H 32W (N/E) H 3.7W (N/E) E 2.7W (N/E) H GH06
Sula leucogaster SGJ (SON) 53W (2006) H M09
SPMT (SON) 52W (2006) H M09
SIF (SIN) 34W (2006) H M09
IISB (NAY) 38W (2006) H M09
IMT (JAL) 49W (2006) H M09
IPR (JAL) 22W (2006) H M09
IPB (COL) 12W (2006) H M09
IMP (MCH) 14W (2006) H M09
Pandion haliaetus LSI (BCS) 0.9W (2001) S 0.4W (2001) S 2.3W (2001) W 0.09W (2001) S 0.2W (2001) H RR-RE11
Phalacrocorax sp. AEP (SIN) 5824D (1991) M 284D (1991) M 13.5D (1991) M 1.2D (1991) M C02
AEP (SIN) 12047D (1991) H 1200D (1991) H 45D (1991) H 1.1D (1991) H C02
Mammals
Delphinus capensis BGY (SON) 18000L (1999) B GR14
Zalophus californianus GCFR (N/A) 2750L (2005-06) B 35L (2005-06) B NT07
Crocodiles
Crocodylus moreletti CHPTN (CAM) 1800L (2005-06) S 550L (2005-06) S ND (2005-06) S GJ12

UR: Estero Urías; AEP: Altata- Ensenada del Pabellón; GCFR: Golfo de California; BGY: Bahía Guaymas; GSNR Granjas de Sonora; GSNL: Granjas de Sinaloa; INM: Laguna San Ignacio-Navachiste-Macapule; BCT: Bahía de Cueta; BBCN: Bocana; LTM: Laguna de Términos; SMR: Santa María- LA Reforma; PNGC: Parte Norte del Golfo de California; PXN: Punta Xen; LSI: Laguna de San Ignacio; PAO: Punta Abreojos; LAV: Laguna Alvarado; LVT: Laguna Vega de La Torre; BAP: Laguna Agiabampo; BOH: Bahía de Ohuria; CSC: Cienega Santa Clara; BMGD: Bahía Magdalena; SCY: Sacubay; CLSNR: Canal Sonora; DRC: Delta del Río Colorado; LTSC: Laguna de Terminos - Sistema Candelaria-Panlau; LSCL: Laguna San Cristóbal; LMD: Laguna Madre; EPR: Estero Pozo del Rey; BYV: Laguna de Yavaros; LGVT: Laguna Grande- Laguna Vega de La Torre; BPZ: Bahía La Paz; ERCZ: estero del Rio Coatzacoalcos; RCL: Río Colorado; LCTC: Lago de Catemaco; SGJ: San Jorge; SPMT: San Pedro Mártir; SIF: San Ildefonso; IISB: Isla Isabel; IMT: Isla Marieta; ICND: Islas Coronado; BLB: Bahía de Lobos; RMYR: El Mayor; ZCO: Zona Costera de Oaxaca; IPR: Isla Pajarera; IPB: Isla Peña Blanca; CCP: Cucapa; LMCN: Lago Mechoacán; LMTT: Lago Metztitlán; IMP: Morro El Postosí; LTMH: Laguna de Tamiahua; LMCH: Laguna de la Mancha; LMXT: Laguna de Mexcaltitlan; XNH: Xnoha; MCU: Mocu; CDOC: El Doctor; CHPTN: Río Champoton-Los Petenes; PVG: Presa Vicente Guerrero; PAL: Presa Agua Limpia; RHD: Rio Hardy; LMDG: Laguna Mandinga.DG05: Díaz-González et al. (2005); C02: Carvalho et al. (2002); GB07: Gold-Bouchot et al. (2007); C09: Carvalho et al. (2009); OL09: Osuna-López et al. (2009); CC11: Castañeda-Chavez et al. (2011); LR13: Lango-Reynoso et al. (2013); VB14: Vazquez-Boucard et al. (2014); GH01: Garcia-Hernández et al. (2001); VG16: Vargas-Gonzales et al. (2016); GH15: García-Hernández et al. (2015); GM10: Gonzalez-Mille et al. (2010); ER12: Espinosa-Reyes et al. (2012); RM13: Reyes-Montiel et al. (2013); GG15: Granados-Galván et al. (2015); MV14: Martínez-Villa et al. (2014); FB08: Fernández-Bringas et al. (2008); UM08: Uresti-Marín et al. (2008); AZ11: Aranguré-Zúniga et al. (2011); HG16: Hinojosa-Garro et al. (2016); GH13: García-Hernández et al. (2013); CV01: Calderon-Villagomez et al. (2001); G02: Gardner et al. (2003); LM11: Labrada-Martagón et al. (2011); GB14: García-Besné et al. (2014); GH06: García-Hernández et al. (2006); M09: Mellink et al. (2009); RR-RE11: Rivera-Rodríguez & Rodríguez-Estrella (2011); GR14: Gallo-Reinoso et al. (2014); NT07: Niño-Torres et al. (2009); GJ12: González-Jauregui et al. (2012); RM06: Robledo-Marenco et al. (2006); C09: Carvalho et al. (2009). SON: Sonora; SIN: Sinaloa; NAY: Nayarit; JAL: Jalisco; COL: Colima; MIC: Michoacán; GRO: Guerrero; OAX: Oaxaca; CHP: Chiapas; CAM: Campeche; ROO: Quintana Roo; YUC: Yucatán; TAB: Tabasco; VER: Veracruz; TAM: Tamaulipas; BCS: Baja California Sur; BCN: Baja California Norte; AGU: Aguascalientes; MEX: Mexico; CMX: Ciudad de México. N/E: not specified; ND: not detect, -: not analized;

Ddry weight;

Wwet weight; M: muscle; ST: soft tissue; T: whole body; S: blood; B: biopsy; H: eggs.∑DDTs: refers to the sum of Dichlorodiphenyltrichloroethane (DDT), DDE (dichlorodiphenyldichloroethylene), and DDD (dichlorodiphenyldichloroethane). ∑HCHs: refers to the sum of Alpha-hexachlorocyclohexane (α-HCH), beta-hexachlorocyclohexane (β-HCH), gamma-hexachlorocyclohexane (γ-HCH), delta-hexachlorocyclohexane (δ-HCH). ∑Drines: refers to the sum of Dialdrine, Aldrine, endrine, endrin aldehyde, endrin ketone. ∑Endosulfans: refers to the sum of Endosulfan I, Endosulfan II, Endosulfan sulfate. ∑Heptachlors: refers to the sum of Heptachlor, heptachor hepoxide.

In the case of freshwater mollusks, Corbicula sp. collected in the Colorado River had average concentrations of 350-1050 ng g−1 dw. The highest ∑DDTs (50-300 ng g−1 dw) concentrations in crustaceans were found in P. clarkii collected at different sites and the Colorado River system. García-Hernández et al. (2015) conducted a biomonitoring study of POCs in several coastal lagoons of southern Sonora and northern Sinaloa, using C. bellicosus biomonitor. They found average concentrations of <0.01-180 ng g−1 dw of ∑DDTs, <0.01-355 ng g−1 dw of ∑HCHs, <0.01-405 ng g−1 dw of ∑Drines, <0.01-1035 ng g−1 dw of ∑Endosulfans, and <0.01-310 ng g−1 dw of ∑Heptachlor. The authors point out that these concentrations are relatively high and may be associated with the intense agricultural activity in the area and pesticides to control infectious vectors.

In the case of fish, the species associated with sediments showed high concentrations of POCs. Uresti-Marín et al. (2008), for example, found average ∑DDT concentrations of 1060 and 1245 ng g−1 dw in muscle tissue of Ictalurus punctatus and Cyprinus carpio collected in the Vicente Guerrero Dam (Chihuahua), respectively. Similarly, García-Hernández et al. (2001) reported average whole-body concentrations of 875 ng g−1 dw of ∑DDTs in I. punctatus collected in the Colorado River area. Furthermore, Reyes-Montiel et al. (2013) found average ∑HCH concentrations of 1015 ng g−1 dw in muscle tissue of M. cephalus from the San Ignacio-Navachiste-Macapule lagoon system. There were very few cases showing the behavior of POCs in the predator-prey relationship. In muscle tissue of M. cephalus, Reyes-Montiel et al. (2013) found average concentrations of 155 ng g−1 dw of ∑DDTs, 625 ng g−1 dw of ∑Drines, 215 ng g−1 dw of ∑Endosulfans, and 75 ng g−1 dw of ∑Heptachlor. Granados-Galván et al. (2015) reported average concentrations of <0.01 −50 ng g−1 dw of ∑DDTs, 115-190 ng g−1 dw of ∑HCHs, 15-20 ng g−1 dw of ∑Drines, 45-75 ng g−1 dw of ∑Endosulfans, and 30-40 ng g−1 dw of ∑Heptachlor in three species of snappers. Both studies were conducted in the San Ignacio-Navachiste-Macapule lagoon system in the period 2011-2013. No biomagnification was observed, which may be related to the different detoxification rates of the various species. Moreover, low concentrations of POCs were observed in large pelagic fish, including sharks.

In marine mammals, a large amount of adipose tissue in them, their large size, longevity, and high trophic level allows them to bioaccumulate huge POCs amounts. Gallo-Reinoso et al. (2014), for example, found maximum concentrations of 87,300 ng g−1 lw (lipid weight) in biopsies of Delphinus capensis, while Niño-Torres et al. (2009) found maximum concentrations of 11,000 ng g−1 lw in a biopsy of Zalophus californianus. The transfer of POCs via the mother became evident in sea turtles and aquatic birds. Average concentrations of 12-61 ng g−1 ww were found in seabird eggs collected throughout the Mexican Pacific. Carvalho et al. (2002) found higher levels of ∑DDTs, ∑HCHs, ∑Drines, and ∑Endosulfans in eggs in the muscle and liver tissue of Phalacrocorax sp. García-Besné et al. (2014) reported concentrations of POCs hundreds of times higher in eggs of E. imbricata and C. mydas than in blood. However, long-term effects on the embryo exposure to these contaminants via the mother have not been thoroughly studied yet.

Effect of PBTSs on aquatic organisms and human health

The effect of acute exposure to many substances on different aquatic organisms (micro and macroinvertebrates, fish, reptiles, amphibians, birds, and mammals) has been well studied. Despite this, the effect of such exposure on wild organisms is not yet well known, mainly due to the technical complexity of the field experiments, and to the fact that, in the vast majority of cases, the concentrations in which the pollutants occur in different environmental matrices are barely noticeable, which means their effects are not observable in the short term. However, these compounds' bioaccumulation in different tissues reveals chronic exposure to wild organisms.

The concentration of contaminants in different tissues can be correlated with direct observations made in the field (biometric, reproductive and behavioral, among others), or compared with reference values for residual concentrations in tissue or tissue residue guidelines (TRG), which establish the maximum concentration (quantitatively) of a substance in different tissues (including food) that is recommended for wildlife protection (CCME, 1998). These TRGs are based on many field and laboratory experiments and aim to link measurements made in wild organisms with robust experimental toxicological information to predict the populations under study's potential risks.

This review shows the reported concentrations of the main PBTS in many aquatic species (Tables 13). Weng & Wang (2017) found that Cd concentrations between 17-27 μg g−1 dw in Crassostrea hongkongensis were associated with low fertility rates and slow larval growth compared to organisms sampled at reference sites. In the present review, we found that, in 93% of cases, Cd's average concentration in bivalves was 0.2-17 μg g−1 dw, reaching up to 22, 28, 36, 42, and 57 μg g−1 dw in particular sites and dates. Wiener et al. (2003) indicated that Hg concentrations of 6-20 μg g−1 ww in muscle tissue of adult fish were associated with sublethal effects, including behavioral alterations, brain lesions, and deterioration of gonadal development.

All cases of Hg in fish muscle reviewed here were below this concentration. In birds, Ceyca et al. (2016) indicated that Hg concentrations of 0.5-1 μg g−1 ww in sea bird eggs could cause mortality, malformations, and neurological damage. Ceyca et al. (2016) also reported maximum Hg values of 0.55-187 μg g−1 ww in eight species of seabirds collected on the coast of Sinaloa. Zhang et al. (2013) reported that the lowest probable adverse effect (LOAEL) of Hg on aquatic birds' blood occurred at 0.73 μg g−1 ww. Lerma et al. (2016) reported Hg values of 1.1 ppm dw in the blood of Sula leucogaster collected on the coast of Sinaloa.

Niño-Torres et al. (2009) reported that DDT values <980,000 μg g−1 lw in fatty tissue of marine mammals were associated with premature deliveries, while PCB concentrations <17 μg g−1 lw in fatty tissue could cause endocrine disruption and immunosuppression. Gallo-Reinoso et al. (2014) reported DDT concentrations of 21 μg g−1 lw in the biopsy of a common dolphin sampled in the Gulf of California. Regarding TRGs, the Canadian Council of Ministers of the Environment (CCME) establishes a reference value of 0.033 μg g−1 ww for Hg in food for all wildlife that consumes aquatic organisms. The reference value for ∑DDTs is set at 14 ng g−1 ww in food. In the present work, we found that 41% of bivalves, 76% of crustaceans, 76% of fish, and 96% of sharks and rays exceeded the limit for Hg, while 15% of bivalves, 26% of crustaceans, and 40% of fish exceeded the limit for ∑DDTs. These results show the risks that wildlife face in aquatic ecosystems in Mexico.

The potential risk to human health from the consumption of PBTS through food consumption of aquatic origin is a global concern. Various diseases have been associated with exposure to low concentrations of contaminants, such as cancer, neurotoxicity, cardiovascular diseases, endocrine disruption, and immunological disorders (Dórea, 2008). As a result, various national and international agencies have established maximum permissible limits, seeking to protect consumers from the adverse effects of consuming toxic residues. The USEPA, for example, establishes maximum permissible limits of 1 and 0.1 μg g−1 ww for Cd and Hg in fish, respectively. The European Community (EC) establishes maximum permissible of 1, 0.5, and 0.5 μg g−1 ww for Hg, Cd, and Pb in fish muscle, respectively. In contrast, the INECC (Mexico) establishes maximum permissible limits of 1, 0.5, and 1 μg g−1 ww for Hg, Cd, and Pb, respectively.

In the present review, we found that close to 90% of the cases of mollusks, crustaceans, fish, sharks, and rays did not involve average concentrations exceeding the limit of 0.5 μg g−1 ww for Hg. In the case of fish, only Caranx caninus collected in Topolobampo Bay, Sinaloa, in 2004, exceeded this limit, with a Hg concentration in the muscle of 1 μg g−1 ww. However, about 35% of shark cases exceeded this value, even exceeding the reference value of 1 μg g−1 ww for Hg. An extreme case involved a specimen of S. zygaena collected in the Gulf of California, with Hg levels exceeding 8 μg g−1 ww. In contrast, about 90% of fish, sharks, and crustaceans showed Cd levels in muscle lower than 0.5 μg g−1 ww. Regarding mollusks, about 45% of the organisms reviewed exceeded the limit of 0.5 μg g−1 ww for Cd, while 18% exceeded 1 μg g−1 ww, and close to 20% exceeded the limit of 1 μg g−1 ww for Pb. For ∑DDTs, the EC establishes a maximum permissible limit of 1000 ng g−1, while the Codex Alimentarius Guidelines of the Food and Agriculture Organization of the United Nations (USFDA) and the World Health Organization (WHO) establishes a maximum permissible limit of 5,000 ng g−1. All the cases reviewed in this work were below the limit of 1,000 ng g−1 for ∑DDTs.

The potential risk of fish consumption to human health can be evaluated considering a risk ratio (HQ) defined by the equation HQ = E / RfD (Newman & Unger, 2002); where RfD is the reference dose (in μg kg−1 kg−1 of weight d−1), and E is the level of exposure or consumption of the contaminant, which is calculated using the equation E = C × I / W, where C is the concentration of the contaminant (in μg g−1 ww), I is the per capita intake rate (in g d−1), and W is the average weight (in kg). Considering an RfD of 0.3, 0.5, 0.5, 1, and 3.5 for ∑HCHs, ∑DDTs, Hg, Cd, and Pb, respectively, I of 30 g d−1 for Mexicans consumers, and W of 70 kg, only in about 5% of cases does the value of HQ exceeds 1 for all contaminants. However, in some communities with high fish consumption rates, with an RfD of 200-400 g/d, the risk increases considerably, especially in infants and pregnant women (Zamora-Arellano et al., 2017; Astorga-Rodríguez et al., 2018).

CONCLUSIONS

This review synthesizes a large amount of information on the biomonitoring of the main PBTS in aquatic ecosystems in Mexico, and this information can serve as a basis for future research. In general, the levels of pollution found in Mexico's aquatic ecosystems are similar to those found in other regions of the world. However, given Mexico's enormous ecological wealth, especially its aquatic ecosystems, there is insufficient information on environmental pollutants. Moreover, there is a great disparity in the amount of information available between the country's different areas. Just the Gulf of California concentrates about 80% of the studies reviewed here, which shows the need to increase research efforts in the country's currently neglected areas such as the Central Pacific or the Mexican Caribbean, whose participation in this work did not exceed 5%.

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Received: November 11, 2019; Accepted: July 21, 2020

Corresponding author: Adrián Tintos-Gómez, (atintos48@gmail.com)

Corresponding editor: Sergio Contreras

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