Jane L. Guentzel Enrique Portilla-Ochoa

Alejandro Ortega-Argueta Blanca E. Cortina-Julio

Edward O. Keith

THE ALVARADO LAGOON – ENVIRONMENT,IMPACT, AND CONSERVATION

In: "Lagoons: Biology, Management and Environmental Impact”

Editor: Adam G. Friedman

ISBN: 978-1-61761-738-6 2011

400 Oser Avenue, Suite 1600Hauppauge, N. Y. 11788-3619Phone (631) 231-7269Fax (631) 231-8175E-mail: Main@novapublishers.comhttp://www.novapublishers.com

Science Publishers, Inc.OVAN

In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6

Editor: Adam G. Friedman, pp. 397-415 © 2011 Nova Science Publishers, Inc.

Chapter 14

THE ALVARADO LAGOON – ENVIRONMENT,

IMPACT, AND CONSERVATION

Jane L. Guentzel1*

, Enrique Portilla-Ochoa2,

Alejandro Ortega-Argueta2,3

, Blanca E. Cortina-Julio2

and Edward O. Keith 4**

1Department of Marine Science, Coastal Carolina University, Conway, SC, USA

2 Investigaciones Biologicas, Universidad Veracruzana, Xalapa, Ver., Mexico 3 Ambiente y Sustentabilidad, Instituto de Ecología, Xalapa, Ver., Mexico

4 Oceanographic Center, Nova Southeastern University, Ft. Lauderdale, FL , USA

ABSTRACT

The Alvarado Lagoon System (ALS) in south-central Veracruz State, Mexico, is a

mangrove dominated coastal wetland formed by the confluence of the Acula, Blanco,

Limon and Papaloapan rivers. The ALS has a maximum width of 4.5 km, a mean surface

area of 62 km2, and is connected to the Camaronera Lagoon by a narrow channel and to

the Gulf of Mexico (GOM) via a 0.4 km wide sea channel. Water samples were collected

during the wet (September 2005) and dry (March 2003 and 2005) seasons. Salinity

ranged from 1-25.5 psu and pH was slightly alkaline (7.6-8.6). Levels of total organic

carbon (TOC), total mercury (Hg), and total suspended solids (TSS) ranged from 3.9-20.9

mg C/L, 0.92-26.1 ng Hg/L, and 1-39.2 mg TSS/L, respectively. The strong correlation

(R2=0.71; P=0.001) between total mercury and TSS in the water column suggests that

particulate matter is a carrier phase for mercury within the Alvarado and Camaronera

Lagoons.

The ALS is one of the most productive estuarine-lagoon systems in the Mexican

GOM. Model studies suggest that primary production by sea grasses provides more

energy input to the ecosystem than detritus, which is contrary to most other Mexican

GOM lagoons and estuaries. In 2004 the ALS was nominated Ramsar site no. 1355

because of its important biodiversity, ecological attributes, and high resource production.

* Corresponding authors: Email: jguentze@coastal.edu

** edwardok@nova.edu

The license for this PDF is unlimited except that no part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

398

Over 100 fish species have been collected from the ALS, representing four ecological

guilds: marine stenohaline, marine euryhaline, estuarine, and freshwater fishes. These

assemblages have not experienced significant changes over the past 40 years, but there

has been a recent decline in diversity. Antillean manatees (Trichechus manatus manatus)

historically have occurred in the ALS but were reduced in the 1970s and 1980s by

hunting and are now considered endangered. The rescue of 6 orphan calves between 1998

and 2000 suggests that manatees are reinhabiting the ALS as a result of conservation

measures. Manatees are most commonly sighted in the Alvarado Lagoon, Acula River

and adjacent lagoons, and are rarely sighted in the Limon River and adjacent lagoons. To

protect the manatees and their habitat an educational program was developed in 1998 and

an assessment of their current status and critical habitat in the ALS was conducted. Our

manatee conservation efforts were recognized in 2001 when September 7th was officially

declared the ―National Day of the Manatee‖ in Mexico. Almost 350 species of birds

occur in the ALS, including the Mexican Duck (Anas diazi), which is undergoing a slow

but marked decline due to habitat destruction and overhunting. The largest threats to the

ALS include unsustainable sugar cane cultivation, cattle-ranching, coastal urban

development, oil and gas exploration and exploitation, water pollution by urban waste

and agricultural runoff, and increases in port and tourism industries. Despite the

establishment of government policy and measures to protect the coastal wetlands of ALS,

the identified threats continue to menace the important biodiversity and human well-

being of the region.

INTRODUCTION

The Alvarado Lagoon System (ALS) in south-central Veracruz state (Figure 1), Mexico,

is a large mangrove dominated coastal wetland located 70 km southeast of the Port of

Veracruz. It has a total area of 2800 km2 of which 258 km

2 are covered by water. The

Alvarado Lagoon (AL) is a shallow system (average depth 1.5 m) connected to the

Camaronera Lagoon by a narrow channel and to the Gulf of Mexico (GOM) via a 0.4 km

wide sea channel [Moran-Silva et al., 2005, Cruz-Escalona et al., 2007]. The AL has a

maximum width of 4.5 km and a mean surface area of 62 km2. The ALS is mainly formed by

the Alvarado, Buen Pais, Camaronera and Tlalixcoyan lagoons, but it is also associated with a

great number of smaller aquatic bodies, flood zones, and parts of the Acula, Blanco, Limon

and Papaloapan rivers. The Papaloapan River extends through the states of Oaxaca, Puebla

and Veracruz and traverses a distance of 445 km, passing through the city of Tlacotalpan and

finally emptying into the AL. The Papaloapan drainage basin covers an area of approximately

39,200 km2.

The ALS is one of the most productive estuarine-lagoon systems in the Mexican GOM

[Cruz-Escalona et al. 2007]. It is characterized by a large diversity of interactions with its

adjacent systems, particularly an extensive marsh, which contributes greatly to its biological

productivity. Seasonal changes are well pronounced and are mainly influenced by the

precipitation-drought regime conditions associated with its ecosystem. The ALS has three

separate zones based on physicochemical characteristics; Camaronera Lagoon, Buen Pais

Lagoon and the urban zone of Alvarado Lagoon, and the river zone of Alvarado Lagoon

[Moran-Silva et al., 2005].

Model studies suggest that primary production by sea grasses provides more energy input

to the ecosystem than detritus, which is the opposite of most other Mexican GOM lagoons

The Alvarado Lagoon – Environment, Impact, and Conservation

399

and estuaries. This may be a consequence of relatively rapid flushing (50 x 109 m

3 of water

each year), a short water exchange time (0.5 days), mangrove deforestation, and overfishing

[Cruz-Escalona et al., 2007]. The increase of anthropogenic activities in the surrounding

terrestrial areas coupled with limited waste management planning have contributed to both

local and regional deterioration of the hydrological characteristics of the ALS [Cruz-Escalona

et al., 2007].

Figure 1. Satellite photograph of the Alvarado Lagoon System showing the major lagoons and rivers of

the area. Image courtesy of the Consejo de Desarrollo del Papaloapan (CODEPAP, 2003), Xalapa, Ver.,

Mexico

ENVIRONMENT AND IMPACT

Mercury and Other Water Quality Parameters

We collected sediment, fish, and unfiltered water samples from the Alvarado Lagoon,

Lagoon Camaronera, and the Gulf of Mexico during the wet (September 2005) and dry

(March 2003 and 2005) seasons (Table 1). Water column pH values were slightly alkaline

(7.6-8.6) and the salinity ranged from 1-25.5 psu. Precipitation amounts for the dry season

months of March 2003 and March 2005 were 0.23 cm, and 2.79 cm, respectively, and the wet

season month of September 2005 was 272 cm. Salinity in the ALS was inversely correlated

with rainfall, with highest levels occurring in the dry season samples (March 2003 and 2005)

and lowest levels occurring in the wet season samples (September 2005) (Table 2). Our

salinity values are similar to the salinity ranges (1-14 psu) reported for the lagoon during the

2000-2001 wet, dry, and storm seasons [Moran-Silva et al., 2005]. Levels of nitrate (NO3-N

mg/L) during the 2000-2001 season ranged from 0.03-0.14 mg N/L [Moran-Silva et al.,

2005]. Our values for nitrate (NO3-N mg/L) during the 2003 dry season ranged from 0.73-2.3

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

400

mg NO3-N/L. These values are slightly higher than the 2000-2001 values and may be

indicative of increasing anthropogenic stressors within the lagoon system. Estuaries are

considered at medium risk for eutrophication when nitrate values range from 0.1-1 mg N/L

and high euthrophic risk when the values are greater than 1 mg N/L [Bricker et al., 1999]. It

has been noted that nutrient levels within the lagoon can vary seasonally and spatially as a

result of river discharge, rainfall, resuspension of sediments, and biological activity [Moran-

Silva, et al. 2005]. Concentrations of total inorganic carbon (TIC) ranged from 14.4-22.1 mg

C/L and did not vary seasonally. Levels of total organic carbon (TOC) ranged from 3.9-20.9

mg C/L, with the highest concentrations observed during the rainy season (Table 2).

Total mercury and total suspended solids (TSS) ranged from 0.92-26.1 ng Hg/L and 1-

39.2 mg TSS/L, respectively (Table 2). The strong correlation (R2=0.71; P=0.001) between

total mercury and TSS in the water column suggests that particulate matter is a carrier phase

for mercury within the Alvarado and Camaronera lagoons. A more comprehensive study of

the Alvarado Lagoon, and the Limon, Acula, Blanco, and Papaloapan rivers conducted during

the March 2003 and 2005 dry seasons and the September 2005 wet season found that mercury

concentrations were significantly correlated with total suspended solids in the water column

(R2=0.82; P<0.001) [Guentzel et al., 2007]. The mercury concentrations in the Alvarado

Lagoon, and the Blanco, Acula, and Limon rivers during the March 2003 and 2005 dry

seasons (0.9-4.9 ng Hg/L) were similar to the September 2005 wet season (1.9-4.9 ng Hg/L),

with higher Hg levels associated with higher levels of TSS. Water samples collected from the

Papaloapan River were higher in Hg (10.9-12.7 ng (Hg/L) and TSS (89.1-154.7 mg TSS/L)

during the September 2005 wet season than the March 2003 and 2005 dry seasons (0.9-2.7 ng

Hg/L; 4.8-39.7 mg TSS/L). The sites from the Papaloapan River were sampled within 12

hours of a nighttime rainfall (15cm) event during the September 2005 wet season. The

elevated Hg concentrations from this site during the wet season are likely a result of increased

particulate matter transport within the river during high flow conditions and or input of

dissolved and particulate Hg from precipitation [Guentzel et al., 2007]. A Mercury Deposition

Network (MDN) monitoring site (HD01) within this region reported a rainfall Hg

concentration of 11.4 ng Hg/L during the time period that the samples were collected from the

Papaloapan River [Mercury Deposition Network]. The water column values that we observed

for total Hg (0.92-26.1 ng/L) are below the US EPA ambient surface water quality criteria for

freshwater (0.77-1.4 µg/L) and saltwater (0.94-1.8 µg/L) (US EPA, 2006) and the Mexican

marine aquatic life criteria of 0.02 µg/L [Jimenez et al., 1999].

Table 1. Station identifications and locations for

mercury and other water quality parameters

Latitude Longitude

Station Identification (N) (W)

Alvarado Lagoon I 18 46.132 095 47.333

T 18 45.955 095 48.607

BB 18 44.995 095 44.966

Lagoon Camaronera DD 18 51.178 095 54.654

EE 18 51.589 095 55.187

FF 18 51.716 095 54.412

Gulf of Mexico AA 18 48.422 095 44.420

Table 2. Water quality parameters measured during the March 2003 and 2005

dry season and the September 2005 wet season

, Month Station Salinity

(psu)

Nitrate

NO3-N

(mg/L)

pH Total

Inorganic

Carbon

(mg C/L)

Total

Organic

Carbon

(mg C/L)

Total

Suspended

Solids

(mg/L)

Total

Mercury

(ng/L)

Alvarado Lagoon March 2003 I 9.9 2.3±0.9 8.1 14.9±4.2 5.4±2.1a 9.1±4.5a 0.92±0.05a

March 2003 T 9.8 1.35 8.0 14.4 4.7a 1a 1.78a

March 2003 BB 6.7 1.51 7.9 14.7 3.9a 14.1a 2.67a

March 2005 T 12.9 - 8.1 22.1±0.16 9.5±0.98a 9.1±5.6a 0.92±0.03a

September 2005 T 1 - 7.6 16.7 20.9a 25a 3.8a

Lagoon Camaronera March 2003 DD 14.5 0.86 8.2 17.2 7.3 39.2 26.1

EE 14 1.08 8.2 17.6 7.8 18.6 5.2

FF 13.8 0.75 8.3 17.9 7.6 20.5 10.3

Gulf of Mexico March 2003 AA 25.5 0.73±0.8 8.6 16.4±0.47 6.5±0.04a 1.13a 1.27±0.01a

The values for March 2003 stations I and AA, and March 2005 station T represent the mean and standard deviation of 2 replicate field samples. ―a‖ denotes that

the total organic carbon, total suspended solids and total mercury data for the Alvarado Lagoon and Gulf of Mexico are taken from Guentzel et al., 2007. ―-

― denotes that there is no data for this parameter.

Table 3. Mercury concentrations in fish, crab, shrimp, and squid and log bioconcentration

(BCF) factors from the Alvarado Lagoon system

n Total Hg (ug Hg/g-wet) Log BCF

March March September March March September

2003 2005 2005 2003 2005 2005

Brown Shrimp (Peneus aztecus)* 20, 20, 20 0.008±0.001 0.065±0.01 0.008±0.001 3.6 4.6 3.6

Bay Squid (Lolliguncula brevis)* 3 0.024±0.002 4.2

Blue Crab (Callinectes rathbunae)* 3 0.026±0.002 4.2

White Mullet (Mugil curema)* 2 0.057±0.026 5.6

Sheepshead (Archosargus

probatocephalus)*

1 0.082 4.7

Big Mouth Sleeper (Gobimorus dormitor)* 2 0.106±0.02 4.8

Fat Snook (Centropomus parallelus)* 2 0.152±0.034 4.9

Spine Snook (Centropomus ensiferus)* 1 0.184 5.1

Striped Moharra (Eugerres plumeri)* 1, 2 0.35 0.301±0.117 5.3 5.3

Catfish (Bagre marina)* 1 0.291 5.3

*The data for mercury concentration is taken from Guentzel et al., 2007. The log BCF is calculated as Log 10([Hg in tissue]/[Hg in water]). The average water

concentration of Hg was 1.6 ng/L. n=the number of samples.

The Alvarado Lagoon – Environment, Impact, and Conservation

403

We collected sediment from the lagoons and nearby rivers within the ALS. Total mercury

at station T in the AL ranged from 13-22 ng Hg/g-wet and the %C and %N ranged from 0.23-

0.77% and 0.31-0.37%, respectively. Total Hg from sediments in the adjacent rivers (Acula,

Limon, Blanco, and Papaloapan) ranged from 10-78 ng Hg/g wet and the %C and %N ranged

from 05-8.9% and 0.31-0.9%, respectively. There was a moderate correlation (R2=0.435,

p=0.020) between the total Hg and % carbon in the sediments from the ALS [Guentzel et al.,

2007]. The total Hg values for the sediment we collected are below the threshold effects level

of 130 ng Hg/g dry for marine sediments [Buchman 1999] and are within the US EPA

background sediment criteria of 0-300 ng Hg/g dry (US EPA 1997). Aquatic biota that

represent ~87% of the annual catch from the ALS [Cruz-Escalona et al., 2007] were collected

and analyzed for total Hg (Table 3). The total Hg concentration in the invertebrate species

(shrimp, squid, crab) ranged from 0.008-0.026 μg Hg/g wet and the vertebrate species ranged

from 0.082-0.35 μg Hg/g wet. The levels of Hg in the piscivorous and omnivorous fish

(catfish, moharra) are at or slightly above the recommended consumption level of 0.3 μg Hg/g

wet [NAS, 2000].

The log bioconcentration factors for total Hg in the organisms we collected ranged from

3.9-5.3, with no observable seasonal difference (Table 3). Activities such as biomass burning

for land clearing, mangrove deforestation, and urbanization are known stressors to the ALS.

These activities are also associated with increased mercury mobilization in aquatic and

terrestrial environments, which can result in an increase in the bioaccumulation of mercury in

biota from these systems [Friedli et al., 2003; Porvari et al., 2003; Munthe et al., 2007]. There

are a large number of indigenous riverbank communities within the ALS that rely on fishing

for comestible and economic subsistence. Reported total Hg levels in hair samples from

individuals that reside and consume fish from within the ALS ranged from 0.10-3.36 µg Hg/g

(n=47) [Guentzel et al., 2007]. Of these values, 58% are above the recommended

consumption limit of 0.1 µg Hg/kg body/day which corresponds to a hair level of 1.0 µg Hg/g

[NAS, 2000]. Anthropogenic activities that mobilize Hg could result in an increase in the

mercury content of the fish and seafood from the ALS which may ultimately lead to increased

body burdens of mercury in the indigenous peoples that reside in this region.

Vegetation

The ALS features representative and diverse ecosystems of Mexico´s Gulf coastal plain,

such as coastal dunes, reed beds of Cyperus spp., cattail Typha spp., palm forests of Sabal

mexicana, Scheelea liebmannii, and Acrocomia mexicana, oak forest of Quercus oleoides;

apompales (Pachira aquatica), and a large mangrove forest dominated by Avicenia

germinans, Laguncularia racemosa, and Rhizophora mangle [Vazques-Torres, 1998]. There

are 15 distinguishable landscape units (LU) in the area [Portilla-Ochoa et al., 1998 and Silva-

López and Portilla-Ochoa 1998]. The LU were first differentiated as areas disturbed by

agricultural activities, areas disturbed by cattle ranching, and areas where human intervention

is not yet considerable, such that natural vegetation remains the dominant landscape element.

Each LU was described in terms of land use, seasonal flooding, vegetation cover (i.e. primary

and secondary), predominant exploitation systems, the physical medium (i.e. substrate origin

and soil type), hydrologic characteristics, and other data (e.g. human settlements, main roads,

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

404

and observations on deforestation, urban and rural infrastructure, and industrial development)

[Silva-López and Portilla-Ochoa 1998 ].

Fish

There are 107 fish species that have been collected in the ALS which represent four

ecological guilds: marine stenohaline, marine euryhaline, estuarine, and freshwater fishes.

Fish assemblages of the Alvarado Lagoon Estuary have not experienced significant changes

over 40 years, but there may have been a decline in fish biodiversity during that period

[Chávez-López et al., 2005a]. A comprehensive study of Mayan cichlids conducted in the

ALS, by Chavez-Lopez et al., 2005b, reports that there are three genera and seven species of

cichlids (Cichlidae) with the Mayan cichlid (Cichlasoma urophthalmus) being the species

with the highest abundance. The Mayan cichlid is distributed throughout southeastern Mexico

where it inhabits rivers and coastal lagoons. In the ALS it is distributed towards the north in

Camaronera Lagoon. The Mayan cichlid inhabits oligohaline to mesohaline sites that are well

oxygenated and contain submerged vegetation and deep transparent water. The major

abundance and biomass of this species was obtained during December to February. The diet

of Mayan cichlids is primarily herbivorous and consists mainly of plant detrital material and

algae. There are two size classes that occur during the dry and rainy seasons which

correspond to young of the year and reproductive fish. There is only one modal size class of

fish between 60–100 mm during the stormy season. Although individuals with developed

gonads are found throughout the year, the most reproductive adults are found between April

and December. The highest gonadosomatic index (GSI) values occurred during the May

through July time period of peak reproductive activity [Chávez-López et al., 2005b]. Other

families with numerous species reported within the ALS include the Eleotridae and the

Gobiidae, and the species with the highest abundance and biomass were Gambusia affinis,

Petenia splendida, Cathoropus melanopus, Diapterus auratus, and Bathygobius soporator

[Shareet et al., 2009].

A study by Pelaez-Rodriguez et al., (2005) examined the diet of demersal piscivorous

fishes captured as bycatch by the commercial shrimping fleet just ouside of the ALS . Nine

collections distributed throughout the stormy, wet, and dry seasons from November 1993 to

January 1995 yielded a total of 646 fishes which represented 10 families and 14 species.

44.9% of these collections had empty digestive tracts and were excluded from the study. The

most abundant species of dermersal predators found were Trichiurus lepturus and Synodus

foetens. Differences in food consumption of the seven most abundant predators were

observed among the 3 seasons. The greatest variety of prey (20 species) occurred during the

stormy season and the lowest variety (nine species) occurred during the dry season. Prey type

and location of prey within the water column helped to determine the classification of five

distinct trophic guilds based on an overall index of relative importance of prey. The

occurrence of these different trophic guilds may contribute to decreased competition for food

resources on the continental shelf off of Alvarado lagoon [Peláez-Rodríguez et al., 2005].

The Alvarado Lagoon – Environment, Impact, and Conservation

405

River Otters

A study of the neotropical river otter (Lontra longicaudis annectens) and its habitat based

on personal observations and the information provided by fishermen of the ALS, yielded

three observations of adult otters hunting and eating in lagoons and rivers, together with

records of otter tracks and feces. In addition, an adult otter skin was found in a fisherman‘s

house in November 2002, where residents of the ALS said the otter was killed that year. All

of these records were collected in three of the most conserved LU of the system, which

include an area of 607 km2, encompassing more than 22.7 % of the total area of the ALS

[Silva-López, 2009]. These observations and records, along with comments made by other

Alvarado fishermen, suggest the neotropical river otter occupies the ALS year-round, and

emphasizes the need to conduct more detailed surveys and studies to determine the present

status and ecology of the ―perro de agua‖ (as it is locally known) and its habitat [Silva-López,

2009].

Manatees

Antillean manatees (Trichechus manatus manatus) have historically occurred in the ALS,

representing one of the most important areas for manatees in the southern GOM.

Overexploitation reduced their numbers in the 1970s and 1980s and they are now considered

endangered throughout their range in Mexico. However, the rescue of six orphan calves

suggests that manatees may be increasing in the ALS. Historically, the Antillean manatee was

found from northern Veracruz state along the west coast of the GOM to the eastern coast of

the Yucatan peninsula and the Mexico-Belize border [Lluch, 1965, Lefebvre et al., 2001,

Morales-Vela et al., 2005]. However; hunting, water quality degradation, and the destruction

of breeding habitat has caused a decline in the number of manatees [Campbell and Gicca,

1978, Colmenero and Hoz, 1986].

There is little information regarding the life history of manatees in the state of Veracruz.

It is not known if they migrate, as the Florida subspecies (Trichechus manatus latirostris)

does in the United States [Deutsch et al., 2003], or whether they are year-round residents of

their local habitat, as is typical of Antillean manatees in the Yucatan Peninsula of Mexico and

in Belize [Morales-Vela et al., 2000, Self-Sullivan et al., 2003]. Movements of Antillean

manatees in Chetumal Bay, on the east coast of the Yucatan Peninsula, do not appear to be

influenced by cloudiness, atmospheric pressure, or temperature, in contrast to the Florida

manatee that migrates seasonally in response to intra-annual changes in water temperature

[Axis-Arroyo et al., 1998, Deutsch et al., 2003]. However, movements of Antillean manatees

in Chetumal Bay were moderately associated with water salinity (as in Florida), depth and

group structure [Axis-Arroyo et al., 1998]. Manatees in Florida seem to prefer areas with

access to freshwater that they require for osmoregulation. The salinity in the waters of the

ALS decreases with distance from the ocean, and the potential influence of this salinity

gradient on the movements of manatees in the ALS is unknown. Manatees in Nicaragua

undergo seasonal migrations, and their daily movements appear to be influenced by tides,

which may also influence water salinity [Jimenez, 2002]. In the ALS fishermen have reported

that manatees were quite common in the region in the mid-1900s. Even though large scale

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

406

hunting of manatees was not practiced in ALS, the sale of meat in the town market of

Alvarado during the 1970‘s was common [Ortega-Argueta, 1999], and poaching continues to

be an important threat to the species. Studies conducted in the mid 1980s reported the

disappearance of manatees from the ALS [Colmenero, 1984]. Nevertheless, recent reports

from local residents of the ALS, and the incidental capture of manatee calves, have confirmed

their continued occurrence in the Alvarado region [Ortega-Argueta, 1999; Portilla-Ochoa et

al., 1999]. A recent study assessing manatee distribution and habitat utilization found that

manatees could potentially be found in 3150 km2 of lowlands and wetlands in the ALS

(Figure 2) [Ortega-Argueta, 2002]. Habitats selected by manatees include estuaries, mangrove

wetlands and unpopulated areas. The marine zone appears not to be utilized permanently by

manatees, although they may move locally between rivers along the coast through the marine

zone. Threats to the manatees in the ALS include the clearing of land for sugar cane

cultivation, cattle-ranching, coastal urban development, mangrove deforestation, increases in

port and tourism industries in the coastal zone, water pollution, and oil and gas exploration

and exploitation [Ortega-Argueta, 1999, 2002].

Rodriguez-Ibañez [2004] investigated the knowledge, use, and cultural traditions of the

inhabitants of the ALS with respect to the Antillean manatee using oral interviews. She found

a large number of correlations between the inhabitants‘ oral history knowledge of manatee

movements and habitat use with current scientific knowledge as determined by a review of

the literature. Additionally, many inhabitants knew a lot about the hunting, butchering, and

preparing of manatee meat for human consumption. Such hunting has reduced the manatee

population in the ALS to very low levels [Ortega-Argueta et al., 2003].

Figure 2. Classification of manatee habitat within the Alvarado Lagoon System (from Ortega-Argueta,

2002). Most of the best habitat lies in the lagoons along the Limon river and in lagoons between the

Limon and Acula rivers. The Papaloapan river is not good manatee habitat due to its rapid current and

channelizing with dikes that prevent animals from entering and leaving the river easily.

The Alvarado Lagoon – Environment, Impact, and Conservation

407

During several interview surveys conducted with local inhabitants and fishermen,

besides boat and airplane surveys in 2000, 2005 and 2006 it was revealed that manatees are

common in the ALS around the year [Ortega-Argueta, 2002, Portilla-Ochoa et al., 2006,

2007, Keith et al., 2009]. Manatees are most commonly sighted in the Acula River and

adjacent lagoons, and are rarely sighted in the Limon River and adjacent lagoons (Figure 3).

Most of the interviewees reported that manatees are not as abundant now as compared to

three decades ago, but their numbers have increased in the past few years (Figure 4). Most of

the sightings are of adult animals, although females and calves are infrequently seen (Figure

5). Most sightings occur in the rainy season (Figure 6), and most sightings are unique in the

sense that an animal is usually only seen once, rather than frequently or repeatedly (Figure 6).

Respondents thought that manatees predominantly feed on marsh plants and water hyacinth,

with ―grasses‖ and other emergent plants also being important in the diet (Figure 7). A recent

survey of the ALS using visual, acoustic, and side-scan sonar methods estimated the

abundance of manatees in the ALS at 0.93 manatees/ha ± 0.39 (95% CI) [Serrano-Solis,

N.D.].

Figure 3. Locations of manatee sightings (from both vessels and aircraft), interviews and evidence of

manatee butchering (from Ortega-Argueta, 2002).

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

408

Figure 4. Increase in the number of manatee sightings over the past decade as determined by interviews

with residents of the ALS. Most of the interviewees reported that manatees are not as abundant now as

compared to three decades ago, but their numbers have increased recently. This increment in

observations may reflect a recovery of the manatee population; a more dedicated monitoring effort; or

an increase of the appeal of the species as results of the education and awareness campaigns.

Figure 5. Age-class of manatees sighted in the ALS as determined by interviews with residents. Most of

the sightings are of adult animals, although females and calves are infrequently seen

Figure 6. Seasonality and frequency of manatee sightings in the ALS as determined by interviews with

the residents. Most of the sightings occur in the rainy season and most sightings are unique in the sense

that an animal is usually only seen once, rather than frequently or repeatedly

The Alvarado Lagoon – Environment, Impact, and Conservation

409

Figure 7. Foods of manatees as reported by residents of the ALS. Respondents thought that manatees

predominantly ate marsh plants and water hyacinth, with ―grasses‖ and other things also being

important in the diet

We also found that the inhabitants of the ALS maximized their use of the manatees killed

in the distant past, including the medicinal use of powdered manatee bones and manatee fat,

and the use of manatee bones and teeth in the production of artifacts. This suggests that

manatees played a significant role in the culture of these riverbank communities in the past. A

majority of those interviewed (82%) said they were interested in protecting animals liberated

near their homes in the ALS. However, several respondents expressed concern that neighbors

would kill released animals and/or that hunting would continue because of lack of

enforcement of the laws [Portilla-Ochoa et al., 2006, 2007, Keith et al., 2009]. Manatee

poaching continues in many areas despite official protection. This illegal activity is still

practiced for a number of reasons: tradition; an appreciation of manatee meat, which is

considered a delicacy; ignorance of national laws and sanctions in force to protect the

manatee, and limited inspection and vigilance by Mexican environmental and regulatory

authorities (Ortega-Argueta, 1999).

CONSERVATION

The coastal wetland lagoon system of Alvarado is one of the most productive such

systems in Veracruz and the third largest wetland in Mexico. A total 350 species of birds have

been registered in the ALS, including the Mexican Duck (Anas diazi), which is undergoing a

slow but marked decline due to habitat destruction and overhunting. The ALS has been

considered a high priority region for conservation [Arriaga-Cabrera et al., 1998; CONABIO,

1998; Dugan, 1993], including recognition by the North American Wetlands Conservation

Council (NWCCA), the International Council for Bird Preservation-Mexico Chapter

(CIPAMEX), and Mexico‘s Commission on Biodiversity (CONABIO). Notable, too, are the

threats, including agricultural encroachment and increasing levels of contamination from

urban wastewater and pesticides. A newly funded program will enable the municipality of

Alvarado and Pronatura Veracruz (local NGO) to strengthen the environmental education

program in Alvarado schools; teach sustainable management techniques to local communities

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

410

and train them to be conservation promoters; and develop wetland-conservation outreach

materials for use by local authorities. A conservation easement will be pursued at a site of

high importance to wetland-associated birds. Partners will work to reduce the effects of cattle

ranching on wetland resources and will continue monitoring resident and migratory birds in

the area. These activities will be coordinated with the newly formed Veracruz State

Committee for Conservation of Wetlands.

One of the most important achievements of our conservation activities in Veracruz was

the nomination of Alvarado lagoon system as a Ramsar Site. On February 4th

, 2004, the ALS

was designated Ramsar Site No. 1355 through the efforts of the Institute for Biological

Research (IBR) at the University of Veracruz, and other organizations such as the North

American Wetlands Conservation Council. The area encompasses 2671 km2 that includes

most of our proposed critical manatee habitats and other areas that are crucial to manatee

survival. The ecological description of the site mentions the region‘s importance to this

endangered species. The IBR is taking further actions with the collaboration of local

authorities in order to assure the implementation of protective measures and to establish a

Regional Management Plan for the area. Further information on the ALS Ramsar Site can be

found on the following web page: http://www.ramsar.org/wwd2004_rpt_mexico1.htm.

After several workshops involving specialists and governmental agencies, including the

―Technical Advisory Subcommittee for Manatee Recovery in Mexico‖, it was concluded that

in order to protect the manatees in the ALS from continued poaching, the primary mortality

factor, an education and awareness program should be developed throughout the ALS.

Additional components included an assessment of the current status of manatees in the ALS

and the identification of critical manatee habitats within the ALS [Ortega-Argueta, 1999,

2002, Portilla-Ochoa et al., 2002]. These efforts led to the preparation of a ―Regional Manatee

Recovery Plan in the Wetlands of Alvarado, Veracruz, Mexico‖ [Ortega-Argueta et al., 2001,

2002, 2003], and culminated in 2001 when September 7th

was officially declared the

―National Day of the Manatee‖ in Mexico. With the potential for the release of rehabilitated

manatees from the Veracruz Aquarium into the ALS, there is need for continued educational

and informational campaigns to further educate the local community about the need to protect

and conserve manatees and their habitat. Over the intervening years our educational,

conservation, and outreach activities have continued, including informative workshops for

children and adults in the communities within and surrounding the ALS, boat surveys of the

ALS for manatees, interviews with fishermen and others familiar with the ALS and putative

manatee habitats there, and continued celebration of the ―National Day of the Manatee‖

[Ortega-Argueta et al., 2001, 2002, 2003, Portilla-Ochoa et al., 2002,].

The rescue of orphan manatees in the ALS suggested that the population of manatees

might be rebounding, and this has motivated the conservation and education efforts of the

past decade [Ortega-Argueta et al., 2002, 2003]. During this period, six orphan manatees have

been rescued from the ALS and transported to the Veracruz Aquarium in the city of Veracruz,

Mexico. A seventh animal was rescued but subsequently died from a gunshot wound. As the

captive population in the aquarium has grown, they have constructed a new, larger, manatee

pool and viewing area, sufficient to support 4-6 manatees. The possibility that more orphan

manatee calves may be encountered in the future has raised the concern that the aquarium will

no longer be able to continue to accept new orphans without some mechanism to decrease the

total number of animals being cared for there. The ability to release some animals will

increase the Aquarium‘s capability to foster new orphans if and when they should be found.

The Alvarado Lagoon – Environment, Impact, and Conservation

411

Rehabilitation strategies and sites for release are being discussed in the Manatee Advisory

Committee.

An agency of the government of the state of Veracruz, the ―Papaloapan Development

Council‖ (Consejo de Desarrollo del Papaloapan, CODEPAP) has recently constructed two

concrete-lined tanks suitable for manatee husbandry along the banks of the Acula River in the

central ALS. These tanks were designed and constructed to facilitate the reintroduction of

captive manatees into the ALS. Plans are currently underway to transfer some of the manatees

from the Veracruz Aquarium to these tanks and to begin their transition to a free-ranging

existence. Once the manatees have become accustomed to feeding on the native vegetation,

and have been weaned from their dependence on humans, it is anticipated that they will be

released into an enclosure along the bank of the Acula River, and eventually into their native

habitat. Such husbandry constitutes an opportunity to rehabilitate and release individuals of

one of the most threatened species in Mexico.

CONCLUSION

The Alvarado Lagoon System is a mangrove dominated coastal wetland formed by the

confluence of the Acula, Blanco, Limon and Papaloapan rivers. The ALS is one of the most

productive estuary-lagoon systems in the Mexican GOM. It has a total area of 2800 km2 of

which 258 km2 are covered by water with an average depth of 1.5 m. Vegetation of the ALS

includes diverse ecosystems representative of Mexico´s Gulf coastal plain. Salinity in the

ALS was inversely correlated with rainfall, with highest levels occurring in the dry season

samples (March 2003 and 2005) and lowest levels occurring in the wet season samples

(September 2005). Concentrations of total inorganic carbon did not vary seasonally, while

levels of total organic carbon were higher during the rainy season. A strong correlation

between total mercury and total suspended solids in the water column suggests that

particulate matter may be a carrier phase for mercury within this lagoon system.

Historically, Antillean manatees were found in the ALS and along the west coast of the

Gulf of Mexico to the eastern coast of the Yucatan peninsula and the Mexico-Belize border.

However, hunting, water quality degradation, and the destruction of breeding habitat has

caused a decline in the number of manatees and they are now considered endangered

throughout their range in Mexico. Manatee habitat in the ALS includes estuaries, mangrove

wetlands and unpopulated regions, with a total potential area of 3150 km2.

Interviews with the inhabitants of the ALS reveal important correlations between their

oral history knowledge of manatees with current scientific knowledge. They also knew a lot

about the hunting, butchering, and preparing of manatee meat for human consumption. The

inhabitants maximized their use of the manatee carcass, including the medicinal use of

powdered manatee bones and manatee fat, and the use of manatee bones and teeth in the

artisanal production of artifacts, suggesting that manatees played a significant role in their

culture in the past.

A majority of those interviewed said they were interested in protecting manatees, but

several expressed concern that hunting would continue because of lack of enforcement of the

laws. Manatee poaching continues for a number of reasons including tradition; an

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

412

appreciation of manatee meat that is considered a delicacy; ignorance of national laws and,

and limited vigilance by Mexican environmental and regulatory authorities.

In 2001, September 7th

was officially declared the ―National Day of the Manatee‖ in

Mexico. Our educational and informational campaigns have continued in order to educate the

local communities about the need to protect and conserve manatees and their habitat. In 2004,

the ALS was designated Ramsar Site No. 1355 and a ―Regional Manatee Recovery Plan in

the Wetlands of Alvarado‖ was prepared. Over the past decade, six orphan manatees have

been rescued from the ALS and transported to the Veracruz Aquarium in the city of Veracruz.

Two concrete-lined tanks suitable for manatee husbandry have recently been constructed

along the banks of the Acula River in the central ALS. These tanks were designed and

constructed to facilitate the reintroduction of captive manatees into the ALS. Such efforts

constitute an important opportunity to rescue, rehabilitate, and release individuals of one of

the most threatened species in Mexico.

Continuing threats to the ALS include increasing anthropogenic activities both within the

lagoon system and in its surrounding terrestrial areas. Limited waste management planning

and practices have contributed to deterioration of its hydrological characteristics. Overfishing,

manatee poaching, and loss of habitat have lead to a significant deterioration in the quality of

ecosystem services provided by the ALS. Despite the establishment of government policy and

measures to protect the coastal wetlands of ALS, the identified threats continue to menace the

important biodiversity and human well-being of the region.

REFERENCES

Arriaga Cabrera, L., Vázquez Domínguez, E., González Cano, J., Jiménez Rosenberg, R.,

Muñoz López, E. & Aguilar Sierra, V. (1998). Regiones Marinas Prioritarias de México.

Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. México D.F.,

México. 1998.

Axis-Arroyo, J., Morales-Vega, B., Torruco-Gomez, D. & Vega-Candejas, M. E. (1998).

Variables asociadas con el uso de hábitat del manatí del Caribe (Trichechus manatus) en

Quintana Roo, México (Mammalia). Rev. Biol. Trop., 46, 1-11.

Bricker, S. B., Clement, C. G., Pirhalla, D. E., Orlando S. P. & Farrow, D. R. G. (1999).

National Estuarine Eutrophication Assessment: Effects of Nutrient Enrichment in the

Nation‘s Estuaries. NOAA, National Ocean Service, Special Projects Office and the

National Centers for Coastal Ocean Science. Silver Spring, MD. 71.

Buchmann M. (1999). NOAA screening quick referente tables. NOAA HAZMAT report 99-

1, Seattle, WA, Coastal Protection and Restoration Division. NOAA. 12.

Campbell, H. W. & Gicca, D. (1978). Reseña preliminar del estado actual del manatí

(Trichechus manatus) en México. Anales del Instituto de Biologia, Universidad Nacional

Autonoma de Mexico, Serie Zoologia, 49, 257-264.

Chávez-López, R., Franco-López, J., Morán-Silva, A. & O‘Connell, M. T. (2005a). Long-

Term Fish Assemblage Dynamics of the Alvarado Lagoon Estuary, Veracruz, Mexico.

Gulf and Caribbean Research, 17, 145-156.

Chávez-López, R., Peterson, M. S., Brown-Peterson, N. J., Morales-Gómez, A. A. & Franco-

López, J. (2005b). Ecology of the Mayan Cichlid, Cichlasoma urophthalmus Günther, in

The Alvarado Lagoon – Environment, Impact, and Conservation

413

the Alvarado Lagoonal System,Veracruz, Mexico. Gulf and Caribbean Research, 17,

123-131.

Colmenero, L. del C. (1984). Nuevos registros del manatí (Trichechus manatus) en el sudeste

de México. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico,

Serie Zoologia, 54, 243-254.

Colmenero-R., L. del C. and M. E. Hoz Z. (1986). Distribución de los manatíes, situación y

su conservación en México. An. Inst. Biol. Univ. Nal. Autón. de Méx., Ser. Zool. 56(3):

955-1020.

CONABIO (1998) La Diversidad Biológica de México: Estudio de País. Comisión Nacional

para el Conocimiento y Uso de la Biodiversidad. México D.F., México, 16.

Cruz-Escalona, V. H., Arrenguin-Sanchez, F. & Zetina-Rejon, M. (2007). Analysis of the

ecosystem structure of Laguna Alvarado, western Gulf of Mexico, by means of a mass

balance model. Estuarine, Coastal and Shelf Science, 72, 155-167.

Dugan, P. (1993). Wetlands in Danger: A World Conservation Atlas. IUCN-The World

Conservation Union. Oxford University Press, USA. 1993. 187.

Deutsch, C. J., Reid, J. R., Bonde, R. K., Easton, D. E., Kochman, H. I. & O‘Shea, T. J.

(2003). Seasonal movements, migratory behavior, and site fidelity of West Indian

manatees along the Atlantic coast of the United States. Wildlife Monographs, 151, 1-77.

Friedli, H., Radke, L., Lu, J., Banic, C., Leaitch, W. & MacPherson, J. (2003). Mercury

emissions from burning of biomass from temperate North American forests: laboratory

and airborne measurements. Atmospheric Environment, 37, 253-267.

Guentzel, J. L, Portilla, E., Keith, K. M. & Keith, E. O. (2007). Mercury transport and

bioaccumulation in riverbank communities of the Alvarado Lagoon System, Veracruz

State, Mexico. Science of the Total Environment, 388, 316-324.

Jimenez, B., Ramos, J. & Quezada, L. (1999). Analysis of water quality criteria in Mexico.

Water Science and Technology, 40, 169-75.

Jimenez, I. (2002). Heavy poaching in prime habitat: The conservation status of the West

Indian manatee in Nicaragua. Oryx, 36, 272-278.

Keith, E. O., Portilla-Ochoa, E., Ortega-Argueta, A., Cortina-Julio, B., Contreras-Torres, C.

& Hernandez-Montero, J. (2009). Status and recovery of the Antillean manatee in the

Alvarado Lagoon System, Veracruz Mexico. Sirenews – Newsletter of the IUCN Sirenia

Specialist Group. 41, 18.

Lefebvre, L. W., Marmontel, M., Reid, J. P., Rathbun, G. B. & Domning, D. P. (2001). Status

and biogeography of the West Indian manatee. In C. A. Woods, & F. F. Sergile, (editors)

Biogeography of the West Indies: Patterns and perspectives. CRC Press, Boca Raton, FL.

425-474.

Lluch, B. D. (1965). Algunas notas sobre la biología del manatí. Anales del Instituto Nacional

de Investigaciones Biólogo-Pesqueras. 1, 405-419.

Mercury Deposition Network, National Atmospheric Deposition Program. www.nad

p.sws.uius.edu

Morales-Vela, B., Olivera-Gomez, D., Reynolds, J. E. & Rathbun, G. B. (2000). Distribution

and habitat use by manatees in Belize and Chetumal Bay, Mexico. Biological

Conservation, 95, 67-75.

Morales-Vela, B. D., Padilla-Saldivar, J. A. & Mignucci-Giannoni, A. A. (2005). Status of

the manatee (Trichechus manatus) along the northern and western coasts of the Yucatán

peninsula. Caribbean Journal of Science, 36, 42-49.

Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

414

Morán-Silva, A., Martínez- Franco, L. A., Chávez-López, R., Franco-López, J., M. Bedia-

Sánchez, C. M., Espinosa, F. C., Mendieta, F. G. Brown-Peterson, N. J. & Peterson, M.

S. (2005). Seasonal and Spatial Patterns in Salinity, Nutrients, and Chlorophyll a in the

Alvarado Lagoonal System, Veracruz, Mexico. Gulf and Caribbean Research, 17, 133-

143.

Munthe, J., Hellsten, S. & Zetterberg, T. (2007). Mobilization of mercury and methymercury

from forest soils after a severe storm-fell event. Ambio, 36, 111-113.

National Academy of Sciences (NAS). (2000). Toxicological effects of methylmercury.

National Academy Press, Washington, DC USA. 368.

Ortega-Argueta, A. (1999). Situación actual y las perspectivas de conservación del manatí en

el sistema lagunar de Alvarado, Veracruz, Mexico. Informe Técnico presentado a la

Dirección General de Vida Silvestre, INE-SEMARNAP. Instituto de Ecología, A.C.,

Xalapa, Ver., México.

Ortega-Argueta, A. (2002). Evaluación del Hábitat del Manatí (Trichechus manatus) en el

Sistema Lagunar de Alvarado, Veracruz, México. M.Sc. Thesis. Wildlife Management

Program, Instituto de Ecología, A. C. Xalapa, Ver., México.

Ortega-Argueta, A., Portilla-Ochoa, E. & Keith, E. O. (2001). A Regional Manatee Recovery

Plan for the Alvarado Lagoon System, Veracruz, Mexico. Poster presented at the XIV

Biennial Conference on the Biology of Marine Mammals, Vancouver, BC, Canada. 28

November-3 December.

Ortega-Argueta, A., Portilla-Ochoa, E. & Keith, E. O. (2002). Manatee recovery plans for

wetlands of Alvarado, Veracruz, Mexico. Final Report to the Save the Manatee Club, 35.

Ortega-Argueta, A., Portilla-Ochoa, E. & Keith, E. O. (2003). Manatee recovery plan for

wetlands of Alvarado, Veracruz, Mexico. Annual Report to the Wildlife Trust, Ref. #02-

03-099. 32.

Pelaez-Rodríguez, E., Franco-López, J., Matamoros, W. A., Chávez-López, R. & Brown-

Peterson, N. J. (2005). Trophic Relationships of Demersal Fishes in the Shrimping Zone

off Alvarado Lagoon, Veracruz, Mexico. Gulf and Caribbean Research, 17, 157-167.

Portilla-Ochoa, E., Silva-López, G., García Campos, H. & Ramírez-Salazar, M. (1998).

Paisajes amenazados en el complejo lagunar de Alvarado. In: G., Silva-López, Vargas-

G. Montero, & J. Velasco-Toro, (editors). De Padre Río y Madre Mar: Reflejos de la

Cuenca Baja del Papaloapan, Veracruz. Editora del Gobierno del Estado de Veracruz-

Llave, Veracruz, México. Vol. II. 257-263.

Portilla-Ochoa, E., Paradowska K. & Cortina-Julio, B. E. (1999). Educación ambiental y

planeación participativa para la conservación del manatí en Alvarado, Veracruz, México.

Informe Técnico presentado a la Dirección General de Vida Silvestre, INE-SEMARNAP.

Instituto de Investigaciones Biológicas, Universidad Veracruzana.

Portilla-Ochoa, E., Cortina-Julio, B. E., Ortega-Argueta, A., Keith, E. O. & Vanoye-Lara, F.

(2002). Achievements of the manatee conservation program in Veracruz, Mexico.

Manatee Conservation Workshop accompanying the XXVII International Annual Meeting

for the Study of Marine Mammals, Veracruz, Ver., Mexico.

Portilla, E., Hernández, J. R., Contreras, C., Cortina, B. E. & Keith, E. O. (2006). Status and

recovery of the Antillean manatee (Trichechus manatus manatus) in the Alvarado

Lagoon System, Veracruz, Mexico. Annual meeting of the Sociedad Mexicana de

Mastozoología Marina and the Sociedad Latinoamericana de Especialistas de Mamíferos

Acuáticos, Mérida, Yuc., México.

The Alvarado Lagoon – Environment, Impact, and Conservation

415

Portilla-Ochoa, E., Ortega-Argueta, A., Cortina-Julio, B., Contreras-Torres, C., Hernández-

Montero J. & Keith, E. O. (2007). Status and recovery of the Antillean manatee

(Trichechus manatus manatus) in the Alvarado Lagoon System, Veracruz, Mexico.

Sirenews – Newsletter of the IUCN Sirenian Specialist Group, 49, 8.

Porvari, P., Verta, M., Munthe, J. & Haapanen, M. (2003). Forestry practices increase

mercury and methymercury output from boreal forest catchments. Environmental Science

and Technology, 37, 2389-2393.

Rodríguez-Ibañez, C. (2004). Conocimiento, uso, y manejo del manatí Trichechus manatus

manatus del Sistema Lagunar de Alvarado, con énfasis en la historia oral. Tesis para el

título de Licenciado en Biología, Universidad Veracruzana, Xalapa, Ver., 96.

Self-Sullivan, C., Smith, G. W., Packard, J. M. & Lacommare, K. S. (2003). Seasonal

occurrence of male Antillean manatees (Trichechus manatus manatus) on the Belize

barrier reef. Aquatic Mammals, 29, 342-354.

Silva-López, G. & Portilla-Ochoa, E. (1998). Conservación y Manejo Sustentable de

Recursos Naturales en Unidades del Paisaje del Humedal de Alvarado, Veracruz,

México. Reporte Académico al US Fish & Wildlife Service (14-48-98210-97-G082).

Universidad Veracruzana, Xalapa, Ver., México.

Silva-Lopez, G. (2009). Records For The neotropical river otter In landscapes of the Ramsar

site Alvarado Lagoon System, México IUCN/SCC Otter Specialist Group Bulletin , 26,1-

62.

Serrano-Solis, A. Diagnostico de poblaciones de manaties: Monitorea ambiental en el sistema

lagunar de Alvarado. Technical Report, Universidad Veracruzana, Tuxpan, Ver. N.D. 54.

Shareet, C. F. Z., Jonathan, F. L., Escorcia, H. B., Arenas, L. G. A., Sanchez, C. B., Silva, A.

M. & Vasquez-Lopez, H. (2009). Trophic Seasonal Behavior of the Ichthyofauna of

Camaronera Lagoon, Veracruz. Journal of Fisheries and Aquatic Sciences, 4, 75-89.

U.S. EPA Mercury study report to congress, (1997). http://www.epa.gov/mercury

U.S. EPA National recommended water quality criteria, (2006). http://www.epa.gov/wa

terscience/criteria/wqctable/

Vasquez-Torres, M., Humedal de Alvarado: diversidad vegetal. In Vazques-Torres, S.M.

(editor). (1998) Biodiversidad y problematica en el humedal de Alvarado, Veracruz,

Mexico. Editorial Universidad Veracruzana. Veracruz, Mexico. Pp 143-168.