Lead from hunting activities and its potential environmental threatto wildlife in a protected wetland in Yucatan, Mexico

Flor Arcega-Cabrera n, Elsa Noreña-Barroso, Ismael Oceguera-VargasFacultad de Química, Unidad Sisal, Universidad Nacional Autónoma de México, Puerto de Abrigo Sisal, Yucatán 97355, Mexico

a r t i c l e i n f o

Article history:Received 28 June 2013Received in revised form4 November 2013Accepted 7 November 2013Available online 25 November 2013

Keywords:LeadSedimentsMultivariate analysisAnthropogenic lead potential threatYucatanMexico

a b s t r a c t

This study provides insights into the status of lead in the protected wetland of El Palmar, located on thenorthwestern littoral of the Yucatan Peninsula. This reserve is ecologically and economically importantbecause it provides feeding and breeding habitats for many species, as well as being an ecotourismdestination (especially for bird watching). Although it is a protected area, duck species are heavily huntedwithin the reserve during the winter. As a result, animals feeding or living in sediments could be exposedto anthropogenic lead. Total lead and its geochemical fractionated forms were measured in sedimentcores from six selected sites in “El Palmar” wetland, during pre- and post-hunting seasons, toapproximate the potential environmental threat (especially for benthonic living/feeding organisms).Anthropogenic lead concentrations detected in soil cores ranged from below the minimum infaunalcommunity effect level (30.24 μg g�1) during the pre-hunting season, to bordering the probable infaunalcommunity effect level (112.18 μg g�1) during the post-hunting season, according to SquiiRTs NOAAguidelines. Yet, these results were lower than expected based on the intensity of hunting. Consequently,this article explores the possibility that the lower than expected lead concentration in sediments resultsfrom (1) degradation of shot and transformation to soluble or particulate forms; or (2) ingestion of leadshot by benthic and other lacustrine species living in the protected area. Geochemical fractionation oflead demonstrated that in the top 6 cm of the soil column at heavily active hunting sites (EP5 and EP6),lead was associated with the lithogenic fraction (average 45 percent) and with the organic fraction(average 20 percent). Bioavailable lead (sum of lead adsorbed to the carbonates, Fe/Mn oxyhydroxidesand organic fractions) in sediments was lower than 50 percent for the heavily active hunting areas andhigher for the rest of the sites. Multivariate analysis showed that the environmental chemistry, thephysicochemical characteristics of the water, and the geochemical qualities of the sediments do not favorthe release of lead into the water column. Thus, the direct consumption of lead shot by organisms feedingin sea grass or in the top 10 cm of sediment is perhaps the major process preventing lead from beingdeposited in sediments, and, as such, these species (e.g., flamingos and/or ducks) could be threatened byanthropogenic lead pollution.

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1. Introduction

Lead poisoning in waterfowl and species frequenting wet-lands is common (Ancora et al., 2008; Romero et al., 2007;Scheuhammer and Norris, 1996; Beyer et al., 1988; Eisler, 1988).Birds are exposed to many sources of lead contamination, includ-ing lead in petrol (banned in Mexico in 1990), as well as urban andindustrial wastes (Lucia et al., 2009; Pain, 1992). Nevertheless,poisoning also occurs through the ingestion of lead objects such asgunshots or fishing weights (Ancora et al., 2008; Mateo et al.,2005; Schnug and Haneklaus, 2000; Scheuhammer and Norris,1996; Thompson et al., 1989). Lead has several negative impacts onbirds; for example, it impairs the growth and survival of nestlings,

as well as causing anemia and behavioral impairments (Lucia et al.,2009). Furthermore, hunting may cause disturbance and displace-ment of waterfowl in wetlands, since birds tend to move toneighboring or distant sites in response to shooting (Bregnballeand Madsen, 2004).

As reported by numerous studies worldwide (Pain, 1991, 1992;Baldassarre and Arengo, 2000; Fisher et al., 2006; Gangoso et al.,2009), the use of lead in hunting activities, sooner or later causespoisoning or death of associated fauna that live or feed in bottomsediments. Water birds often consume lead shots as grit since theyfall in the sediments and can remain trapped in the first 2–3 mm(Ancora et al., 2008). Once ingested the lead is released into theblood stream resulting in acute or chronic poisoning (Scheuhammerand Norris, 1996; Mostaghni et al., 2005).

In El Palmar, regulated hunting activities began approximately30 years ago, and during each hunting season 170 hunting permitsare issued, which allow 150 cartridges, containing 30 g of lead

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Ecotoxicology and Environmental Safety

0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ecoenv.2013.11.002

n Corresponding author. Fax: þ52 988912 0147x7203.E-mail addresses: fac72@hotmail.com, farcega@unam.mx (F. Arcega-Cabrera).

Ecotoxicology and Environmental Safety 100 (2014) 251–257

each, to be fired per permit. According to Pain (1991), approxi-mately 300 pellets enter the environment for each cartridge fired.Therefore, in total, approximately 23 metric tons of lead could bedeposited and concentrated in El Palmar reserve. Not surprisingly,flamingo deaths attributed to lead poisoning have been reportedfor the Yucatan Peninsula. Immediately following HurricaneGilberto in 1988, a total of 52 flamingos died of lead intoxication;postmortem dissection revealed that their gastrointestinal systemswere packed with lead shot. They exhibited lead blood levelsaround 300 ppm, when levels as low as 10 ppm have beenreported to be lethal for this species (Schmitz et al., 1990).

Lead shot degrades into particulate or molecular Pb species(Scheuhammer and Norris, 1996) at a specific rate depending onthe environmental characteristics of the site. Lead in the environ-ment is mostly in the inorganic form and accumulates in sedi-ments, but it also can be present as charged ions or complexes inthe interstitial and estuarine waters or in particulate phases thatdirect its mobility (Sadiq, 1992).

Metals in sediments could represent a potential threat for theaquatic biota and water quality (Charriau et al., 2011). Environ-mental studies on soil and sediment analysis often use leaching orsequential extraction procedures, which allow researchers toapproximate the bioavailable metal present (Rauret et al., 1998).For lead, in the sequential extraction procedure, adsorption to Fe,Mn oxyhydroxides4carbonate4organic matter/sulfides fractionsin sediments are generally expected (Sadiq, 1992). Though, bioa-vailability determined by this method should be considered moreas a guide for assessing potential environmental threat, than as aconclusive statement.

The necessity for information on the emergent status of lead inthe environment is especially important when two economicallyimportant and antagonistic activities occur concurrently (huntingand bird watching). Some protected organisms' living/feedinghabits could put them in direct contact with lead shot fromhunting activities (Thompson et al., 1989) by ingestion or throughthe trophic web (Gangoso et al., 2009). Therefore, the aim of thisstudy was to determine total lead and its geochemical fractionatedforms in hunting areas by analyzing core sediments from selectedsites in El Palmar in order to (1) detect the influence of hunting onlead variations and (2) approximate the potential environmentalthreat of anthropogenic lead for a protected wetland (in terms oftotal concentrations present and geochemical form).

2. Materials and methods

2.1. Study area and sampling

This study took place in El Palmar natural reserve in Yucatan, Mexico, wherehunting is allowed, being a permitted and quasi-regulated activity with animportant economical impact for the region. This reserve covers about 50,000 haand the climate is characterized by three seasonal regimes: a dry season, a rainyseason, and a “nortes” season (characterized by strong winds from the north).Approximately 60 percent of El Palmar is covered with mangroves and it isconsidered a wetland. El Palmar shows strong seasonal behavior with a highevaporation regime that results in almost complete drying during the dry seasonand flooding during the rainy and “nortes” seasons. Algae and sea grass (Rupiamaritima) cover the sediments until physicochemical parameters become tooextreme for their survival during the dry season.

The hunting and management histories of El Palmar were investigated throughinterviews with local authorities (SEDUMA) and local hunting guides from the onlyneighboring village, Sisal (located approximately 4.4 km southeast of the firstsampling station). Based on interviews with park rangers, sampling locations (EP1-15N 802068.95 2341819.55; EP2-15N 799974.45 2340641.89; EP3-15N 799499.32340395.08; EP4-15N 799392.2 2340443.34; EP5-15N 796734.7 2338927.89; EP6-15N 796177.76 2338314.44) were selected at sites where hunting activities have notoccurred in the past 5–8 years (EP1) and at sites that have been constantly usedsince the 1980s at variable intensities: low (50–100 hunters/year) intensity (EP2),medium (100–150 hunters/year) intensity (EP3 and EP4) and high (4150 hunters/year) intensity (EP5 and EP6).

Hunting in El Palmar takes place in open wetland pockets that are interspersedthroughout the mangrove forest where seasonal inundation limits tree growth andopen water is present for at least part of the year. Hunters construct blinds, locallyknown as “chucks”, at the forest-open water interface on small raised areas thatremain above water level year-round. Chucks provide views of open water areaswhile hiding the hunter from view of their prey. As a result, firing angles fromchucks are relatively limited, probably only reaching 1401 in the best case scenariosand often are less than 901. Therefore, once the wetland pockets had been selectedfor sampling based on use history, discrete sampling stations were placed at theheart of firing viewsheds at least 5–10 m away from hunting blinds to optimize leadshot and Pb concentration recovery. Future sampling at these sites should coverentire viewsheds to more accurately characterize how lead is dispersed across thesurface. Also X-ray analysis of sediments could be used to accurately determine thedensity of microscopic lead shot fragments (Mateo et al., 2005). However, oursampling strategy, involving the placement of sites based on the identification ofhunting viewsheds and interviews with park rangers and hunting guides, probablycaptured the highest anthropogenic lead concentrations or at least a goodrepresentation of these levels.

In order to determine lead concentration and changes between the pre-huntingseason (PreHS) August 2009 and the post-hunting season (PostHS) February 2010,cores of 30 cm in length and 10 cm wide were taken at each of the six samplingsites during each season with a PVC corer. Samples were kept refrigerated andcarefully transported to the laboratory. Overlying water physicochemical para-meters, (pH, temperature, conductivity, dissolved oxygen and redox potential) wereobtained in situ using a portable multiparameter instruments YSI 85 and HachHQ40d. Water depth was obtained with a measuring tape.

2.2. Total lead concentration, organic matter, and fine grain percentage

Cores were divided into segments from the top of the core downward at0–3 cm, 3–6 cm, 6–10 cm, 10–15 cm, 15–20 cm, and 20–30 cm. Sediment sectionswere homogenized and freeze dried in a Labconco FreeZone 2.5 freeze dryer. Grainsize was obtained by sieve analyses, using a stack of sieves of various mesh size upto 230 mesh to separate fine grain particles. The sum of the percentage of particleso0.065 mm were considered as fine grain. Percentage of organic matter insediment samples was determined using the Walkley and Black wet oxidationmethod (Franco et al., 1985). Homogenized samples were inspected for macro-scopic lead shot (40.1 cm).

Total lead was determined in triplicate (i.e., three individual digestions for eachcore segment) using the o0.065 mm fraction from the homogenized samples(thus, intact lead shot was not include in the atomic absorption analysis) accordingto Rubio and Ure (1993), and using the method proposed by Loring and Rantala(1992). The average standard deviation per segment was 4.2 percent (lowest value2.4 percent, highest value 7.7 percent, N¼36). All subsequent analyses wereperformed using the triplicate average for each segment. Analytical quality ofanalysis was obtained by using a NIST SRM 1646a Estuarine Sediment. A mean of10.64 μg g�1 with a 0.55 μg g�1 standard deviation was obtained. Mean percen-tage recovery was 94.90 percent with a standard deviation of 7.3 percent. PerkinElmer lead atomic spectroscopy standard (N9300175) was used for quantification.

2.3. Geochemical fractionation and bioavailable lead

Geochemical fractionation was performed using the BCR (European Commu-nity Bureau of Reference) technique (Rauret et al., 1998) and bioavailable lead wasobtained according to Kwon and Lee's (2001) method.

2.4. Multivariate analyses

Multivariate exploratory techniques were used to identify the origin of lead atEl Palmar, and the influence of the geochemical and physicochemical variables ofthe environment on the geochemical fractionation. The statistics program STATIS-TICA StatSoft was used and the analyses performed were correlation, cluster, andfactor analyses.

3. Results and discussion

3.1. Concentrations and sources of lead

Lead shot is not environmentally stable or inert and could be asource of contamination and food chain transfer. Once in theenvironment, it may be transformed into particulate and molecu-lar lead species that form preferentially oxides and carbonates(Scheuhammer and Norris, 1996, Sadiq, 1992). Lead baselineconcentration in sediments is around 3–10 μg g�1 (Fig. 1a–f; seeconstant lead concentration found in the core sediments at a

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depth of 15–30 cm). However, the top 10 cm of the El Palmarwetland has been significantly contaminated by Pb. Lead concen-trations are two to twenty times greater than in non-pollutedcoastal environments (Sadiq, 1992), and are one to ten timesgreater than baseline concentrations (taken at a depth of15–30 cm). Such pollution levels are most likely related to huntingactivities in this case (c.f., Ancora et al., 2008; Peterson et al., 1993)especially at EP5 and EP6 (see below). Also, according to NOAASquiRTs (Screening quick reference tables for inorganics –

Buchman, 1999), lead concentrations for the collected coresin this study range from below the minimum infaunal communityeffect level (30.24 μg g�1) during the pre-hunting season,to bordering the probable infaunal community effect level(112.18 μg g�1) during the post-hunting season. Thus, this degreeof Pb contamination within 10 cm of the surface means thatanimals living and feeding in El Palmar wetland could be directlyexposed to lead.

For EP1 (Fig. 1a), there is a depletion of lead concentrations (seelower value at 3 cm) in the post-hunting season, which is mostlikely the result of a recent cessation in hunting activities. Thehigher concentration peak found at a depth of 6 cm supports thisconclusion. At EP2 (Fig. 1b), EP3 (Fig. 1c), and EP5 (Fig. 1e),a significant increase in lead concentrations was found in theupper 10 cm. For EP4 (Fig. 1d) and EP6 (Fig. 1f), this increase waspresent only in the first 6 cm. This increase was present during thepost-hunting season suggesting a probable relation to huntingactivities. The clearest example of this is site EP5 (Fig. 1e), wherePb increased more than 40 μg g�1 from the pre- to the post-hunting season.

Li concentration was used to determine if Pb in the sedimentcores is natural or anthropogenic (see Loring and Rantala, 1992).Dispersion analyses showed that lead concentrations within thesix cores do not have a relationship with Li during either the pre-or post-hunting seasons (PreHS r¼0.2518; PostHS r¼0.3456,

p40.05 for both seasons). The outliers correspond to the 0–6 cmdata for EP4 and EP6 and for 0–10 cm data at EP5. These dataindicated that lead present in the first 10 cm of the sedimentarycolumn at El Palmar is primarily anthropogenic (Loring andRantala, 1992). The absence of nearby point sources (closest otherprobable source is 4.4 km away form EP1) coupled with thepresence of lead shot 40.1 cm (at stations EP5 and EP6) indicatesthat the most likely principal source is hunting.

This conclusion is consistent with other studies of lead deposi-tion from firearms and hunting. Depth and density of lead shot inthe homogenized samples (at EP5, a single shot at a depth of0–3 cm and another one at 3–6 cm; and at EP6, a single shot at0–3 cm) is consistent with studies by Pain (1991) and Mateo et al.(2005). Specifically, Pain (1991) found, in controlled experimentsof lead shot densities and settlement rates, that 497 percent ofshot remained in the upper 6 cm of sediment. A finding consistentwith our data, since lead shot was not recovered below a depth of6 cm. Furthermore, Mateo et al. (2005) found densities (0–25 shotpellets m�2 in the top 6 cm) similar to the ones obtained in thisstudy (0–2 shot pellets m�2 in the top 6 cm). Other studies byScheuhammer and Norris (1996) and Storgaard Jorgensen andWillems (1987) indicate that only half of the metallic lead contentof a shot would be transformed into lead compounds within 54–63 years and that total pellet transformation would required 100–300 years.

Given that lead shot, deposited during 30 years of hunting,should reach as much as 23 metric tons and assuming that oursampling stations were well placed considering ethnographicinformation and firing viewsheds, the Pb concentrations reportedhere are much lower than expected (approximating lead concen-tration by quantity of shot per permit [c.f., Pain, 1991]). Therefore,chemical, physical, or biogenic processes may be removing somelead from sediments after it has been deposited during thehunting season. In the following discussion, we evaluate thedegree to which either physico-geochemical or biogenic processesare acting to remove anthropogenic lead from sediments.

3.1.1. Geochemical fractionationA geochemical fractionation was carried out on the first two

sections of the cores, from 0 to 3 cm and from 3 to 6 cm for bothsampling seasons to determine if geochemical conditions werepromoting degradation of lead shot and transformation to solubleor particulate forms that migrate to the water column (c.f.,Scheuhammer and Norris, 1996) (Fig. 2a–f). In general terms, thereis no significant variation (po0.05) between sampling seasons foreach of the sampling sites. Average preferences for geochemicalfractions are as follows: lithogenic4organic matter/sulfur com-pounds4oxyhydroxides4carbonates. A higher percentage oflead bonded to carbonates in this karstic area was expected, sinceArcega-Cabrera et al. (2009) found such a pattern in anotherkarstic area of Mexico. An expectation supported by Sadiq's(1992) observation that lead adsorption onto calcite surfaces

Fig. 1. Variations of lead in pre-hunting season and post-hunting season for:(a) EP1, (b) EP2, (c) EP3, (d) EP4, (e) EP5, and (f) EP6.

Fig. 2. Geochemical fractionation ad bioavailable lead in pre- and post-hunting season at 0–3 cm and 3–6 cm of depth for: (a) EP1, (b) EP2, (c) EP3, (d) EP4, (e) EP5, and(f) EP6.

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may not simply be physical but may involve chemisorption orprecipitation of a new solid phase.

Thus, the high bonding affinity with organic matter or sulfurcompounds in the El Palmar samples was not expected since leadmay exist as cations or complexes and can, therefore, adsorb ontonegatively charged surfaces such as clays, carbonates, and oxidesand hydroxides of Fe and Mn (Sadiq, 1992). But according toCharriau et al. (2011), lead has a weak affinity with carbonates if anundersaturation in pore water (interstitial) is present and a strongaffinity with humic substances, especially the phenolic groups(tannins).

In this case, the mangroves, which are spatially extensive, areproducing high concentrations of humic substances, which are,apparently, preventing lead from becoming bioavailable (undersuch conditions lead will only become bioavailable when majorchanges in pH or redox occur). In addition, anoxic sedimentsulfate-reducing bacteria, present in the study zone, producesulfides that re-oxidize or precipitate metals (Morse and Luther,1999), which contribute to lead stabilization in sediments unlessthe oxic barrier at the water–sediment interface weakens ordisappears. With respect to the affinity for oxide and Fe and Mnhydroxides, Sadiq (1992) suggests that in estuarine sediments Fetends to precipitate as hydroxides because of the freshwater–seawater mixing, and since they are electrically active they canscavenge lead. Therefore, it is probable that the geochemical formsof lead present in El Palmar will remain stable in sediments and itsmobility may be influenced more by geodynamics than by thephysicochemistry or geochemistry of the study zone.

3.1.2. Environmental geochemistry of leadIn order to ascertain if geochemical conditions at the time of

sampling were, in fact, impeding the release of lead from sedi-ments to the overlying water column, the potential mobility oflead at the sediment-aqueous boundary was evaluated. Accordingto Salomons (1995), the mobility of metals is determined by pH,redox conditions, and the presence of complexing agents such asdissolved organic matter and inorganic anions. He refers to theseparameters as “capacity controlling parameters” or “master vari-ables”. In order to approximate the influence of these mastervariables (Fig. 3a–f,) on lead behavior, at the boundary layerbetween the surface of the sediments and the overlying watercolumn, during both sampling seasons, multivariate exploratorytechniques were used. At EP4 (Fig. 3d) and EP5 (Fig. 3e), no data onthe water variables were collected because these sites were waterdepleted (dry season). Only organic matter content and fine grainsediments were obtained. These sites show extreme variation insalinity and conductivity as is expected for a seasonal wetland(Herrera-Silveira, 2006). Also, the high content of organic matterand fine grain sediments promote reducing conditions.

A cluster analysis was performed to indentify groupingbetween sampling sites and seasons (Fig. 4). Ward's method with

Pearson's correlation was used in order to obtain the highestlikeliness between each member of a given group. This analysisincluded the variables: lead, salinity, pH, Eh, dissolved oxygen,temperature, conductivity, organic matter content, and fine grainpercentage. Its objective is to approximate a probable scenario forlead mobility between surface sediments and overlying water,according to the physicochemical wetland seasonal variation (seesimilar studies by Langston, 1990; Santschi et al., 1990; Bryan andLangston, 1992; Arcega-Cabrera et al., 2009; Zhao et al., 2013).Such mobility would deliver bioavailable lead into open water andthreaten all species living in this habitat (Dong, 2002; Zhou, 2002;Lee et al., 2008).

Two groups were formed, which separates pre-hunting seasonfrom post-hunting season sites. EP4 and EP5 are absent since theywere dry, and no physicochemical parameters could be taken.Case wise deletion was applied and these two sites were elimi-nated from cluster analysis. Significant differences (po0.05) in thephysicochemical and geochemical parameters were presentbetween the pre-and post-hunting seasons at the time of sam-pling. Thus, after grouping results, separate multivariate analyseswere performed for each seasonal group.

A factor analysis was carried out for each of the two groups.Table 1 presents the results for the pre-and post-hunting seasons.For the pre-hunting season, two factors explain 85 percent of thetotal variability of the observed process. Factor 1 (63 percent oftotal variability) represents the probable physicochemical pro-cesses involved in the formation of insoluble complexes of lead,which showed a direct, significant, relation with salinity, conduc-tivity, and temperature. Most of the lead in the environment is inan inorganic form. Thus, in brackish or marine environments, ittends to accumulate in sediments where complexes can form inthe presence of chlorides, sulfates, and carbonates. Where fresh-water and seawater mix, free Pb2þ disappears and Pb-chlorocomplexes are formed (Sadiq, 1992). As expected, lead and waterpH are inversely related because under low pH and moderateto high redox conditions solubilization of metals is expected(Bourg and Loch, 1995). Eh in the overlying water shows areductive environment, this along with the presence of organicmatter and fine grain sediments (Factor 2, 22 percent of totalvariability), may be promoting the formation of sulfide complexes.These complexes have an extremely low solubility and may be

Fig. 3. Variations of physicochemical and geochemical variables at both samplingseason in the six (a–f) sampling sites.

Fig. 4. Grouping of sampling sites and seasons of the El Palmar wetlands using Pbconcentration, salinity, pH, Eh, dissolved oxygen, conductivity, organic mattercontent and fine grain percentage as variables for analysis. Ward's method withPearson's correlation was used to secure highest likeness of groups. EP4 and EP5pre-hunting season sites are not shown since no water was present and case wisedeletion was used.

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precipitating into the sediment. Such redox conditions, whichdetermine mobility, are largely controlled by bacterial decomposi-tion of organic matter (Salomons, 1995), which can in turn explainthe relationship with temperature. Together, these data indicatethat physicochemical processes, Eh, organic matter, and fine grainsediments are working together to keep lead from degrading to itschemical form during the pre-hunting season.

For the post-hunting season, two factors explain 86 percent ofthe variability of the observed process. Factor 1 (49 percent of totalvariability) consists of a series of variables related to the filling ofthe wetland by freshwater from pluvial precipitation and theaquifer's hydraulic head. Consequently, an inverse relationshipwith depth (more water), lower salinity, and conductivity results.Lead in sediments is directly related to these parameters since adepletion of lead (assuming entering waters have lower concen-trations than the ones found at El Palmar) in interstitial oroverlying waters will promote a desorption to the water column.But, it is more probable that this factor could be promoting theformation of insoluble compounds such as Pb(OH)2, PbO, PbSO4, orPb5(PO4)3Cl, Pb2(CO3)Cl2 and in anoxic sediments PbS (Sadiq,1992), given the direct relationship with pH and DO and theindirect relation with Eh in Factor 2 (37 percent of total varia-bility). Also an inverse relationship between fine grain sedimentsand lead was found, which is probably associated with theresuspension of the sediments as the result of both anthropogenicand biogenic activities during this particular season. As in thepre-hunting season, environmental conditions are blocking thedegradation of lead and its entry into the food chain duringthe post-hunting season.

From these analyses, it may be concluded that both physico-chemical and geochemical variables are controlling the retentionof lead probably by absorption on to inorganic anions and poster-ior precipitation in the study area. Whereas, dissolved complexa-tion, probably with organic compounds, influences advective anddispersive transport (Salomons, 1995). Also, it is highly probablethat lead in the Pb2þ form, which is considered the most toxicinorganic form for estuarine and marine organisms, decreases intoxicity since an inverse relationship exists between toxicity andsalinity, suspended particles, alkalinity and concentrations oforganic matter (Sadiq, 1992). Thus, assuming relative stabilitywithin individual seasons, these data indicate that physicochem-ical and geochemical conditions are impeding the release of leadfrom the surface of sediments into overlying water. However,conditions could potentially vary dramatically within one seasonand our preliminary multivariate analysis provides a basis forpostulating the magnitude of changes necessary to release lead tothe water column for future research.

3.2. Bioavailability of lead

Regarding the bioavailability of lead, defined as the sum of thelead bound to the carbonates, Fe and Mn oxy-hydroxides, and theorganic matter and sulfur compounds fraction, the results showedthat bioavailable lead is above 50 percent. Metals weakly boundwith carbonates may equilibrate with aqueous phase thus becom-ing more rapidly bioavailable (Gibbs, 1977) followed by the oxy-hydroxides fraction and the organic matter and sulfur fraction.Whereas, metals present in the lithogenic fraction can be taken asa measure of the contribution by natural sources (Salomons andForstner, 1980). The risk assessment code states that a sedimentwith a sum of more than 50 percent of metal bounded to thecarbonates, oxy-hydorides or sulfur and organic matter fraction,has to be considered highly dangerous and can easily enter thefood chain (Perin et al., 1985; Jain, 2004).

Therefore, under these conditions, all of El Palmar reserve ispotentially threatened by bioavailable lead. Nevertheless, lead'srelease to the water column is not likely because of its chemicalcharacteristics, since the greater percentage of Pb, in naturalenvironments, is present as a Pb2þ species; so, it tends to occuras hydroxy or polynuclear species and not as a dissolved elementin the water column (e.g., Burguess, 1978; Claudio et al., 2003).A finding consistent with the geochemical analysis, which showedthat transformation to soluble or particulate Pb forms is probablynot a significant process in El Palmar wetland.

3.3. Discussion

The preceding study has demonstrated that the top 10 cm ofsediment in El Palmar wetland is contaminated with lead and thatconcentrations are two to twenty times higher than non-pollutedcoastal wetlands and one to ten times higher than local baselines(recovered at a depth of 15–30 cm). It has also demonstrated thatthe source of this lead is anthropogenic and the primary sourceis probably from hunting. Analysis of geochemical fractionation,the environmental geochemistry, and the bioavailability of lead allsuggest that lead is remaining in particulate form and not enteringthe water column and, thus, the trophic web.

However, the analysis showed that in the most heavily huntedareas, Pb concentrations are just barley nearing the probable effectlevel for the infaunal community (112.18 μg g�1), despite 30 yearsof hunting that should have already resulted in extremely highlead concentrations. Consequently, it appears that organisms livingand feeding in the top 10 cm of sediment are consuming particu-late lead and intact lead shot at very high rates and removingit from the sediment. A conclusion supported by the fact thatexamination of deceased flamingos, following Hurricane Gilberto,revealed massive ingestion of lead shot (Schmitz et al., 1990) andthe fact that field observations indicate that flamingos are livingand feeding at the sampling stations. Furthermore if lead shotcontinues in use in El Palmar, Pb concentrations could reachextremely polluted levels in the short-term future, placing eco-nomically important species (e.g., flamingo and duck), as well asthe entire El Palmar ecosystem, at severe risk. Therefore, the use ofalternative metals for shot such as Fe, Mo, Ni, Bi, Zn, and Sn(Schnug and Haneklaus, 2000) should be requested and/or pro-moted by the local authorities as it has been in other parts of theworld (e.g., Fisher et al., 2006).

4. Conclusions

Total concentrations of lead in El Palmar are in the range fromlow to moderately polluted. Moreover, they are found in thesurface sediments where benthonic species, including protected

Table 1Factor analyses for the pre- and post-hunting seasons sampling. Totl. Prp.¼totalproportionality. N¼10.

Variable Pre-hunting season Post-hunting season

Factor 1 Factor 2 Factor 1 Factor 2

pH 0.89 �0.38 �0.09 0.99Eh �0.89 0.38 0.09 �0.99DO 0.33 0.03 0.65 0.72Temperature �0.98 �0.13 0.98 �0.18Salinity �0.91 0.38 0.89 0.31Conductivity �0.99 0.05 0.99 0.05Depth 0.94 �0.19 �0.83 �0.1Organic Matter 0.13 0.90 �0.32 0.82Fine grain 0.25 �0.92 �0.19 �0.95Pb �0.95 �0.26 0.93 0.12Totl. Prp. 0.63 0.22 0.49 0.37

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and economically important species like pink flamingo, live andeat. This research determined that lead concentrations arebetween two and twenty times greater than baseline concentra-tions for unpolluted costal environments. It also indicates thathunting activities with firearms may be the most likely source oflead since lead shot is limited to the top 6 cm, density of shot iscomparable to other cases of lead contamination by hunting, andlead concentrations show their greatest values during the post-hunting season and have no relation with Li (used as a naturaltracer).

Geochemical fractionation demonstrated that non-lithogeniclead prefers to bind to organic matter, as well as probably forminginsoluble complexes with sulfides in the anoxic reductive sedi-mentary environment. Although Fe and Mn oxyhydroxides alsoplay an important role. Surprisingly, carbonates were the leastimportant fraction to which lead prefers to adsorb. These tworesults suggest that lead in sediments will not be easily released tothe overlying water column, unless significant Pb water depletionor physicochemical changes take place.

Almost all the sampling sites had 450 percent of bio-available lead. However, considering the chemistry of this metaland the benign physicochemical and geochemical characteris-tics of the environment, we can suggest that the main potentialhazard to the environment from lead may be lead shot ingestionand not transfer of Pb from sediments to the overlying watercolumn.

More research into the distribution and density of Pb shot andingestion is needed to conclude that lead poisoning in waterfowl isa significant process and, that it is related to the presence of leadshots in sediments. Nevertheless, this research suggests a potentialenvironmental threat for biota living/feeding in the sediments;therefore, the authors recommend that hunters should be requiredto use alternatives to lead shot, as a preventing measure.

Acknowledgments

The authors wish to thank CONACyT-SEP-CB (Project 101720)and the PAIP 9700-02 Facultad de Química, UNAM for funding thisproject. We also thank Fernando Mex Esquivel, the local huntingguides from Sisal, and officials from SEDUMA for their help duringthe sampling campaign. The authors thank Dr. Lane F. Fargher,Dr. James M. Fargher and Mrs. Georgann P. Fargher for their helpwith editing our English. The authors also thank the reviewers fortheir insightful remarks that significantly improve the quality ofthe article.

Appendix A. Supplementary material

Supplementary data associated with this article can be found inthe online version at http://dx.doi.org/10.1016/j.ecoenv.2013.11.002.

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