Research Article Effluents of Shrimp Farms and Its ...

9
Hindawi Publishing Corporation e Scientific World Journal Volume 2013, Article ID 306370, 8 pages http://dx.doi.org/10.1155/2013/306370 Research Article Effluents of Shrimp Farms and Its Influence on the Coastal Ecosystems of Bahía de Kino, Mexico Ramón H. Barraza-Guardado, 1,2 José A. Arreola-Lizárraga, 3 Marco A. López-Torres, 2 Ramón Casillas-Hernández, 1 Anselmo Miranda-Baeza, 4 Francisco Magallón-Barrajas, 3 and Cuauhtemoc Ibarra-Gámez 1 1 Instituto Tecnol´ ogico de Sonora (ITSON), 85000 Ciudad Obreg´ on, SON, Mexico 2 Departamento de Investigaciones Cient´ ıficas y Tecnol´ ogicas de la Universidad de Sonora (DICTUS), 83000 Hermosillo, SON, Mexico 3 Centro de Investigaciones Biol´ ogicas del Noroeste, S.C. (CIBNOR, S.C.), 85454 Guaymas, SON, Mexico 4 Universidad Estatal de Sonora (US), 85800 Navojoa, SON, Mexico Correspondence should be addressed to Jos´ e A. Arreola-Liz´ arraga; [email protected] Received 23 March 2013; Accepted 5 May 2013 Academic Editors: F. Amezcua-Mart´ ınez, M. G. Frias-Espericueta, J. R. Ruelas-Inzunza, M. F. Soto-Jimenez, and M. Teichberg Copyright © 2013 Ram´ on H. Barraza-Guardado et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. e impact on coastal ecosystems of suspended solids, organic matter, and bacteria in shrimp farm effluents is presented. Sites around Bah´ ıa de Kino were selected for comparative evaluation. Effluent entering Bahia Kino (1) enters Laguna La Cruz (2). A control site (3) was outside the influence of effluents. Water quality samples were collected every two weeks during the shrimp culture period. Our data show that the material load in shrimp farm effluents changes biogeochemical processes and aquatic health of the coastal ecosystem. Specifically, the suspended solids, particulate organic matter, chlorophyll a, viable heterotrophic bacteria, and Vibrio-like bacteria in the bay and lagoon were two- to three-fold higher than the control site. is can be mitigated by improvements in the management of aquaculture systems. 1. Introduction Worldwide, brackish-water aquaculture production (4.7 mil- lion tons) consisted of crustaceans (57%), freshwater fishes (19%), diadromous fishes (15%), marine fishes (7%), and marine mollusks (2%) in 2010; more than 99 percent of the crustaceans were marine shrimps [1]. It shows the importance of research about the effect of shrimp farming on the environment [2], with water pollution from shrimp pond effluents as the most common complaint [35]. is activity depends directly or indirectly on a range of coastal and marine ecosystem services some of which may be used at rates that are not sustainable [6, 7]. Most of shrimp production is carried out in ponds. e most common shrimp aquaculture systems use inland ponds that are near or on the coast. Water is discharged from these shrimp ponds to coastal ecosystem as part of the water exchange when ponds are drained. e main components in the shrimp farm effluents are organic matter mainly in particulate form from different sources, as well as nitrogen and phosphorus in both organic and inorganic forms, and suspended solids [8, 9]. Production systems in the culture of marine shrimp, semi-intensive or intensive, lead to significant increases in the levels of nutrients, phytoplankton biomass, organic matter, and suspended solids in the environment receiving the farm’s effluents [1013]. In addition, it has been reported that water quality shows short term increases in parameters of water bodies receiving shrimp discharge waters, but other studies indicate that there are no significant differences over back- ground levels on an annual basis [14, 15]. e impact of pond effluents on adjacent ecosystems is variable and depends on various factors, including the magnitude of the discharge, the chemical composition of the pond effluents, and the specific characteristics of the environment that receives the discharge, such as circulation and dilution rates [16].

Transcript of Research Article Effluents of Shrimp Farms and Its ...

Page 1: Research Article Effluents of Shrimp Farms and Its ...

Hindawi Publishing CorporationThe Scientific World JournalVolume 2013 Article ID 306370 8 pageshttpdxdoiorg1011552013306370

Research ArticleEffluents of Shrimp Farms and Its Influence on the CoastalEcosystems of Bahiacutea de Kino Mexico

Ramoacuten H Barraza-Guardado12 Joseacute A Arreola-Lizaacuterraga3 Marco A Loacutepez-Torres2

Ramoacuten Casillas-Hernaacutendez1 Anselmo Miranda-Baeza4 Francisco Magalloacuten-Barrajas3

and Cuauhtemoc Ibarra-Gaacutemez1

1 Instituto Tecnologico de Sonora (ITSON) 85000 Ciudad Obregon SON Mexico2Departamento de Investigaciones Cientıficas y Tecnologicas de la Universidad de Sonora (DICTUS)83000 Hermosillo SON Mexico

3 Centro de Investigaciones Biologicas del Noroeste SC (CIBNOR SC) 85454 Guaymas SON Mexico4Universidad Estatal de Sonora (US) 85800 Navojoa SON Mexico

Correspondence should be addressed to Jose A Arreola-Lizarraga aarreola04cibnormx

Received 23 March 2013 Accepted 5 May 2013

Academic Editors F Amezcua-Martınez M G Frias-Espericueta J R Ruelas-Inzunza M F Soto-Jimenez and M Teichberg

Copyright copy 2013 Ramon H Barraza-Guardado et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The impact on coastal ecosystems of suspended solids organic matter and bacteria in shrimp farm effluents is presented Sitesaround Bahıa de Kino were selected for comparative evaluation Effluent entering Bahia Kino (1) enters Laguna La Cruz (2) Acontrol site (3) was outside the influence of effluents Water quality samples were collected every two weeks during the shrimpculture period Our data show that the material load in shrimp farm effluents changes biogeochemical processes and aquatichealth of the coastal ecosystem Specifically the suspended solids particulate organic matter chlorophyll a viable heterotrophicbacteria and Vibrio-like bacteria in the bay and lagoon were two- to three-fold higher than the control site This can be mitigatedby improvements in the management of aquaculture systems

1 Introduction

Worldwide brackish-water aquaculture production (47 mil-lion tons) consisted of crustaceans (57) freshwater fishes(19) diadromous fishes (15) marine fishes (7) andmarine mollusks (2) in 2010 more than 99 percent of thecrustaceansweremarine shrimps [1] It shows the importanceof research about the effect of shrimp farming on theenvironment [2] with water pollution from shrimp pondeffluents as the most common complaint [3ndash5] This activitydepends directly or indirectly on a range of coastal andmarine ecosystem services someofwhichmay be used at ratesthat are not sustainable [6 7]

Most of shrimp production is carried out in ponds Themost common shrimp aquaculture systems use inland pondsthat are near or on the coast Water is discharged fromthese shrimp ponds to coastal ecosystem as part of the waterexchange when ponds are drained The main components

in the shrimp farm effluents are organic matter mainly inparticulate form from different sources as well as nitrogenand phosphorus in both organic and inorganic forms andsuspended solids [8 9]

Production systems in the culture of marine shrimpsemi-intensive or intensive lead to significant increases in thelevels of nutrients phytoplankton biomass organic matterand suspended solids in the environment receiving the farmrsquoseffluents [10ndash13] In addition it has been reported that waterquality shows short term increases in parameters of waterbodies receiving shrimp discharge waters but other studiesindicate that there are no significant differences over back-ground levels on an annual basis [14 15] The impact of pondeffluents on adjacent ecosystems is variable and depends onvarious factors including the magnitude of the discharge thechemical composition of the pond effluents and the specificcharacteristics of the environment that receives the dischargesuch as circulation and dilution rates [16]

2 The Scientific World Journal

The characterization of the shrimp farmrsquos effluents interms of water quality is very important to gauge the envi-ronmental health of an ecosystem in order to achieve a betterregulation of the industry [17 18] Further the continuousmonitoring of the physical chemical and biological param-eters of pond effluent and inlet waters helps not only topredict and control negative conditions for shrimp farmingbut also avoids environmental damages and collapse of theproduction process [19]

In Mexico about 97 of shrimp aquaculture ponds arelocated around the Gulf of California in the states of BajaCalifornia Baja California Sur Sonora Sinaloa and NayaritBeginning in the mid-1980s the Gulf of California ecoregionexperienced an increase in shrimp aquaculture and becamethe second largest producer in the western hemisphere [20]Recently Mexico was the sixth largest producer of shrimpculture worldwide sim110000 t [1] The State of Sonora con-tributed with 37 of this production in 2011 and specificallyBahıa deKino regionwhich is themain shrimp producer [21]

The goals of this study were to examine the effluent loadsfrom shrimp farms and its influence on the coast in Bahıa deKino We measured concentrations of total suspended solidsparticulate organicmatter chlorophyll a viable heterotrophicbacteria and Vibrio-like bacteria in the effluent and in thecoastal ecosystems We then assessed the influence of theseeffluents on the coastal ecosystems

2 Materials and Methods

21 Study Area Bahıa de Kino is located on the Gulf ofCalifornia in the State of SonoraMexico (28∘471015840N 111∘541015840W)Into this bay effluents from 1350 hectares (effluents rate sim160000m3 haminus1 yrminus1) from four shrimp farms that operatefrom April through October are delivered into the bayabout 2 km south of the mouth of the Laguna de la CruzSeawater is taken directly from the open sea for shrimpfarming (Figure 1) Bahıa de Kino has a seasonal patternof water temperature a maximum of 322∘C in August andminimum of 156∘C in January Salinity varies from 35ndash383[22] This region has a dry desert climate with evaporation ofsim3000mmyrminus1 which exceeds rainfall of lt300mmyrminus1 [23]

22 Sampling andMeasurements Water quality was sampledevery two weeks at 12 sampling stations in June Septemberand October (2009) the period when the most effluents andorganic matter from partial and final harvest of shrimp takesplace

A control station outside the influence of the shrimpeffluents (sim6 km) was located at Isla Alcatraz four stationswere established in the southern part of the bay near the outletof the effluents three stations were established in the effluentchannel and four stations were established inside Laguna laCruz (Figure 1)

Water samples were taken between 0700 and 1300 h Ateach station water was collected near the surface in 1 L plasticbottles these samples were used tomeasure suspended solidschlorophyll a and pH Samples for study of bacteria were

collected in sterile 120mLWhirl pack bags All samples weretransported to the laboratory in ice

At each station temperature dissolved oxygen and salin-ity were measured (YSI field oxygen meter 85 YSI YellowSpringsOH)water transparencywasmeasuredwith a Secchidisk and pH was measured in the laboratory with pH meter(model 220A Hanna Instruments Woonsocket RI)

23 Water Quality Analysis The water samples collected forthe analysis of suspended solids and organic matter werefiltered through precombusted and preweighed WhatmanGFC (Whatman International Ltd) glass fibers Then thefilters were dried in an oven at 60∘C for 24 h and weighedto determine total suspended solids (TSS) for particulateorganic matter (POM) estimation (ash-free dry weight)filters and suspended material were then ignited to constantweight at 550∘C for 8 h and weighed again Inorganic sus-pended solids (ISSs) were estimated by subtracting the valueof POM on the TSS [24] Samples for analysis of chlorophylla were collected by filtration through Whatman GFC glassfibre filters extracted with 90 vv acetone andmeasured byspectrophotometry according to [25]

For the quantification of culturable bacteria includingviable heterotrophic bacteria (VHB) andVibrio-like bacteria(VLB) the spread plate method [26 27] in Marine Agar 2216and Thiosulfate-citrate-bile-sucrose agar (TCBS DIFCOUSA) was used A 10-fold dilution series were preparedwith30 of sterile seawater diluted with distilled waterThe plateswere incubated for 48 plusmn 2 h to 30 plusmn 2∘C and the bacterialcolonies were counted and reported as colony-forming unitsfor mLminus1 (CFUmLminus1)

24 Statistical Data Analysis We used multivariate mul-tidimensional and nonparametric scaling of data whichwas transformed (log119909 + 1) and standardized to determinewhether the sites (island effluent bay and lagoon) weresimilar in terms of water quality Statistical software (Primer-E 60 Primer-E Ivybridge UK) was used to perform theanalyses

The data grouped by area (island effluent bay andlagoon) were subjected to a normality and equal variancetest [28] After this parametric tests were made through aone way ANOVA with its respective Tukey test of multiplecomparisons and also a nonparametric test using one wayANOVAand aKruskal-Wallis a posteriori testwith a 95 levelof significance [29] The NCSS program (2007) was used forstatistical analysis [30]

3 Results

The result from the similarity analysis for the multivariatemethod of nonparametric multidimensional scaling (nMDS)indicated a difference of similarity among the study areas(Figure 2) Effluents and water quality parameters near theisland had lower similarity while the bay and lagoon hadsimilar water quality conditions but differed from the waterquality conditions of the effluent

The Scientific World Journal 3

North

USA

SonoraN

Gulf of CaliforniaPacificOcean

Water inlet

Dischargeoutlet

Shrimpfarms

LagunaLa Cruz

(km)0 1 2 5

111∘55998400

111∘50998400

111∘50998400

111∘55998400

28∘45998400

28∘50998400

28∘45998400

28∘50998400

Bahıa de Kino

Figure 1 Bahıa Kino area including Laguna La Cruz and Isla de Alcatraz showing seawater inlet to shrimp farms and discharge channel tothe bay

Transform log(119883 + 1)NormaliseResemblance D1 euclidean distance

2D stress 01

IslandEffluent

LagoonBay

Figure 2 nMDS ordination of water quality parameters for thestudy areas Temperature salinity dissolved oxygen suspendedsolids particulate organicmatter chlorophyll aVibrio-like bacteriaand viable heterotrophic bacteria were included in the multivariateanalysis

The average water temperature during all the time of thestudy on the island was 273 plusmn 33∘C effluent of 248 plusmn 53∘Cat the bay of 255 plusmn 46∘C and the lagoon of 266 plusmn 44∘Cwithout showing any statistical differences among areas (119867 =527 119875 = 015) (Table 1) However a seasonal behavior was

Table 1 Average values (plusmnSD) of physicochemical parameters fordifferent parts of the study area during discharge of effluent

Areas Temperature(∘C) Salinity Dissolved oxygen

(mg Lminus1) pH

Island 273 plusmn 33a 367 plusmn 04a 66 plusmn 12b 83 plusmn 01a

Effluent 248 plusmn 53a 393 plusmn 13b 45 plusmn 14a 82 plusmn 02a

Bay 255 plusmn 46a 372 plusmn 06a 57 plusmn 09b 82 plusmn 02a

Lagoon 266 plusmn 44a 372 plusmn 04a 60 plusmn 06b 82 plusmn 01a

Different letters among areas for each parameter indicate significant differ-ences (119875 lt 005 119899 = 96)

observed when high temperatures were recorded in June andSeptember and the lowest in October

Salinity values were found significantly higher (119865 = 745119875 lt 0001) in the effluent (393 plusmn 13) over the island (367 plusmn04) bay (372 plusmn 06) and lagoon (372 plusmn 04) (Table 1) Itwas noted that the bay lagoon and the control area (island)remained similar in salinities among them

In the effluent significantly lower values of DO (45 plusmn13mgLminus1) (119865 = 202 119875 lt 0001) were found in comparisonto the rest of the other study areas (Table 1) No significantdifferences were found (119875 gt 005) of DO among theisland bay and lagoon areas The pH did not show statisticaldifferences among the areas studied (119867 = 441 119875 = 022)(Table 1)

Water transparency had average values on the islandeffluent bay and lagoon of 25 plusmn 08 02 plusmn 01 09 plusmn 04

4 The Scientific World Journal

Tran

spar

ency

(m)

Island Effluent Bay Lagoon

4

3

2

1

0

a

bb

c

(a)

TSS

(mg Lminus1)

Island Effluent Bay Lagoon

400

300

200

100

0a

b b

c

(b)

Island Effluent Bay Lagoon

400

300

200

100

0

a

b b

c

ISS

(mg Lminus1)

(c)

Figure 3 Average values (plusmnSD) of selected variables (a) Water transparency (b) total suspended solids and (c) inorganic suspended solidsDifferent letters among zones for each variable indicate significant differences (119875 lt 005)

and 09 plusmn 04m respectively (Figure 3) Significantly lowervalues were recorded in the effluent and higher on the island(119865 = 3405 119875 lt 0001) Water transparency both in the bayand lagoon had intermediate values not statistically differentbut significantly lower than the island (Figure 3)

The average concentration of total suspended solids(TSS) was found to be 267 plusmn 12mgLminus1 in waters near theisland (control area) 2332 plusmn 957mgLminus1 in the effluent area562 plusmn 451mgLminus1 in the bay and 527 plusmn 306mgLminus1 in thelagoon The inorganic suspended solids (ISSs) showed thesame pattern as TSS Both TSS and ISS presented averagessignificantly (TSS 119867 = 3315 and 119875 lt 0001 ISS 119867 =3314 and 119875 = 0001) lower in the island and higher in theeffluent with intermediate values in both bay and lagoon butsignificantly higher than near the island (Figure 3)

Particulate organicmatter (POM) had average concentra-tions near the island of 462plusmn051mgLminus1 261plusmn92mgLminus1 ineffluent zone 71plusmn 42mgLminus1 in the bay and 70 plusmn 27mgLminus1in the lagoon Significantly higher values (119867 = 3107 119875 lt0001) of POM were observed in the effluent zone and lowerones near the island while POM values in both bay andlagoon remained similar it was observed that the lagoonpresented higher levels than the island (Figure 4)

Chlorophyll a concentration in the control area (island)had average values of 23 plusmn 07mgmminus3 a value which issignificantly (119867 = 3872 119875 lt 0001) lower when itis compared with the other areas (Figure 4) By contrastsignificantly higher values (119875 lt 0001) were found inthe effluent zone during the complete culture period with

219plusmn67mgmminus3 Chl a of bay (48plusmn14mgmminus3) and lagoon(75 plusmn 37mgmminus3) was maintaining similar values

The average concentration of viable heterotrophic bacte-ria (VHB) in the control area (island) was of 564 times 102 plusmn035times10

1 CFU mLminus1 while effluent was of 907times103plusmn024times10

1 CFU mLminus1 bay 176 times 103 plusmn 020 times 101 CFUmLminus1 andlagoon 311times103plusmn018times101 CFUmLminus1 Significantly higherconcentrations (119867 = 4576 119875 lt 0001) were quantifiedin the effluent zone and lower ones near the island Therewas no difference in VHB between island and bay whereasconcentrations in the lagoon were higher than both islandand bayTheVibrio-like bacteria (VLB) presented the same asthan the viable heterotrophic bacteria (119867 = 506 119875 lt 0001)(Figure 5)

4 Discussion

The multivariate analysis (nMDS) showed that water con-ditions varied considerably among the four areas especiallybetween the sites in the effluent channel and the other areasThe effluent had no effect on water quality in the controlarea The bay and lagoon are similar because there is a largeexchange of materials between the two areas mainly fromtidal exchange Our results suggested that pollutants from theshrimp farm influence environmental conditions in the bayand lagoon

41 Water Quality of Shrimp Farmrsquos Effluents Low dissolvedoxygen (DO) in the effluent results from a heavy load of

The Scientific World Journal 5

Island Effluent Bay Lagoon

40

30

20

10

0

abab

cPO

M (m

g Lminus1)

(a)

Island Effluent Bay Lagoon

40

30

20

10

0

a

bb

c

Chla

(mg mminus3)

(b)

Figure 4 Average values (plusmnSD) of selected variables (a) Particulate organic matter and (b) chlorophyll a Different letters among zones foreach variable indicate significant differences (119875 lt 005)

1

15

2

25

3

35

4

45

Island Effluent Bay Lagoon

a

c

a

c

ab

VLB VHB

a

b

Island Effluent Bay Lagoon

Log

CFU

mLminus1

Figure 5 Average concentration (plusmnSD) of Vibrio-like bacteria (VLB) and viable heterotrophic bacteria (VHB) in the different areas of studyDifferent letters among zones for each group of bacteria indicate significant differences (119875 lt 005)

organic matter generated in the shrimp farms [8 9 31 32]which includes unconsumed shrimp food detritus phyto-plankton zooplankton and bacteria The level of oxygen atthe discharge outlet at the bay was 45 plusmn 14mgLminus1 withinthe range of water quality standards for shrimp farm effluentsrecommended by the Global Aquaculture Alliance [33]

Effluent was highly saline because of the high evaporationrates in the shrimp ponds in this subtropical desert regionwhich is consistent with [34] who report salinity 40ndash42in effluents in this region The suspended solids (TSS andISS) increased during the course of effluent water flowbecause the bottom sediments were resuspended and thechannel walls were eroded The effluent was less transparentcaused by the concentrations of suspended solids POM andphytoplankton biomass

Water quality standards for shrimp farm effluents recom-mended by the Global Aquaculture Alliance for TSS has astandard of lt100mg Lminus1 and a target standard of lt50mg Lminus1[33] Effluents discharging into Bahıa de Kino had TSSconcentrations of 2332 plusmn 957mgLminus1

High phytoplankton biomass and organic matter ob-served in the wastewater is promoted by inorganic fertilizersin the cultivation system With current management prac-tices the ponds are rich in phytoplankton and organicmatterand this water is later discharged [11 13 15 35]

Microorganisms in general and bacteria in particular arekey elements in the marine ecosystems operation and reactquickly to changes in environmental parameters [36 37]Thequantity of bacteria is an important variable in monitoringof shrimp farm effluent Vibrio bacteria are opportunisticpathogens in shrimp farms at the larval and grow-out stagesit is the most serious pathogen causing up to 100 mortality[38ndash40]

In summary our results showed that shrimp farm efflu-ents reaching the bay have higher concentrations of TSSPOM phytoplankton biomass and bacteria than the baythis is consistent with observations in other studies [10ndash13 15] The control site at the island had low concentrationsof TSS POM phytoplankton biomass and bacteria thus theeffluent loadings are still a good indicator of likely impact

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

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MeteorologyAdvances in

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

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Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

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Environmental Chemistry

Atmospheric SciencesInternational Journal of

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ClimatologyJournal of

Page 2: Research Article Effluents of Shrimp Farms and Its ...

2 The Scientific World Journal

The characterization of the shrimp farmrsquos effluents interms of water quality is very important to gauge the envi-ronmental health of an ecosystem in order to achieve a betterregulation of the industry [17 18] Further the continuousmonitoring of the physical chemical and biological param-eters of pond effluent and inlet waters helps not only topredict and control negative conditions for shrimp farmingbut also avoids environmental damages and collapse of theproduction process [19]

In Mexico about 97 of shrimp aquaculture ponds arelocated around the Gulf of California in the states of BajaCalifornia Baja California Sur Sonora Sinaloa and NayaritBeginning in the mid-1980s the Gulf of California ecoregionexperienced an increase in shrimp aquaculture and becamethe second largest producer in the western hemisphere [20]Recently Mexico was the sixth largest producer of shrimpculture worldwide sim110000 t [1] The State of Sonora con-tributed with 37 of this production in 2011 and specificallyBahıa deKino regionwhich is themain shrimp producer [21]

The goals of this study were to examine the effluent loadsfrom shrimp farms and its influence on the coast in Bahıa deKino We measured concentrations of total suspended solidsparticulate organicmatter chlorophyll a viable heterotrophicbacteria and Vibrio-like bacteria in the effluent and in thecoastal ecosystems We then assessed the influence of theseeffluents on the coastal ecosystems

2 Materials and Methods

21 Study Area Bahıa de Kino is located on the Gulf ofCalifornia in the State of SonoraMexico (28∘471015840N 111∘541015840W)Into this bay effluents from 1350 hectares (effluents rate sim160000m3 haminus1 yrminus1) from four shrimp farms that operatefrom April through October are delivered into the bayabout 2 km south of the mouth of the Laguna de la CruzSeawater is taken directly from the open sea for shrimpfarming (Figure 1) Bahıa de Kino has a seasonal patternof water temperature a maximum of 322∘C in August andminimum of 156∘C in January Salinity varies from 35ndash383[22] This region has a dry desert climate with evaporation ofsim3000mmyrminus1 which exceeds rainfall of lt300mmyrminus1 [23]

22 Sampling andMeasurements Water quality was sampledevery two weeks at 12 sampling stations in June Septemberand October (2009) the period when the most effluents andorganic matter from partial and final harvest of shrimp takesplace

A control station outside the influence of the shrimpeffluents (sim6 km) was located at Isla Alcatraz four stationswere established in the southern part of the bay near the outletof the effluents three stations were established in the effluentchannel and four stations were established inside Laguna laCruz (Figure 1)

Water samples were taken between 0700 and 1300 h Ateach station water was collected near the surface in 1 L plasticbottles these samples were used tomeasure suspended solidschlorophyll a and pH Samples for study of bacteria were

collected in sterile 120mLWhirl pack bags All samples weretransported to the laboratory in ice

At each station temperature dissolved oxygen and salin-ity were measured (YSI field oxygen meter 85 YSI YellowSpringsOH)water transparencywasmeasuredwith a Secchidisk and pH was measured in the laboratory with pH meter(model 220A Hanna Instruments Woonsocket RI)

23 Water Quality Analysis The water samples collected forthe analysis of suspended solids and organic matter werefiltered through precombusted and preweighed WhatmanGFC (Whatman International Ltd) glass fibers Then thefilters were dried in an oven at 60∘C for 24 h and weighedto determine total suspended solids (TSS) for particulateorganic matter (POM) estimation (ash-free dry weight)filters and suspended material were then ignited to constantweight at 550∘C for 8 h and weighed again Inorganic sus-pended solids (ISSs) were estimated by subtracting the valueof POM on the TSS [24] Samples for analysis of chlorophylla were collected by filtration through Whatman GFC glassfibre filters extracted with 90 vv acetone andmeasured byspectrophotometry according to [25]

For the quantification of culturable bacteria includingviable heterotrophic bacteria (VHB) andVibrio-like bacteria(VLB) the spread plate method [26 27] in Marine Agar 2216and Thiosulfate-citrate-bile-sucrose agar (TCBS DIFCOUSA) was used A 10-fold dilution series were preparedwith30 of sterile seawater diluted with distilled waterThe plateswere incubated for 48 plusmn 2 h to 30 plusmn 2∘C and the bacterialcolonies were counted and reported as colony-forming unitsfor mLminus1 (CFUmLminus1)

24 Statistical Data Analysis We used multivariate mul-tidimensional and nonparametric scaling of data whichwas transformed (log119909 + 1) and standardized to determinewhether the sites (island effluent bay and lagoon) weresimilar in terms of water quality Statistical software (Primer-E 60 Primer-E Ivybridge UK) was used to perform theanalyses

The data grouped by area (island effluent bay andlagoon) were subjected to a normality and equal variancetest [28] After this parametric tests were made through aone way ANOVA with its respective Tukey test of multiplecomparisons and also a nonparametric test using one wayANOVAand aKruskal-Wallis a posteriori testwith a 95 levelof significance [29] The NCSS program (2007) was used forstatistical analysis [30]

3 Results

The result from the similarity analysis for the multivariatemethod of nonparametric multidimensional scaling (nMDS)indicated a difference of similarity among the study areas(Figure 2) Effluents and water quality parameters near theisland had lower similarity while the bay and lagoon hadsimilar water quality conditions but differed from the waterquality conditions of the effluent

The Scientific World Journal 3

North

USA

SonoraN

Gulf of CaliforniaPacificOcean

Water inlet

Dischargeoutlet

Shrimpfarms

LagunaLa Cruz

(km)0 1 2 5

111∘55998400

111∘50998400

111∘50998400

111∘55998400

28∘45998400

28∘50998400

28∘45998400

28∘50998400

Bahıa de Kino

Figure 1 Bahıa Kino area including Laguna La Cruz and Isla de Alcatraz showing seawater inlet to shrimp farms and discharge channel tothe bay

Transform log(119883 + 1)NormaliseResemblance D1 euclidean distance

2D stress 01

IslandEffluent

LagoonBay

Figure 2 nMDS ordination of water quality parameters for thestudy areas Temperature salinity dissolved oxygen suspendedsolids particulate organicmatter chlorophyll aVibrio-like bacteriaand viable heterotrophic bacteria were included in the multivariateanalysis

The average water temperature during all the time of thestudy on the island was 273 plusmn 33∘C effluent of 248 plusmn 53∘Cat the bay of 255 plusmn 46∘C and the lagoon of 266 plusmn 44∘Cwithout showing any statistical differences among areas (119867 =527 119875 = 015) (Table 1) However a seasonal behavior was

Table 1 Average values (plusmnSD) of physicochemical parameters fordifferent parts of the study area during discharge of effluent

Areas Temperature(∘C) Salinity Dissolved oxygen

(mg Lminus1) pH

Island 273 plusmn 33a 367 plusmn 04a 66 plusmn 12b 83 plusmn 01a

Effluent 248 plusmn 53a 393 plusmn 13b 45 plusmn 14a 82 plusmn 02a

Bay 255 plusmn 46a 372 plusmn 06a 57 plusmn 09b 82 plusmn 02a

Lagoon 266 plusmn 44a 372 plusmn 04a 60 plusmn 06b 82 plusmn 01a

Different letters among areas for each parameter indicate significant differ-ences (119875 lt 005 119899 = 96)

observed when high temperatures were recorded in June andSeptember and the lowest in October

Salinity values were found significantly higher (119865 = 745119875 lt 0001) in the effluent (393 plusmn 13) over the island (367 plusmn04) bay (372 plusmn 06) and lagoon (372 plusmn 04) (Table 1) Itwas noted that the bay lagoon and the control area (island)remained similar in salinities among them

In the effluent significantly lower values of DO (45 plusmn13mgLminus1) (119865 = 202 119875 lt 0001) were found in comparisonto the rest of the other study areas (Table 1) No significantdifferences were found (119875 gt 005) of DO among theisland bay and lagoon areas The pH did not show statisticaldifferences among the areas studied (119867 = 441 119875 = 022)(Table 1)

Water transparency had average values on the islandeffluent bay and lagoon of 25 plusmn 08 02 plusmn 01 09 plusmn 04

4 The Scientific World Journal

Tran

spar

ency

(m)

Island Effluent Bay Lagoon

4

3

2

1

0

a

bb

c

(a)

TSS

(mg Lminus1)

Island Effluent Bay Lagoon

400

300

200

100

0a

b b

c

(b)

Island Effluent Bay Lagoon

400

300

200

100

0

a

b b

c

ISS

(mg Lminus1)

(c)

Figure 3 Average values (plusmnSD) of selected variables (a) Water transparency (b) total suspended solids and (c) inorganic suspended solidsDifferent letters among zones for each variable indicate significant differences (119875 lt 005)

and 09 plusmn 04m respectively (Figure 3) Significantly lowervalues were recorded in the effluent and higher on the island(119865 = 3405 119875 lt 0001) Water transparency both in the bayand lagoon had intermediate values not statistically differentbut significantly lower than the island (Figure 3)

The average concentration of total suspended solids(TSS) was found to be 267 plusmn 12mgLminus1 in waters near theisland (control area) 2332 plusmn 957mgLminus1 in the effluent area562 plusmn 451mgLminus1 in the bay and 527 plusmn 306mgLminus1 in thelagoon The inorganic suspended solids (ISSs) showed thesame pattern as TSS Both TSS and ISS presented averagessignificantly (TSS 119867 = 3315 and 119875 lt 0001 ISS 119867 =3314 and 119875 = 0001) lower in the island and higher in theeffluent with intermediate values in both bay and lagoon butsignificantly higher than near the island (Figure 3)

Particulate organicmatter (POM) had average concentra-tions near the island of 462plusmn051mgLminus1 261plusmn92mgLminus1 ineffluent zone 71plusmn 42mgLminus1 in the bay and 70 plusmn 27mgLminus1in the lagoon Significantly higher values (119867 = 3107 119875 lt0001) of POM were observed in the effluent zone and lowerones near the island while POM values in both bay andlagoon remained similar it was observed that the lagoonpresented higher levels than the island (Figure 4)

Chlorophyll a concentration in the control area (island)had average values of 23 plusmn 07mgmminus3 a value which issignificantly (119867 = 3872 119875 lt 0001) lower when itis compared with the other areas (Figure 4) By contrastsignificantly higher values (119875 lt 0001) were found inthe effluent zone during the complete culture period with

219plusmn67mgmminus3 Chl a of bay (48plusmn14mgmminus3) and lagoon(75 plusmn 37mgmminus3) was maintaining similar values

The average concentration of viable heterotrophic bacte-ria (VHB) in the control area (island) was of 564 times 102 plusmn035times10

1 CFU mLminus1 while effluent was of 907times103plusmn024times10

1 CFU mLminus1 bay 176 times 103 plusmn 020 times 101 CFUmLminus1 andlagoon 311times103plusmn018times101 CFUmLminus1 Significantly higherconcentrations (119867 = 4576 119875 lt 0001) were quantifiedin the effluent zone and lower ones near the island Therewas no difference in VHB between island and bay whereasconcentrations in the lagoon were higher than both islandand bayTheVibrio-like bacteria (VLB) presented the same asthan the viable heterotrophic bacteria (119867 = 506 119875 lt 0001)(Figure 5)

4 Discussion

The multivariate analysis (nMDS) showed that water con-ditions varied considerably among the four areas especiallybetween the sites in the effluent channel and the other areasThe effluent had no effect on water quality in the controlarea The bay and lagoon are similar because there is a largeexchange of materials between the two areas mainly fromtidal exchange Our results suggested that pollutants from theshrimp farm influence environmental conditions in the bayand lagoon

41 Water Quality of Shrimp Farmrsquos Effluents Low dissolvedoxygen (DO) in the effluent results from a heavy load of

The Scientific World Journal 5

Island Effluent Bay Lagoon

40

30

20

10

0

abab

cPO

M (m

g Lminus1)

(a)

Island Effluent Bay Lagoon

40

30

20

10

0

a

bb

c

Chla

(mg mminus3)

(b)

Figure 4 Average values (plusmnSD) of selected variables (a) Particulate organic matter and (b) chlorophyll a Different letters among zones foreach variable indicate significant differences (119875 lt 005)

1

15

2

25

3

35

4

45

Island Effluent Bay Lagoon

a

c

a

c

ab

VLB VHB

a

b

Island Effluent Bay Lagoon

Log

CFU

mLminus1

Figure 5 Average concentration (plusmnSD) of Vibrio-like bacteria (VLB) and viable heterotrophic bacteria (VHB) in the different areas of studyDifferent letters among zones for each group of bacteria indicate significant differences (119875 lt 005)

organic matter generated in the shrimp farms [8 9 31 32]which includes unconsumed shrimp food detritus phyto-plankton zooplankton and bacteria The level of oxygen atthe discharge outlet at the bay was 45 plusmn 14mgLminus1 withinthe range of water quality standards for shrimp farm effluentsrecommended by the Global Aquaculture Alliance [33]

Effluent was highly saline because of the high evaporationrates in the shrimp ponds in this subtropical desert regionwhich is consistent with [34] who report salinity 40ndash42in effluents in this region The suspended solids (TSS andISS) increased during the course of effluent water flowbecause the bottom sediments were resuspended and thechannel walls were eroded The effluent was less transparentcaused by the concentrations of suspended solids POM andphytoplankton biomass

Water quality standards for shrimp farm effluents recom-mended by the Global Aquaculture Alliance for TSS has astandard of lt100mg Lminus1 and a target standard of lt50mg Lminus1[33] Effluents discharging into Bahıa de Kino had TSSconcentrations of 2332 plusmn 957mgLminus1

High phytoplankton biomass and organic matter ob-served in the wastewater is promoted by inorganic fertilizersin the cultivation system With current management prac-tices the ponds are rich in phytoplankton and organicmatterand this water is later discharged [11 13 15 35]

Microorganisms in general and bacteria in particular arekey elements in the marine ecosystems operation and reactquickly to changes in environmental parameters [36 37]Thequantity of bacteria is an important variable in monitoringof shrimp farm effluent Vibrio bacteria are opportunisticpathogens in shrimp farms at the larval and grow-out stagesit is the most serious pathogen causing up to 100 mortality[38ndash40]

In summary our results showed that shrimp farm efflu-ents reaching the bay have higher concentrations of TSSPOM phytoplankton biomass and bacteria than the baythis is consistent with observations in other studies [10ndash13 15] The control site at the island had low concentrationsof TSS POM phytoplankton biomass and bacteria thus theeffluent loadings are still a good indicator of likely impact

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 3: Research Article Effluents of Shrimp Farms and Its ...

The Scientific World Journal 3

North

USA

SonoraN

Gulf of CaliforniaPacificOcean

Water inlet

Dischargeoutlet

Shrimpfarms

LagunaLa Cruz

(km)0 1 2 5

111∘55998400

111∘50998400

111∘50998400

111∘55998400

28∘45998400

28∘50998400

28∘45998400

28∘50998400

Bahıa de Kino

Figure 1 Bahıa Kino area including Laguna La Cruz and Isla de Alcatraz showing seawater inlet to shrimp farms and discharge channel tothe bay

Transform log(119883 + 1)NormaliseResemblance D1 euclidean distance

2D stress 01

IslandEffluent

LagoonBay

Figure 2 nMDS ordination of water quality parameters for thestudy areas Temperature salinity dissolved oxygen suspendedsolids particulate organicmatter chlorophyll aVibrio-like bacteriaand viable heterotrophic bacteria were included in the multivariateanalysis

The average water temperature during all the time of thestudy on the island was 273 plusmn 33∘C effluent of 248 plusmn 53∘Cat the bay of 255 plusmn 46∘C and the lagoon of 266 plusmn 44∘Cwithout showing any statistical differences among areas (119867 =527 119875 = 015) (Table 1) However a seasonal behavior was

Table 1 Average values (plusmnSD) of physicochemical parameters fordifferent parts of the study area during discharge of effluent

Areas Temperature(∘C) Salinity Dissolved oxygen

(mg Lminus1) pH

Island 273 plusmn 33a 367 plusmn 04a 66 plusmn 12b 83 plusmn 01a

Effluent 248 plusmn 53a 393 plusmn 13b 45 plusmn 14a 82 plusmn 02a

Bay 255 plusmn 46a 372 plusmn 06a 57 plusmn 09b 82 plusmn 02a

Lagoon 266 plusmn 44a 372 plusmn 04a 60 plusmn 06b 82 plusmn 01a

Different letters among areas for each parameter indicate significant differ-ences (119875 lt 005 119899 = 96)

observed when high temperatures were recorded in June andSeptember and the lowest in October

Salinity values were found significantly higher (119865 = 745119875 lt 0001) in the effluent (393 plusmn 13) over the island (367 plusmn04) bay (372 plusmn 06) and lagoon (372 plusmn 04) (Table 1) Itwas noted that the bay lagoon and the control area (island)remained similar in salinities among them

In the effluent significantly lower values of DO (45 plusmn13mgLminus1) (119865 = 202 119875 lt 0001) were found in comparisonto the rest of the other study areas (Table 1) No significantdifferences were found (119875 gt 005) of DO among theisland bay and lagoon areas The pH did not show statisticaldifferences among the areas studied (119867 = 441 119875 = 022)(Table 1)

Water transparency had average values on the islandeffluent bay and lagoon of 25 plusmn 08 02 plusmn 01 09 plusmn 04

4 The Scientific World Journal

Tran

spar

ency

(m)

Island Effluent Bay Lagoon

4

3

2

1

0

a

bb

c

(a)

TSS

(mg Lminus1)

Island Effluent Bay Lagoon

400

300

200

100

0a

b b

c

(b)

Island Effluent Bay Lagoon

400

300

200

100

0

a

b b

c

ISS

(mg Lminus1)

(c)

Figure 3 Average values (plusmnSD) of selected variables (a) Water transparency (b) total suspended solids and (c) inorganic suspended solidsDifferent letters among zones for each variable indicate significant differences (119875 lt 005)

and 09 plusmn 04m respectively (Figure 3) Significantly lowervalues were recorded in the effluent and higher on the island(119865 = 3405 119875 lt 0001) Water transparency both in the bayand lagoon had intermediate values not statistically differentbut significantly lower than the island (Figure 3)

The average concentration of total suspended solids(TSS) was found to be 267 plusmn 12mgLminus1 in waters near theisland (control area) 2332 plusmn 957mgLminus1 in the effluent area562 plusmn 451mgLminus1 in the bay and 527 plusmn 306mgLminus1 in thelagoon The inorganic suspended solids (ISSs) showed thesame pattern as TSS Both TSS and ISS presented averagessignificantly (TSS 119867 = 3315 and 119875 lt 0001 ISS 119867 =3314 and 119875 = 0001) lower in the island and higher in theeffluent with intermediate values in both bay and lagoon butsignificantly higher than near the island (Figure 3)

Particulate organicmatter (POM) had average concentra-tions near the island of 462plusmn051mgLminus1 261plusmn92mgLminus1 ineffluent zone 71plusmn 42mgLminus1 in the bay and 70 plusmn 27mgLminus1in the lagoon Significantly higher values (119867 = 3107 119875 lt0001) of POM were observed in the effluent zone and lowerones near the island while POM values in both bay andlagoon remained similar it was observed that the lagoonpresented higher levels than the island (Figure 4)

Chlorophyll a concentration in the control area (island)had average values of 23 plusmn 07mgmminus3 a value which issignificantly (119867 = 3872 119875 lt 0001) lower when itis compared with the other areas (Figure 4) By contrastsignificantly higher values (119875 lt 0001) were found inthe effluent zone during the complete culture period with

219plusmn67mgmminus3 Chl a of bay (48plusmn14mgmminus3) and lagoon(75 plusmn 37mgmminus3) was maintaining similar values

The average concentration of viable heterotrophic bacte-ria (VHB) in the control area (island) was of 564 times 102 plusmn035times10

1 CFU mLminus1 while effluent was of 907times103plusmn024times10

1 CFU mLminus1 bay 176 times 103 plusmn 020 times 101 CFUmLminus1 andlagoon 311times103plusmn018times101 CFUmLminus1 Significantly higherconcentrations (119867 = 4576 119875 lt 0001) were quantifiedin the effluent zone and lower ones near the island Therewas no difference in VHB between island and bay whereasconcentrations in the lagoon were higher than both islandand bayTheVibrio-like bacteria (VLB) presented the same asthan the viable heterotrophic bacteria (119867 = 506 119875 lt 0001)(Figure 5)

4 Discussion

The multivariate analysis (nMDS) showed that water con-ditions varied considerably among the four areas especiallybetween the sites in the effluent channel and the other areasThe effluent had no effect on water quality in the controlarea The bay and lagoon are similar because there is a largeexchange of materials between the two areas mainly fromtidal exchange Our results suggested that pollutants from theshrimp farm influence environmental conditions in the bayand lagoon

41 Water Quality of Shrimp Farmrsquos Effluents Low dissolvedoxygen (DO) in the effluent results from a heavy load of

The Scientific World Journal 5

Island Effluent Bay Lagoon

40

30

20

10

0

abab

cPO

M (m

g Lminus1)

(a)

Island Effluent Bay Lagoon

40

30

20

10

0

a

bb

c

Chla

(mg mminus3)

(b)

Figure 4 Average values (plusmnSD) of selected variables (a) Particulate organic matter and (b) chlorophyll a Different letters among zones foreach variable indicate significant differences (119875 lt 005)

1

15

2

25

3

35

4

45

Island Effluent Bay Lagoon

a

c

a

c

ab

VLB VHB

a

b

Island Effluent Bay Lagoon

Log

CFU

mLminus1

Figure 5 Average concentration (plusmnSD) of Vibrio-like bacteria (VLB) and viable heterotrophic bacteria (VHB) in the different areas of studyDifferent letters among zones for each group of bacteria indicate significant differences (119875 lt 005)

organic matter generated in the shrimp farms [8 9 31 32]which includes unconsumed shrimp food detritus phyto-plankton zooplankton and bacteria The level of oxygen atthe discharge outlet at the bay was 45 plusmn 14mgLminus1 withinthe range of water quality standards for shrimp farm effluentsrecommended by the Global Aquaculture Alliance [33]

Effluent was highly saline because of the high evaporationrates in the shrimp ponds in this subtropical desert regionwhich is consistent with [34] who report salinity 40ndash42in effluents in this region The suspended solids (TSS andISS) increased during the course of effluent water flowbecause the bottom sediments were resuspended and thechannel walls were eroded The effluent was less transparentcaused by the concentrations of suspended solids POM andphytoplankton biomass

Water quality standards for shrimp farm effluents recom-mended by the Global Aquaculture Alliance for TSS has astandard of lt100mg Lminus1 and a target standard of lt50mg Lminus1[33] Effluents discharging into Bahıa de Kino had TSSconcentrations of 2332 plusmn 957mgLminus1

High phytoplankton biomass and organic matter ob-served in the wastewater is promoted by inorganic fertilizersin the cultivation system With current management prac-tices the ponds are rich in phytoplankton and organicmatterand this water is later discharged [11 13 15 35]

Microorganisms in general and bacteria in particular arekey elements in the marine ecosystems operation and reactquickly to changes in environmental parameters [36 37]Thequantity of bacteria is an important variable in monitoringof shrimp farm effluent Vibrio bacteria are opportunisticpathogens in shrimp farms at the larval and grow-out stagesit is the most serious pathogen causing up to 100 mortality[38ndash40]

In summary our results showed that shrimp farm efflu-ents reaching the bay have higher concentrations of TSSPOM phytoplankton biomass and bacteria than the baythis is consistent with observations in other studies [10ndash13 15] The control site at the island had low concentrationsof TSS POM phytoplankton biomass and bacteria thus theeffluent loadings are still a good indicator of likely impact

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 4: Research Article Effluents of Shrimp Farms and Its ...

4 The Scientific World Journal

Tran

spar

ency

(m)

Island Effluent Bay Lagoon

4

3

2

1

0

a

bb

c

(a)

TSS

(mg Lminus1)

Island Effluent Bay Lagoon

400

300

200

100

0a

b b

c

(b)

Island Effluent Bay Lagoon

400

300

200

100

0

a

b b

c

ISS

(mg Lminus1)

(c)

Figure 3 Average values (plusmnSD) of selected variables (a) Water transparency (b) total suspended solids and (c) inorganic suspended solidsDifferent letters among zones for each variable indicate significant differences (119875 lt 005)

and 09 plusmn 04m respectively (Figure 3) Significantly lowervalues were recorded in the effluent and higher on the island(119865 = 3405 119875 lt 0001) Water transparency both in the bayand lagoon had intermediate values not statistically differentbut significantly lower than the island (Figure 3)

The average concentration of total suspended solids(TSS) was found to be 267 plusmn 12mgLminus1 in waters near theisland (control area) 2332 plusmn 957mgLminus1 in the effluent area562 plusmn 451mgLminus1 in the bay and 527 plusmn 306mgLminus1 in thelagoon The inorganic suspended solids (ISSs) showed thesame pattern as TSS Both TSS and ISS presented averagessignificantly (TSS 119867 = 3315 and 119875 lt 0001 ISS 119867 =3314 and 119875 = 0001) lower in the island and higher in theeffluent with intermediate values in both bay and lagoon butsignificantly higher than near the island (Figure 3)

Particulate organicmatter (POM) had average concentra-tions near the island of 462plusmn051mgLminus1 261plusmn92mgLminus1 ineffluent zone 71plusmn 42mgLminus1 in the bay and 70 plusmn 27mgLminus1in the lagoon Significantly higher values (119867 = 3107 119875 lt0001) of POM were observed in the effluent zone and lowerones near the island while POM values in both bay andlagoon remained similar it was observed that the lagoonpresented higher levels than the island (Figure 4)

Chlorophyll a concentration in the control area (island)had average values of 23 plusmn 07mgmminus3 a value which issignificantly (119867 = 3872 119875 lt 0001) lower when itis compared with the other areas (Figure 4) By contrastsignificantly higher values (119875 lt 0001) were found inthe effluent zone during the complete culture period with

219plusmn67mgmminus3 Chl a of bay (48plusmn14mgmminus3) and lagoon(75 plusmn 37mgmminus3) was maintaining similar values

The average concentration of viable heterotrophic bacte-ria (VHB) in the control area (island) was of 564 times 102 plusmn035times10

1 CFU mLminus1 while effluent was of 907times103plusmn024times10

1 CFU mLminus1 bay 176 times 103 plusmn 020 times 101 CFUmLminus1 andlagoon 311times103plusmn018times101 CFUmLminus1 Significantly higherconcentrations (119867 = 4576 119875 lt 0001) were quantifiedin the effluent zone and lower ones near the island Therewas no difference in VHB between island and bay whereasconcentrations in the lagoon were higher than both islandand bayTheVibrio-like bacteria (VLB) presented the same asthan the viable heterotrophic bacteria (119867 = 506 119875 lt 0001)(Figure 5)

4 Discussion

The multivariate analysis (nMDS) showed that water con-ditions varied considerably among the four areas especiallybetween the sites in the effluent channel and the other areasThe effluent had no effect on water quality in the controlarea The bay and lagoon are similar because there is a largeexchange of materials between the two areas mainly fromtidal exchange Our results suggested that pollutants from theshrimp farm influence environmental conditions in the bayand lagoon

41 Water Quality of Shrimp Farmrsquos Effluents Low dissolvedoxygen (DO) in the effluent results from a heavy load of

The Scientific World Journal 5

Island Effluent Bay Lagoon

40

30

20

10

0

abab

cPO

M (m

g Lminus1)

(a)

Island Effluent Bay Lagoon

40

30

20

10

0

a

bb

c

Chla

(mg mminus3)

(b)

Figure 4 Average values (plusmnSD) of selected variables (a) Particulate organic matter and (b) chlorophyll a Different letters among zones foreach variable indicate significant differences (119875 lt 005)

1

15

2

25

3

35

4

45

Island Effluent Bay Lagoon

a

c

a

c

ab

VLB VHB

a

b

Island Effluent Bay Lagoon

Log

CFU

mLminus1

Figure 5 Average concentration (plusmnSD) of Vibrio-like bacteria (VLB) and viable heterotrophic bacteria (VHB) in the different areas of studyDifferent letters among zones for each group of bacteria indicate significant differences (119875 lt 005)

organic matter generated in the shrimp farms [8 9 31 32]which includes unconsumed shrimp food detritus phyto-plankton zooplankton and bacteria The level of oxygen atthe discharge outlet at the bay was 45 plusmn 14mgLminus1 withinthe range of water quality standards for shrimp farm effluentsrecommended by the Global Aquaculture Alliance [33]

Effluent was highly saline because of the high evaporationrates in the shrimp ponds in this subtropical desert regionwhich is consistent with [34] who report salinity 40ndash42in effluents in this region The suspended solids (TSS andISS) increased during the course of effluent water flowbecause the bottom sediments were resuspended and thechannel walls were eroded The effluent was less transparentcaused by the concentrations of suspended solids POM andphytoplankton biomass

Water quality standards for shrimp farm effluents recom-mended by the Global Aquaculture Alliance for TSS has astandard of lt100mg Lminus1 and a target standard of lt50mg Lminus1[33] Effluents discharging into Bahıa de Kino had TSSconcentrations of 2332 plusmn 957mgLminus1

High phytoplankton biomass and organic matter ob-served in the wastewater is promoted by inorganic fertilizersin the cultivation system With current management prac-tices the ponds are rich in phytoplankton and organicmatterand this water is later discharged [11 13 15 35]

Microorganisms in general and bacteria in particular arekey elements in the marine ecosystems operation and reactquickly to changes in environmental parameters [36 37]Thequantity of bacteria is an important variable in monitoringof shrimp farm effluent Vibrio bacteria are opportunisticpathogens in shrimp farms at the larval and grow-out stagesit is the most serious pathogen causing up to 100 mortality[38ndash40]

In summary our results showed that shrimp farm efflu-ents reaching the bay have higher concentrations of TSSPOM phytoplankton biomass and bacteria than the baythis is consistent with observations in other studies [10ndash13 15] The control site at the island had low concentrationsof TSS POM phytoplankton biomass and bacteria thus theeffluent loadings are still a good indicator of likely impact

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 5: Research Article Effluents of Shrimp Farms and Its ...

The Scientific World Journal 5

Island Effluent Bay Lagoon

40

30

20

10

0

abab

cPO

M (m

g Lminus1)

(a)

Island Effluent Bay Lagoon

40

30

20

10

0

a

bb

c

Chla

(mg mminus3)

(b)

Figure 4 Average values (plusmnSD) of selected variables (a) Particulate organic matter and (b) chlorophyll a Different letters among zones foreach variable indicate significant differences (119875 lt 005)

1

15

2

25

3

35

4

45

Island Effluent Bay Lagoon

a

c

a

c

ab

VLB VHB

a

b

Island Effluent Bay Lagoon

Log

CFU

mLminus1

Figure 5 Average concentration (plusmnSD) of Vibrio-like bacteria (VLB) and viable heterotrophic bacteria (VHB) in the different areas of studyDifferent letters among zones for each group of bacteria indicate significant differences (119875 lt 005)

organic matter generated in the shrimp farms [8 9 31 32]which includes unconsumed shrimp food detritus phyto-plankton zooplankton and bacteria The level of oxygen atthe discharge outlet at the bay was 45 plusmn 14mgLminus1 withinthe range of water quality standards for shrimp farm effluentsrecommended by the Global Aquaculture Alliance [33]

Effluent was highly saline because of the high evaporationrates in the shrimp ponds in this subtropical desert regionwhich is consistent with [34] who report salinity 40ndash42in effluents in this region The suspended solids (TSS andISS) increased during the course of effluent water flowbecause the bottom sediments were resuspended and thechannel walls were eroded The effluent was less transparentcaused by the concentrations of suspended solids POM andphytoplankton biomass

Water quality standards for shrimp farm effluents recom-mended by the Global Aquaculture Alliance for TSS has astandard of lt100mg Lminus1 and a target standard of lt50mg Lminus1[33] Effluents discharging into Bahıa de Kino had TSSconcentrations of 2332 plusmn 957mgLminus1

High phytoplankton biomass and organic matter ob-served in the wastewater is promoted by inorganic fertilizersin the cultivation system With current management prac-tices the ponds are rich in phytoplankton and organicmatterand this water is later discharged [11 13 15 35]

Microorganisms in general and bacteria in particular arekey elements in the marine ecosystems operation and reactquickly to changes in environmental parameters [36 37]Thequantity of bacteria is an important variable in monitoringof shrimp farm effluent Vibrio bacteria are opportunisticpathogens in shrimp farms at the larval and grow-out stagesit is the most serious pathogen causing up to 100 mortality[38ndash40]

In summary our results showed that shrimp farm efflu-ents reaching the bay have higher concentrations of TSSPOM phytoplankton biomass and bacteria than the baythis is consistent with observations in other studies [10ndash13 15] The control site at the island had low concentrationsof TSS POM phytoplankton biomass and bacteria thus theeffluent loadings are still a good indicator of likely impact

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 6: Research Article Effluents of Shrimp Farms and Its ...

6 The Scientific World Journal

The knowledge of those loads is useful for understanding theresponses fromwater bodies receiving shrimp farm effluents

42 Influences on Coastal Ecosystems Sustainability ofshrimp culture requires maintenance of good water qualityin the adjacent coastal region Our results showed that thesuspended solids POM Chl a VHB and VLB in the bayand lagoon were two- to three-fold higher than the controlsite Environmental problems from shrimp farm effluents areassociated with water pollution and diseases

An excess of organic matter discharged into the bayand lagoon induces a higher demand of dissolved oxygenwhich negatively affects ecosystems by hypoxia Variationsin effluents with low concentrations of dissolved oxygen inthe bay and lagoon could be explained by winds pattern[41] tidal mixing coastal circulation along the coast of theGulf of California [42] and water exchange time for thelagoon (21 days) [43] These results suggest that the systemwas assimilating the organic matter discharged However themarginal rate of assimilation by the system does not indicatean absence of ecological impact High impact may occurduring the night in the area surrounding the discharge inthe bay creating hypoxic events mainly during the summerwhen winds are less intense water temperature is higherand dissolved oxygen is on average lower This representsa potential negative effect on biogeochemical processes andaquatic life

One of the key environmental concerns about shrimpfarming is the discharge of waters with high levels of nutri-ents into adjacent body waters Pond water is continuouslyexchanged (5ndash30dminus1) with drainage through a ditch thatbrings back diluted waste water to the bay and inlet channelWith 1350 ha of shrimp ponds in operation yielding about25 t haminus1 and disposing of 72 kgN and 13 kg P waste foreach ton of harvested shrimp [44] we estimate a load ofsim243 tN yrminus1 and sim44 t P yrminus1 This contributes to signifi-cantly high levels of Chl a in the bay compared to thecontrol siteNutrient loads have been linked to lower diversityof phytoplankton species and nuisance algae blooms withimpacts the ecological health of coastal ecosystems [45]In a nearby area in April 2003 a harmful algal bloom ofChattonella marina C cf ovata Gymnodinium catenatumand G sanguineum caused a massive die-off of fish andmollusks [46] hence there is a risk potential of harmful algalblooms

Most shrimp diseases are bacterial and viral Most bacte-rial diseases are caused by Vibrio spp Vibriosis outbreaks isa serious problem in intensive shrimp ponds in this region[47] These pathogenic bacteria can affect other cultivatedmarine populations such as oysters in this region as wellas species native to the area When the aquatic environmentis enriched by accumulating organic matter several speciesof Vibrio spp grow rapidly not because it has a high growthrate but because it is adapted to oxygen-deficient conditions[48] Vibrio spp affects fish crustaceans and cultivatedshellfish The important decade-old oyster farming activity(Crassostrea gigas and C corteziensis) surrounding the bayand lagoon [49 50] could be impacted by the shrimp farm

effluentThese results indicate the need for increased researchto determine the consequences of bacterial loads and wastenutrients into the coastal ecosystems

5 Conclusions

Shrimp farm effluent provides significantly high salinity sus-pended solids organic particulate matter chlorophyll a andbacteria to coastal ecosystems as well as reduced dissolvedoxygen and transparency Effluent produced changes in waterquality in the bay and lagoon Accumulation of solidsorganic matter and bacterial biomass affects environmentalconditions and processes of these ecosystems There is stillinsufficient knowledge of how effluents are affecting coastalecosystems and how it affects aquaculture activities Currentwater quality of Bahıa de Kino appears to result from inade-quate management of shrimp ponds Our results suggest thatboth inMexico andworldwide efforts at waste prevention andminimization at the source and onsite treatment and reuse ofeffluent would reduce losses of coastal ecosystem services

Conflict of Interests

The authors declare they have not conflict of interests

Acknowledgments

Leopoldo Encinas Bracamontes Ulises Becerra LamadridFulgencio Garcıa Ochoa and Oscar Acosta Gonzalez ofthe UEK of DICTUS provided technical support duringsampling Marıa del Refugio Lopez Tapia provided wateranalysis and David Urıas Laborın of CIBNOR Guaymasprepared the map Instituto Tecnologico de Sonora Univer-sidad de Sonora Consejo Nacional de Ciencia y Tecnologıa(CONACYT) and Comite de Sanidad Acuıcola del Estadode Sonora provided funding of this project Miguel Cordoba-Matson provided initial English review Ira Fogel providedcomprehensive editorial services The first author would alsolike to thank CONACYT for the grant that has allowed himto pursue his doctoral studies

References

[1] FAO The State of World Fisheries and Aquaculture Food andAgriculture Organization Rome Italy 2012

[2] G Sara ldquoEcological effects of aquaculture on living and non-living suspended fractions of the water column a meta-analysisrdquoWater Research vol 41 no 15 pp 3187ndash3200 2007

[3] C E Boyd ldquoGuidelines for aquaculture effluent management atthe farm-levelrdquo Aquaculture vol 226 no 1ndash4 pp 101ndash112 2003

[4] P T Anh C Kroeze S R Bush and A P J Mol ldquoWaterpollution by intensive brackish shrimp farming in south-eastVietnam causes and options for controlrdquo Agricultural WaterManagement vol 97 no 6 pp 872ndash882 2010

[5] T D Bui J Luong-Van and C M Austin ldquoImpact of shrimpfarm effluent on water quality in coastal areas of the worldheritage-listed Ha Long Bayrdquo American Journal of Environmen-tal Sciences vol 8 no 2 pp 104ndash116 2012

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 7: Research Article Effluents of Shrimp Farms and Its ...

The Scientific World Journal 7

[6] R L Naylor R J Goldburg J H Primavera et al ldquoEffect ofaquaculture on world fish suppliesrdquo Nature vol 405 no 6790pp 1017ndash1024 2000

[7] L Deutsch S Graslund C Folke et al ldquoFeeding aquaculturegrowth through globalization exploitation of marine ecosys-tems for fishmealrdquo Global Environmental Change vol 17 no 2pp 238ndash249 2007

[8] J S Hopkins R D Hamilton II P A Sandifer C L Browdyand A D Stokes ldquoEffect of water exchange rate on productionwater quality effluent characteristics and nitrogen budgets ofintensive shrimp pondsrdquo Journal of the World AquacultureSociety vol 24 no 3 pp 304ndash320 1993

[9] C E Boyd ldquoFarm effluent during draining for harvestrdquo GlobalAquaculture vol 3 pp 26ndash27 2000

[10] A D McKinnon L A Trott D M Alongi and A DavidsonldquoWater column production and nutrient characteristics inmangrove creeks receiving shrimp farm effluentrdquo AquacultureResearch vol 33 no 1 pp 55ndash73 2002

[11] X Biao D Zhuhong andW Xiaorong ldquoImpact of the intensiveshrimp farming on the water quality of the adjacent coastalcreeks from Eastern Chinardquo Marine Pollution Bulletin vol 48no 5-6 pp 543ndash553 2004

[12] L D de Lacerda A G Vaisman L P Maia C A R Silvaand E M S Cunha ldquoRelative importance of nitrogen andphosphorus emissions from shrimp farming and other anthro-pogenic sources for six estuaries along the NE Brazilian coastrdquoAquaculture vol 253 no 1ndash4 pp 433ndash446 2006

[13] A P Cardozo V O Britto and C Odebrecht ldquoTemporalvariability of plankton and nutrients in shrimp culture pondsvs adjacent estuarine waterrdquo Pan-American Journal of AquaticSciences vol 6 no 1 pp 28ndash43 2011

[14] L A Trott and D M Alongi ldquoVariability in surface waterchemistry and phytoplankton biomass in two tropical tidallydominated mangrove creeksrdquoMarine and Freshwater Researchvol 50 no 5 pp 451ndash457 1999

[15] L A Trott and D M Alongi ldquoThe impact of shrimp pondeffluent on water quality and phytoplankton biomass in atropical mangrove estuaryrdquo Marine Pollution Bulletin vol 40no 11 pp 947ndash951 2000

[16] F PAez-Osuna ldquoThe environmental impact of shrimp aquacul-ture causes effects andmitigating alternativesrdquo EnvironmentalManagement vol 28 no 1 pp 131ndash140 2001

[17] GESAMP ldquoThe ecological effects of coastal aquaculturewastesrdquo Report Studies GESAMP 57 IMOFAOUNESCO-IOCWMOWHOIAEAUN-UNEP Joint Group of Expertson the Scientific Aspects of Marine Environmental ProtectionRome Italy 1996

[18] J Fuchs J L M Martin and N T An ldquoImpact of tropicalshrimp aquaculture on the environment inAsia and the PacificrdquoEuropean Commission Fisheries Cooperative Bulletin vol 12 no4 pp 9ndash13 1999

[19] N C Ferreira C Bonetti andW Q Seiffert ldquoHydrological andWater Quality Indices as management tools in marine shrimpculturerdquo Aquaculture vol 318 no 3-4 pp 425ndash433 2011

[20] F Paez-Osuna A Gracia F Flores-Verdugo et al ldquoShrimpaquaculture development and the environment in the Gulf ofCalifornia ecoregionrdquo Marine Pollution Bulletin vol 46 no 7pp 806ndash815 2003

[21] CONAPESCA Estadıstico de Pesca y Acuacultura ComisionNacional de Acuacultura y Pesca Mazatlan Sinaloa Mexico2011

[22] JM Grijalva-Chon and RH Barraza-Guardado ldquoDistributionand abundance of postlarvae and juveniles of shrimps of thegenus Penaeus in Kino Bay and La Cruz Lagoon SonoraMexicordquo Ciencias Marinas vol 18 no 3 pp 153ndash169 1992

[23] E Garcıa Modificaciones al Sistema de Clasificacion Climaticade Koppen (Para Adaptarlo a las Condiciones Climaticas deMexico Instituto de Geografıa UNAM Mexico 5th edition2004

[24] J D H Strickland and T R Parsons Practical Handbook ofSeawater Analysis Fisheries Research Board of Canada Bulletin2nd edition 1972

[25] T R Parsons Y Maita and C M Lalli Manual Chemical andBiological Methods For Seawater Analysis Pergamon Press NewYork NY USA 1984

[26] N Neufeld ldquoProcedures for the bacteriological examinationof seawater and shellfishrdquo in Laboratory Procedures For theExamination of Seawater and Shellfish A E Greenberg and DA Hunt Eds pp 37ndash63 American Public Health Association(APHA) Washington DC USA 1985

[27] L S Clesceri A E Greenberg and A D Eaton MethodsFor the Examination of Water and Wastewater AmericanPublic Health Association (APHA) American Water WorksAssociation (AWWA) and Water Environment Federation(WEF) Washington DC USA 1998

[28] W J Conover Nonparametric Statistics John Wiley amp SonsNew York NY USA 2nd edition 1980

[29] J H Zar Biostatistical Analysis Prentice Hall Englewood NJUSA 2nd edition 1984

[30] NCSS Cruncher Statistical System User Guide Statistical ampPower Analysis Software North Caroline NC USA 2007

[31] A Miranda-Baeza D Voltolina M A Brambila-Gamez MG Frıas-Espiricueta and J Simental ldquoEffluent characteristicsand nutrient loading of a semi-intensive shrimp farm in NWMexicordquo Life and Environment vol 57 no 1-2 pp 21ndash27 2007

[32] R Casillas-Hernandez H Nolasco-Soria T Garcıa-Galano OCarrillo-Farnes and F Paez-Osuna ldquoWater quality chemicalfluxes and production in semi-intensive Pacific white shrimp(Litopenaeus vannamei) culture ponds utilizing two differentfeeding strategiesrdquo Aquacultural Engineering vol 36 no 2 pp105ndash114 2007

[33] C E Boyd and D Gautier ldquoEffluent composition and waterquality standardsrdquo Global Aquaculture vol 3 no 5 pp 61ndash662000

[34] H A Gonzalez-Ocampo L F Beltran-Morales C Caceres-Martınez et al ldquoShrimp aquaculture environmental diagnosisin the semiarid coastal zone in Mexicordquo Fresenius Environmen-tal Bulletin vol 15 no 7 pp 1ndash11 2006

[35] A C Ruiz-Fernandez and F Paez-Osuna ldquoComparative surveyof the influent and effluent water quality of shrimp ponds onMexican farmsrdquoWater Environment Research vol 76 no 1 pp5ndash14 2004

[36] T E Ford ldquoResponse of marine microbial communities toanthropogenic stressrdquo Journal of Aquatic Ecosystem Stress andRecovery vol 7 no 1 pp 75ndash89 2000

[37] HW Paerl J Dyble L Twomey J L Pinckney J Nelson and LKerkhof ldquoCharacterizing man-made and natural modificationsof microbial diversity and activity in coastal ecosystemsrdquoInternational Journal of General and Molecular Microbiologyvol 81 no 1ndash4 pp 487ndash507 2002

[38] C Kwei-Lin ldquoPrawn cultured in Taiwan What went wrongrdquoWorld Aquaculture vol 20 pp 19ndash20 1989

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 8: Research Article Effluents of Shrimp Farms and Its ...

8 The Scientific World Journal

[39] N Bhaskar and T M R Setty ldquoIncidence of vibrios of pub-lic health significance in the farming phase of tiger shrimp(Penaeus monodon)rdquo Journal of the Science of Food and Agri-culture vol 66 no 2 pp 225ndash231 1994

[40] K-K Lee S-R Yu F-R Chen T-I Yang and P-C LiuldquoVirulence of Vibrio alginolyticus isolated from diseased tigerprawn Penaeus monodonrdquo Current Microbiology vol 32 no 4pp 229ndash231 1996

[41] A Pares-Sierra AMascarenhas S GMarinone and R CastroldquoTemporal and spatial variation of the surface winds in the Gulfof Californiardquo Geophysical Research Letters vol 30 no 6 pp1ndash4 2003

[42] M F Lavin and S G Marinone ldquoAn overview of the physicaloceanography of the Gulf of Californiardquo in Processes in Geo-physical Fluid Dynamics O U Velasco-Fuentes J Sheinbaumand J Ochoa Eds pp 173ndash204 Kluwer Academic PublishersDodrecht The Netherlands 2003

[43] M Botello-Ruvalcaba E Valdez-Holguın Estero La Cruz andSonora ldquoComparison of Carbon Nitrogen and Phosphorusfluxes in Mexican coastal lagoonsrdquo in LOICZ Reports amp StudiesNo 10 S V Smith S Ibarra-Obando P R Boudreau and VF Camacho-Ibar Eds pp 21ndash24 LOICZ Core Project OfficeNetherlands Institute for Sea Research (NIOZ) Texe TheNetherlands 1997

[44] R Casillas-Hernandez F Magallon-Barajas G Portillo-Clarckand F Paez-Osuna ldquoNutrient mass balances in semi-intensiveshrimp ponds from Sonora Mexico using two feeding strate-gies trays and mechanical dispersalrdquo Aquaculture vol 258 no1ndash4 pp 289ndash298 2006

[45] R Alonso-Rodrıguez and F Paez-Osuna ldquoNutrients phyto-plankton and harmful algal blooms in shrimp ponds a reviewwith special reference to the situation in the Gulf of CaliforniardquoAquaculture vol 219 no 1ndash4 pp 317ndash336 2003

[46] J Garcıa-Hernandez L Garcıa-Rico M E Jara-Marini RBarraza-Guardado andAHWeaver ldquoConcentrations of heavymetals in sediment and organisms during a harmful algal bloom(HAB) at Kun Kaak Bay Sonora Mexicordquo Marine PollutionBulletin vol 50 no 7 pp 733ndash739 2005

[47] P Menasveta ldquoImproved shrimp growout systems for diseaseprevention and environmental sustainability in Asiardquo Reviewsin Fisheries Science vol 10 no 3-4 pp 391ndash402 2002

[48] G Aguirre-Guzman Y Labreuche D Ansquer et al ldquoPro-teinaceous exotoxins of shrimp-pathogenic isolates of Vibriopenaeicida and Vibrio nigripulchritudordquo Ciencias Marinas vol29 no 1 pp 77ndash88 2003

[49] R H Barraza-Guardado J Chavez-Villalba H Atilano-Silvaand F Hoyos-Chairez ldquoSeasonal variation in the conditionindex of Pacific oyster postlarvae (Crassostrea gigas) in a land-based nursery in Sonora Mexicordquo Aquaculture Research vol40 no 1 pp 118ndash128 2008

[50] J Chavez-Villalba A Arreola-Lizarraga S Burrola-Sanchezand F Hoyos-Chairez ldquoGrowth condition and survival of thePacific oyster Crassostrea gigas cultivated within and outside asubtropical lagoonrdquo Aquaculture vol 300 no 1ndash4 pp 128ndash1362010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 9: Research Article Effluents of Shrimp Farms and Its ...

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of