chain of commercialization of spp. turtles (testudines ... · pdf filechain of...

Chain of commercialization of Podocnemis sppturtles (Testudines Podocnemididae) in the PurusRiver Amazon basin Brazil current status andperspectivesPantoja-Lima et al

JOURNAL OF ETHNOBIOLOGY AND ETHNOMEDICINE

Pantoja-Lima et al Journal of Ethnobiology and Ethnomedicine 2014 108httpwwwethnobiomedcomcontent1018



RESEARCH Open Access

Chain of commercialization of Podocnemis sppturtles (Testudines Podocnemididae) in the PurusRiver Amazon basin Brazil current status andperspectivesJackson Pantoja-Lima1 Paulo HR Aride1 Adriano T de Oliveira1 Daniely Feacutelix-Silva2 Juarez CB Pezzuti2

and George H Rebecirclo3

Abstract

Background Consumption of turtles by natives and settlers in the Amazon and Orinoco has been widely studiedin scientific communities Accepted cultural customs and the local dietary and monetary needs need to be takeninto account in conservation programs and when implementing federal laws related to consumption and fishingmethods This study was conducted around the Purus River a region known for the consumption and illegal tradeof turtles The objective of this study was to quantify the illegal turtle trade in Tapauaacute and to understand its effecton the local economy

Methods This study was conducted in the municipality of Tapauaacute in the state of Amazonas Brazil To estimateturtle consumption interviews were conducted over 2 consecutive years (2006 and 2007) in urban areas andisolated communities The experimental design was randomized with respect to type of household To study theturtle fishery and trade chain we used snowball sampling methodology

Results During our study period 100 of respondents reported consuming at least three species of turtles(Podocnemis spp) Our estimates indicate that about 34 tons of animals are consumed annually in Tapauaacute along themargins of a major fishing river in the Amazon At least five components related to the chain of commercializationof turtles on the Purus River are identified Indigenous Apurinatilde and (2) residents of bordering villages(communities) (3) of local smugglers buy and sell turtles to the community in exchange for manufactured goodsand (4) regional smugglers buy in Tapauaacute Laacutebrea and Beruri to sell in Manaus and Manacapuru Finally (5) thereare professional fishermen

Conclusions We quantify the full impact of turtle consumption and advocate the conservation of the regionrsquosturtle populations The Brazilian government should initiate a new turtle consumption management program whichinvolves the opinions of consumers With these measures the conservation of freshwater turtles in the BrazilianAmazon is possible

Keywords Chelonian Amazon Turtle consumption Illegal trade Endangered species

Correspondence jacksonpantojagmailcom1Instituto Federal de Educaccedilatildeo Ciecircncia e Tecnologia do Amazonas (IFAM)Campus Presidente Figueiredo Av Onccedila Pintada 1308 Galo da SerraPresidente Figueiredo AM CEP 69735-000 BrazilFull list of author information is available at the end of the article

copy 2014 Pantoja-Lima et al licensee BioMed Central Ltd This is an Open Access article distributed under the terms of theCreative Commons Attribution License (httpcreativecommonsorglicensesby20) which permits unrestricted usedistribution and reproduction in any medium provided the original work is properly cited The Creative Commons PublicDomain Dedication waiver (httpcreativecommonsorgpublicdomainzero10) applies to the data made available in thisarticle unless otherwise stated

Pantoja-Lima et al Journal of Ethnobiology and Ethnomedicine 2014 108 Page 2 of 10httpwwwethnobiomedcomcontent1018

BackgroundAccording to Alves et al [1] at least 81 of over 700 speciesof reptiles in Brazil are used by and are culturally signifi-cant to human populations in Brazil Of these 81 species30 are on the States Red List Brazilian Red List or Inter-national Union for Conservation of Nature (IUCN)rsquos RedList of Threatened Species Lizards snakes caimans tor-toises and marine and freshwater turtles are used for foodmedicine leather ornamental and magicreligious pur-poses and kept as pets [1]The consumption of turtles by natives and settlers in

the Amazon and Orinoco basins today [23] and alsohistorically during the pre-Columbian period [4] hasbeen investigated by many researchers from differentscientific communities Gilmore [4] addressed the SouthAmericansrsquo and settlersrsquo use of animal wildlife claimingthat the poaching of Amazon river turtles was by far themost important ethnozoological activity on that contin-ent The capture and sale of the Giant South AmericanTurtle (Podocnemis expansa) and the collection of itseggs is frequently described [15-7] Egg collection is be-lieved to have led to the extinction of this species in theupper Amazon region [78] This dietary intake of meatand eggs remains clandestine providing food and familyincome Turtles are sold in regional markets despitefederal prohibition legislation (law 51971965) [9-14]Several authors have noted that Amazon turtles are usedin local medicine [91516] and as pets and ornaments[17] Interestingly however turtles are subject to well-established and highly respected food taboos In manyinstances potential consumers do avoid eating them [9]The taboo certainly represents an important informalmechanism that could be more effective in conservationthan other top-down initiatives [1819]Following an intense exploitation over the past two

centuries the Giant South American Turtle and theYellow-Spotted River Turtle (Podocnemis unifilis) havebeen listed as endangered by the IUCN since 1996 [20]These species have increased in numbers recently be-cause of the governmentrsquos surveillance of nesting bea-ches [21] Currently Podocnemis expansa is listed ashaving a low extinction risk [22] as a result of conservationprograms The Podocnemis unifilis and P sextuberculataare vulnerable to extinction risk [23] Accepted cul-tural customs and the local dietary and monetaryneeds of the natives can be in conflict with conserva-tion programs and the implementation of federal laws[18] The adopted model of repression reduces but doesnot eliminate the capture and consumption of turtles inthe Negro River [1024-26] Purus River [92728] andSolimotildees River [29]This study was conducted around the Purus River which

is known for the consumption and illegal trade of turtles[28] In spite of the Brazilian legislationrsquos declaration of

illegality in 1967 the consumption of turtles in the city ofTapauaacute is common [30]The majority of people consume turtles because the

price is low compared with that of fish and beef [31]Wilkie and Godoy [32] suggesting that domestic economyhas changed redefining the concept of subsistence andthe patterns of consumption of bushmeat due increased ofincome [32] Therefore domestic consumers of turtles forsubsistence in Tapauaacute are aware of such an irregularity Avariety of factors could be involved that the consumptionof turtles is accepted culturally that the area has a popula-tion of low income [33] and that there is an absence ofstate involvement which although present in Abufari Bio-logical Reserve (ABR) has limited performance due to thelack of human and financial resourcesUnderdeveloped countries in South America have the

following in common (a) colonialism unstable govern-ments and poor democracy (b) production of items forinternational export including feedstock and agriculturalproducts such as ore wood and other materials for nat-ural resourcesndashbased industries and (c) controlled byforeign investment All of these parameters are relatedto the informal economy [34]The aim of this study was to quantify the illegal trade

of turtles in Tapauaacute and understand its impact on thelocal economy based on two components (a) domesticconsumption and (b) the turtle marketing chain in themiddle Purus River

MethodsStudy siteThis study was conducted in the municipality of Tapauaacutelocated 4485 km from Manaus capital of the state ofAmazonas (05deg37primeS and 63deg11primeW) (Figure 1) Tapauaacute hasan estimated population of 20000 inhabitants and anurbanization rate of 5566 in 2000 census [33] In 2007Tapauaacute had 4080 private households of which 3704 wereinhabited [33] About 68 of the population is low in-come based on the Brazilian Institute of Geography andStatistics (IBGE)rsquos 2000 census [33] Inhabitants are mostlydescendants of migrants from the miscegenation of theBrazilian Northeast and indigenous ethnicities (such asApurinatilde Palmari Jamamadi and Catauaxi [3035]) Thecity of Tapauaacute was established in 1938 as an administrativedistrict of the city of Canutama and declared a municipal-ity in 1955 [30]

ProceduresTo estimate turtle consumption interviews were con-ducted over 2 consecutive years (2006 and 2007) duringthe summer period which is the high-consumption sea-son in the Amazon (July to December in previous years)The interviews were conducted in urban areas and iso-lated communities In January of 2006 101 interviews

Ipix

una

Riv

er

River

River

ReserveBiological

Beach

National ParkheadwatersLake Jari

Abufari River

I LApurinatilde Satildeo Joatildeo

I L

Chapeacuteu Lake

Figure 1 Map of the city of Tapauaacute (gray) in the state of Amazonas (AM) and location of fishing areas of turtles in the Purus River


were conducted (72 in urban areas and 29 in ruralareas) In 2007 124 interviews were conducted in urbanareas only due logistics conditionsThe experimental design was randomized with respect

to households Residents interviewed belonged to all agegroups (14ndash80 years) and differed only in schooling (in-complete primary [55] or functionally illiterate [24]formal education completed high school [29] primaryeducation [25] and incomplete high school [24])Data on age were grouped into five age classes (Class I14ndash20 Class II 21ndash30 Class III 31ndash40 Class IV 41ndash50and Class V over 50 years) In January of 2007 the con-sumption of 2006 was classified by classes of annualconsumption per household (Class I 1ndash5 animalsyearClass II 6ndash10 animalsyear Class III 11ndash15 animalsyearClass IV 16ndash20 animalsyear Class V 21ndash25 animalsyearClass VI over 25 animalsyear) In addition the followingwas obtained frequency of egg consumption percep-tion of environmental legislation the number of animalsconsumed per household per species and the purchaseprice and origin of animals consumed

Consumption data collected in 2006 were analyzed ac-cording to the measure of central tendency for groupeddata [36] The Student t-test was used to compare totalconsumption of turtles among households in rural andurban areas (2006 data) A G-test was used to compareconsumption frequency within the consumer classes(IndashVI) between the areas of the municipality (urbanand rural) age classes (I and V) and the educationlevel of the respondentsContinuous data consumption and purchase priceobtained in December 2007 were explored using de-

scriptive statistics [36] From the 2007 analysis were pro-duced estimates of total consumption (EC) biomass (B)consumption per capita (CP) estimated expenditure(EE) and expenditure per capita (EP) as shown in theequations below

EC frac14 Fr 2356 C eth1THORN

where EC is the estimated number of animals consumedFr is the percentage of households (0ndash1) where the


consumption of the species occurred (2356 = number ofoccupied households in the urban area [37] C is themedian intake of animals by species in each householdbecause the values of consumption purchase price andexpenses do not meet normality [36]

B frac14 Fr 2 356 EC eth2THORNCP frac14 B= Fr 10 013eth THORN kg eth3THORN

where B is the estimated biomass of animals consumed inthe urban area of Tapauaacute CP is the per capita consump-tion in kilograms (10013 total population of the urbanarea of Tapauaacute in 2007 [37]) kg is the average weight ofturtles (P sextuberculata = 09 kg P unifilis = 288 kgP expansa = 499 kg) The average weights were calcu-lated from animals seized during surveillance of theABR by the Brazilian Institute of Environment andRenewable Natural Resources (IBAMA) [28] and fromexperimental animals caught in the fishery in 2007

EE frac14 EM Fr 2356 eth4THORNwhere EE is the estimated expenditure for the purchaseof real turtles in Tapauaacute EM is median spending perhousehold in the urban area of Tapauaacute

EP frac14 EE= Fr 2356eth THORN eth5THORNwhere EP is per capita spending in US dollars Medianvalues estimated by Equations 1ndash5 are given a percentilefollowed by the 25 and 75 obtained which corre-sponds to the original dataTo study the turtle fishery and trade chain we used

snowball sampling methodology [38] with the first keyinformant (ldquowho makes a living catching turtles andcould give an interviewrdquo) indicated by the communityInterviews were conducted in January 2007 with fourkey interviewers in Tapauaacute mainly participants of turtleartisan fishermen groups Information such as the num-ber of fishing events per year number of days using afishery number of people involved in fishing number ofteams working on fishing teamsrsquo average number ofweekly fishing events by week different kinds of fishingartifacts (dimensions and mesh size) and yield (numberof turtles caught by species sex of animal estimatedsize the amount of sales and gross changes in prices inBrazilian currency) was estimatedWe developed a model of the supply chain with key

components identified in the following categories (a)free-narrative interviews with three regional fishermenon boats in the Purus River lines with cargo of a capacitybetween 50 and 100 tons (b) interviews with four turtleartisan fishermen (c) interviews with 196 residents ofurban areas and 29 of rural areas (d) the recorded sei-zures [2728] (e) research in the Abufari reproductive

area (f ) study of the resource use and turtle ecology inthe Abufari area and (g) experimental fisheries Fromthis model we constructed four turtle conservation sce-narios in the Purus River floodplain

Results and discussionConsumption of turtles occurred in 100 of urban andrural households (a total of 101) in 2006 A study byRebecirclo and Pezzuti [12] showed that in the city of NovoAiratildeo 188 of interviewees reported never havingconsumed turtles In Manaus these indices were higheramong suburbs (444) and University of Amazonasstudents (583) [12] In Tapauaacute urban consumption oc-curs through all months of the year (414 of house-holds in the city) while in rural areas it occurs mainlyduring the summer (JulyndashDecember in 431 of house-holds [Figure 2])In rural areas the Yellow-Spotted River Turtle (P uni-

filis) (72) is the preferred species while in the city pref-erences were split between the Six-tubercled RiverTurtle (P sextuberculata) (417) and the Yellow-Spotted River Turtle (445) species of small andmedium size respectively Rebecirclo and Pezzuti [12] haveshown that P unifilis and P expansa were the most pre-ferred among interviewers of Manaus Novo Airatildeo andJauacute National Park perhaps due to the size of these spe-cies in relation to P sextuberculata [12] The most con-sumed species in urban and rural areas of Tapauaacute was Psextuberculata (Figure 2) The Yellow-Spotted RiverTurtle was actively consumed in all sites evaluated byRebecirclo and Pezzuti [12] but the most consumed in JauacuteNational Park was the Big-headed Amazon River Turtle(Peltocephalus dumerilianus) in all years of the con-sumption monitoring [910122425] Most cheloniansmarketed in Tapauaacute weighed less than 2 kg similar tothose described at Itacoatiara [8] and Jauacute River [12]Egg consumption occurred only in the summer when all

species perform their nesting Eggs consumed were mostlyfrom the Six-tubercled River Turtle (P sextuberculata)although the preferred eggs were from the Yellow-SpottedRiver Turtle (P unifilis) In households of Tapauaacute theassessed consumption was an average 1457 plusmn 956 kg ofturtles per household for six months of the year (July toDecember) The average turtle consumption was greater inrural areas (2165 plusmn 799 turtles per household) than inurban (1126 plusmn 827 turtles per household) (t = minus5767GL = 99 p lt 0001) in 2007 This pattern was also ob-served for grouped dates collected in 2006 showing that agreater consumption of turtles appears more in rural thanin urban areas (GWillians = 27449 GL = 5 p lt 0001)In urban areas consumption predominates in Classes I(277) II (292) and III (138) while in ruralhouseholds consumption occurs most frequently inClasses II (138) IV (138) and VI (552) There

Figure 2 Results of interviews on the consumption of turtles in the city of Tapauaacute Amazon Brazil in 2006


was no significant difference in consumption frequencyregarding the age of respondent (GWillians = 22267GL = 20 p = 0326) It was found that the educationlevel influences the frequency of consumption perhousehold (GWillians = 46351 GL = 88 p = 00007)Respondents with incomplete primary education ac-count for 194 of consumers in Class V (75) and VI(118) while respondents with high school educationcomplete and incomplete account for 183 of the re-corded consumption frequency of Classes I and IIThe origin of turtles consumed in the city (667 of

households) and in rural areas (552 of households) wasnot specified When asked if animals captured in the ABRwere consumed 862 of households in rural areas and887 of urban areas said yes which corroborates the ob-servations of Ferrarini [30] Most of the respondents inurban (794) and rural areas (580) did not agree withthe law that completely prohibits trade instead of defining

what is and is not allowed The interviewers recognizedcaptive breeding (542) and management (389) as thebest solutions among the options discussed (no opinion181 do not eat more turtles 167 no restriction forcapture in the wild 125)In all of the 124 selected households evaluated in

2007 at least one chelonian was consumed every year(Table 1) In terms of the most-consumed species the re-sults are similar to the 2006 interviews in which theSix-tubercled River Turtle (P sextuberculata) was themost consumed Financially the Giant South AmericanTurtle (P expansa) has a higher market value (Table 2)The maximum spending per household was $21929 USdollars a year for three species which shows consump-tion at all economic levelsIn 2006 over 34 tons (living biomass) of turtles were

acquired by consumers Of this amount 401 was Pexpansa 383 was P sextuberculata and 216 was P

Table 1 Number and percentage of households consuming freshwater turtles in the city of Tapauaacute in 2007

Species N() Animals C EC B CP

P sextuberculata 98 (79) 1102 8 (5ndash15) 14888 (9305ndash27915) 13399 (8374ndash25123) 72 (45ndash135)

P unifilis 69 (55) 169 2 (1ndash3) 2620 (1310ndash3930) 7545 (3773ndash11318) 576 (288ndash864)

P expansa 74 (59) 198 2 (1ndash4) 2812 (1406ndash5624) 14032 (7016ndash28064) 998 (499ndash1996)

N () = number of animals whose consumption was reported C =mean consumption per household EC = number of animals estimated B = estimated biomassconsumed (in kg) CP = Consumption per capita (gday) Values brackets represent 25 and 75 percentiles

Table 2 Median spending per household as declared inJanuary 2007 and estimated annual expenses with thepurchase of turtles by species in urban Tapauaacute

Species Average spending byhousehold (US$)

Annual estimatedspending (US$)

P sextuberculata 1305 (799ndash2319) 2430762 (1488826ndash4317616)

P unifilis 2872 (1665ndash4596) 3765118 (2182252ndash6024189)

P expansa 8010 (3697ndash14741) 11262533 (5198072ndash20723882)

Values brackets represent 25 and 75 percentiles


unifilis for food consumption in Tapauaacute (Table 1) Thisconsumption per capita was 159 gpersonday The aver-age expenditure was estimated about $200 US dollars inthe summer of 2006 (Table 2) in the city of Tapauaacute onlyThe estimated consumer spending in Tapauaacute was $175000US dollars representing 271 of resource transfers fromthe Brazilian Federal Government in 2007 ($644320608US dollars) for this city [39] Tapauaacute is a city with a lowHuman Development Index and great social inequality asmeasured by the Gini Index [33] suggesting that the con-sumption of smaller species is directly related to lower so-cial status The population with a higher purchasing poweracquires more valuable species such as the Giant SouthAmerican Turtle (P expansa) which can cost seven timesmore than the Six-tubercled River Turtle (P sextubercu-lata) and three times more than the Yellow-Spotted RiverTurtle (P unifilis)The turtle fisheries last about two and a half days and

gather groups of up to 6 anglers It was estimated thatthere were 20 groups who sell a production in the muni-cipality (between 45 and 100 fishermen) The turtle arti-san fishermen use modern techniques known locally asldquocapasacordquo to increase fishing yields but these methodsalso lead to a high proportion of damaged turtles thatcannot be soldWe identified six main fishing spots (Figure 1) Three

were within the limits of ABR and three were in neigh-boring areas In 16 weeks (AugustndashNovember) eachfisherman profited an average of $2300 US dollars($17500 US dollarsfishermenweek)The components of the commercial chain (Figure 3) are

(1) indigenous Apurinatilde and (2) residents of bordering vil-lages (communities) both of which capture and collectturtle eggs mainly for food (subsistence) Another group(3) of local smugglers buy and sell turtles to the commu-nity in exchange for manufactured goods and (4) regionalsmugglers buy in Tapauaacute Laacutebrea and Beruri to sell inManaus and Manacapuru These traders use intermedi-aries who resell at higher prices Finally (5) there areprofessional fishermen who have mastered the catchingtechniques and invest time and money during 4 months(August to November) solely to capture turtlesIn the Purus River area 100 of respondents in the

2 years of monitoring reported consuming at least threespecies of turtles (Podocnemis spp) From July to Decemberextensive sandbars arise in the Purus River which turtles

use for nesting [25] Researchers such as Wilkie andGodoy [32] estimate that an increase in income leads to areduced consumption of game meat but the present studyrefutes this theory Several studies have shown that con-sumption and commercialization of turtles in Amazonia isa habit rooted in the culture of local peoples [8-1012-14]The present study shows that the age of respondents didnot influence the frequency of consumption corroborat-ing the idea that consumption in Amazonia is cultural Inthe state of Amazonas people consume turtles weekly asseen in Novo Airatildeo while in Manaus consumption is lessfrequent [12]In the city of Tapauaacute weekly consumption of turtles is

more common among respondents in rural areas especiallyduring the summer Fish is the main source of animal pro-tein for Amazonian riverside populations and per capitaconsumption in the Amazon between different areas variedfrom 165 gpersonday or 600 kgpersonyear in MonteAlegre [40] to 500ndash800 gpersonday or 1825ndash292 kgpersonyear on the Solimotildees River [41] Besides the con-sumption of fish game animals were measured at a percapita consumption of 136 gpersonday in the middleAmazon [40] In Tapauaacute per capita consumption of turtlesis higher (159 gpersonday of turtle) but this value re-flects the biomass of live animals The yield of P expansaranges from 207 [42] to 50 of the weight of turtleswithout the hull [43]The consumption of turtles has other nutritional bene-

fits as well as being a good source of protein and haveone specific market mainly P expansa and P unifilisthat are preferred by many people [7264445] The hullof P expansa is rich in calcium and phosphorus andcontains significant amounts of iron zinc copper man-ganese and cobalt [47] A study performed in the regionof Pracuuacuteba (Amapaacute State Brazil) shows that of the 35plant species that are part of the turtlesrsquo diet 12 present

Environmental factorsoC humidity river level

Demographic parametersbirth rate natural mortality migration emigration predation

Stock of turtles PodocnemididaeP expansa P unifilis

P sextuberculata

Indigenous

Riverine peoples Turtle artisanal fishermen

Boat (fishing and passenger transport)

Intermediariessmugglers

Small urban centersTapauaacute City - This study

Large urban centersManaus Beleacutem and others large cities

Figure 3 Compartment model of chain marketing of turtles in the Purus River Boxes indicate the social actors of the chain arrows indicatethe direction in which the resource is being conducted open clouds indicate indeterminate destination resource or raw


protein greater than 100 4 have lipid content higherthan 100 9 have high content of crude fiber 6 havemore than 50 of mineral matter 6 have more than 10calcium and 5 have more than 02 phosphorus [48] Incaptivity the meat from the males of P expansa hashigher levels of copper calcium and phosphorus whilethe meat of the females has higher sodium and magne-sium [49] The meat of the Giant South American Turtle(P expansa) has higher levels of calcium (mean 189 mg to242 mg for females and males respectively) to those foundin beef (7 mg) and chicken (12 mg) [5051] From an envir-onmental standpoint turtle consumption has a heavy im-pact because it removes long-living organisms that areresponsible for processing energy nutrient cycling disper-sal of riparian vegetation and maintenance of water qualityin the lowland ecosystem [46]Our estimates demonstrate that thousands of animals

are consumed annually in Tapauaacute along the margins of amajor fishing river in the Amazon [5253] where fish isthe main food resource However it is unclear what im-pact this activity has on natural turtle populations It canbe observed that the trading price of the Six-tubercledRiver Turtle (P sextuberculata) is lower than the othertwo species (Table 1) equating to the price of chickenmeat per kilo ($350 US dollars) The purchase price of

the three species of turtle is less than beef on average inTapauaacute ($440 US dollarskg personal observation)The capture and trade of turtles in Tapauaacute generates in-

come for fishermen but its illegality excludes it from officialtax statistics The gross domestic product (GDP) of the cityof Tapauaacute in 2005 was approximately $40000 US dollarsfrom the provision of services and agricultural activities[33] The activity is profitable but has a risk of fines andseizure by environmental protection agencies Althoughthe IBGE names fishing as the largest source of employ-ment and income generation in Tapauaacute the turtle artisanfishermen interviewed did not have a high social statusand were eligible for government welfare benefits [33]Concerned with the need for turtle conservation in

the Purus River respondents identified the developmentof captivity and domestication as the main alternative tothe present situation For human ecology environmen-tal policies seek to change the habits of the populationAlthough both rural and urban consumers refer to the ideaof conservation reform only a small portion of respon-dents in 2006 (1) and none of those 2007 have nevereaten turtle Among the options proposed by respondentsone alternative is a more coherent quota managementof the wild areas similar to ldquoparticipatory managementrdquoproposals [122425] in which users manage the natural


resources Caputo et al [54] show that nest communitymanagement is efficient and can be done at low cost Thesecond alternative was making captive breeding moreviable Podocnemidids grow slowly and consume 12ndash15grams of fish feed per day [55] It has the problem of alow-income hull [4445] which increases the cost andmarket priceConsumption management can involve the community

and the suppliers of young turtles taken from nature butthe federal laws 51971967 and 96051998 (regulatoryframeworks of environmental management in Brazil) donot make this possible We considered that all stake-holders of resource turtles in the lower Purus River shouldbe involved in an integrated process as has occurred inother regions of the Amazon basin [242954] Integrationis imperative because animal use and exploitation com-bined with the cultural aspects of human interaction withanimals can contribute to pressure on animal speciesleading to either their sustainable use or extinction [56]Several authors posit that habitat destruction and preda-

tory use was the main threat to the natural populations ofreptiles [132646] Alves and Santana [13] state that it isessential for conservation and management programs toinvolve the local communities who exploit the natural re-sources Community-based efforts are limited by scarcefunding consistent and effective involvement of stake-holders and political infighting [13] Conway-Gomez [57]argues that a management strategy has the most potentialto redirect human behavior from unrestrained exploitationto the sustainable use of a resourceOther authors recommend community-managed captive

breeding of the faster-maturing P unifilis and P vogli inthe Orinoco Basin to satisfy turtle consumption needsThese measures along with improved nesting-beach pro-tection may encourage the recovery of populations of Pexpansa and make their legal subsistence harvesting pos-sible in the future [58] These authors recognize that ldquoafter21 years of protecting turtles in and around the Arrau Tur-tle Wildlife Refuge (AWR) it has become obvious that usingforce to eliminate consumption of this traditional staple isnot an option in the Middle Orinoco The consumption ofP expansa P unifilis and P vogli are deeply rooted in thelifestyle and economic reality of the riberentildeordquo [58]It may be that catches are sustainable and long-term

monitoring will be able to determine this sustainabilityManaging these resources through participatory plan-ning and an integrated ecosystem-based plan is not cur-rently possible because the law prohibits all turtle use

ConclusionOur results corroborated that consumption of Podocnemisspp turtles is common in the Amazon Basin particularlyalong the Purus River where the major nesting site ofturtles is located in the state of Amazonas

We believe that our results evaluate the full impact ofturtle consumption and advocate the management of tur-tle consumption to contribute to the conservation of theregionrsquos turtle populations Our data show that consump-tion occurred independent of age and social class Thus itis clear that the Brazilian government should alter the par-adigms currently in place and initiate a new turtle con-sumption management program that includes users indecision making and would indeed contribute to the man-agement and conservation of freshwater turtles in Brazilparticularly in the Brazilian Amazon

Competing interestsThe authors declare that they have no competing interests

Authorsrsquo contributionsJPL JCBP DFS and GHR conceived the study and participated in its designand coordination JPL collected the dates during two years on the city ofTapauaacute PHRA and ATO analyzed the data and drafted the results for thediscussion All authors helped to draft the manuscript and read and approvethe final manuscript

AcknowledgmentsThe authors thank the Conselho Nacional de Desenvolvimento Cientiacutefico eTecnoloacutegico (CNPQ) for providing grants (CNPq 5571142005-5 and CNPq5540092006-4) to FAPEAM Foundation for the research fellowship providedto the first author to Human Ecology Laboratory of INPA for the operationalsupport to Program of Post-Graduated in Ecology (PPG-ECO-INPA) forinfrastructure The authors would like to acknowledge the importantcontributions to the manuscript made by Dr Richard Brinn from FloridaInternational University (Miami USA) MSc Harold Wright from AmazonasState University (UEA) and to team of Edanz Editing for a review of theEnglish Our gratitude is extended to the interviewees in the Purus Riverwho made time to share their knowledge with us Thanks also to ElionaiFerreira for help with data collection Thanks are also due to the anonymousreviewers for their truly helpful comments

Author details1Instituto Federal de Educaccedilatildeo Ciecircncia e Tecnologia do Amazonas (IFAM)Campus Presidente Figueiredo Av Onccedila Pintada 1308 Galo da SerraPresidente Figueiredo AM CEP 69735-000 Brazil 2Nuacutecleo de Altos EstudosAmazocircnicos (NAEA) Universidade Federal do Paraacute (UFPA) Campus doGuamaacute Beleacutem PA CEP 66075-110 BRAZIL 3PPG- Ecologia Laboratoacuterio deManejo de Fauna Instituto Nacional de Pesquisas da Amazocircnia (INPA)Manaus AM CEP 69011-970 BRAZIL

Received 17 September 2013 Accepted 8 January 2014Published 27 January 2014

References1 Alves RRN Vieira KS Santana GS Vieira WLS Almeida WO Souto WMS

Montenegro PFGP Pezzuti JCB A review on human attitudes towardsreptiles in Brazil Environ Monit Assess 2012 1846877ndash6901

2 Bates HW The Naturalist on the River Amazon London Murray 18763 Silva Coutinho JM Sur les tortues de LrsquoAmazone Bulletin the la Socieacuteteacute

Zoologique drsquoAclimatation Volume 2 Paris Tome V 18684 Gilmore RM Fauna e Etnozoologia da Ameacuterica do Sul Tropical In Suma

Etnoloacutegica Brasileira Up to data edition of Handbook of South AmericanIndians Edited by Ribeiro BG Ribeiro D Rio de Janeiro Copper Square PublInc 1986189ndash233

5 Carvajal G Relacioacuten del nuevo descubrimiento del famoso Rio Grande de lasAmazonas Fondo de Cultura Econocircmica 1st edition 1955

6 Smith NJH Destructive exploitation of the South American river turtleYearb of the Assoc of Pac Coast Geographers 1974 3685ndash120

7 Pritchard PCH Trebbau P Turtles of Venezuela Society for the studyAmphibians and Reptiles Contributions to Herpetology Oxford Ohio Societyfor the Study of Amphibians and Reptiles 1984


8 Smith NJH Aquatic turtles of Amazonia an endangered resource BiolConserv 1979 16165ndash176

9 Pezzuti JCB Pantoja-Lima J Feacutelix-Silva D Begossi A Uses and taboos ofturtles and tortoises at Negro River Amazonas Brasil J Ethnobiol 201030(1)153ndash168

10 Rebecirclo GH Lugli L The Conservation of Freshwater and the Dwellers ofthe Amazonian Jauacute National Park (Brazil) In Etnobiology in Human WelfareEdited by Jain SK New Delhi Deep Publications 1996253ndash358

11 Pezzuti JCB Vogt RC Nesting ecology of Podocnemis sextuberculata(Testudines Pelomedusidae) in the Japuraacute river Amazonas BrazilChelonian Conserv and Biol 1999 3(3)419ndash424

12 Rebecirclo GH Pezzuti JCB Percepccedilotildees sobre o consumo de quelocircnios naAmazocircnia consideraccedilotildees para o manejo atual Ambiente e Soc 2000685ndash104

13 Alves RRN Santana GG Use and commercialization of Podocnemisexpansa (Schweiger 1812) (Testudines Podocnemididae) for medicinalpurposes in two communities in North of Brazil J Ethnobiol Ethnomed2008 4(3)1ndash6

14 Schneider L Ferrara CR Vogt RC Burger J History of Turtle Exploitationand Management Techniques to Conserve Turtles in the Rio Negro Basinof the Brazilian Amazon Chelonian Conserv and Biol 2011 10(1)149ndash157

15 Alves RRN Rosa IL Zootherapeutic practices among fishing communitiesin North and Northeast Brazil a comparison J Ethnopharmacol 200711182ndash103

16 Alves RRN Rosa IL Zootherapy goes to town The use of animal-basedremedies in urban areas of NE and N Brazil J Ethnopharmacol 2007113541ndash555

17 Colding J Folke C The taboo system lessons about informal institutionsfor nature management Georgetown IntrsquoL Envtl Law Rev 2000 12413ndash445

18 McDonald DR Food Taboos a primitive environmental protectionagency (South America) Anthropos 1977 72734ndash748

19 Salera Junior G Malvasio A Giraldin O Relaccedilotildees Cordiais iacutendios Karajaacutetartarugas e tracajaacutes vivem em harmonia no rio Araguaia Ciecircncia Hoje2006 39(229)61ndash63

20 Machado ABM Martins CS Drummond GM Lista da fauna brasileiraameaccedilada de extinccedilatildeo incluindo as espeacutecies quase ameaccediladas e deficientesem dados Fundaccedilatildeo Biodiversitas Belo Horinzonte 2005

21 IBAMA Projeto Quelocircnios da Amazocircnia - 10 anos Inst Brasileiro do MeioAmbiente e dos Recursos Naturais Renovaacuteveis XVI Brasiacutelia IBAMA 1989

22 IUCN UCN Red List of Threatened Species 2006 httpwwwiucnredlistorgdetails178220


24 Rebecirclo G Pezzuti JCB Lugli L Moreira G Pesca artesanal de quelocircnios noParque Nacional do Jauacute (AM) Bol Mus Para Emilio Goeldi 20051(1)111ndash127

25 Pezzuti JCB Rebecirclo GH Felix-Silva D Pantoja-Lima J Ribeiro MC A caccedilae a pesca no Parque Nacional do Jauacute Amazonas In Janelas para aBiodiversidade Edited by Borges SH Durigan CC Iwanaga S ManausFundaccedilatildeo Vitoacuteria amazocircnica 2004213ndash228

26 Vogt RC In Conservation and Management of Ornamental Fish Resources ofthe Rio Negro Basin Amazonia Brazil - Projeto Piaba Edited by Chao NLPetry P Prang G Sonneschien L Tlusty M Manaus Editora da UniversidadeFederal do Amazonas 2001245ndash262

27 Kemenes A Pantoja-Lima J Tartarugas sob ameaccedila Ciecircncia Hoje 200622870ndash72

28 Kemenes A Pezzuti JCB Estimate of trade traffic of Podocnemis(Testudines Pedocnemididae) from the Middle Purus River AmazonasBrazil Chelonian Conserv and Biol 2007 6(2)259ndash262

29 Fachiacuten-Teraacuten A Vogt RC Thorbjarnarson JB Patterns of use and hunting ofturtles in the Mamirauaacute Sustainable Development Reserve AmazonasBrazil In People and Nature Wildlife Conservation in South and CentralAmerica Edited by Silvius KM Bodmer R Fragoso JM New York ColumbiaUniversity Press 2004362ndash377

30 Ferrarini SA Rio Purus Histoacuteria Cultura e Ecologia 1ordfth edition Satildeo PauloFTD 2009

31 Rushton J Viscarra R Viscarra C Basset F Baptista R Brown D Howimportant is bushmeat consumption in South America now and in thefuture 2005 Downloaded January 10 2010 httpwwwodiorgukpublications2418-important-bushmeat-consumption-south-america-now-future

32 Wilkie DS Godoy RA Income and price elasticities of Bushmeat DemandLowland Amerindian Societies Conserv Biol 2001 153761ndash769

33 IBGE Censo Demograacutefico 2000 e Pesquisa de Orccedilamentos Familiares - POF20022003 2011 httpwwwcidadesibgegovbrxtrastemasphplang=ampcodmun=130410ampidtema=118ampsearch=amazonas|tapaua|Iacutendice-de-desenvolvimento-humano-municipal-idhm-

34 Schneider F In Size and measurement of the informal economy in 110countries around the world Workshop of Australian National Tax CentreANU Canberra Australia 2002 httpwwwrelooneyinfoSI_ExpeditionaryShadow-Economy_13pdf

35 Mello MD Do sertatildeo cearense agraves barrancas do Acre 1ordfth edition CaleraroLtda Manaus 1994

36 Zar JH Biostatistical Analysis 4ordfth edition Prentice - Hall Inc Upper SaddleRiver New Jersey 1999

37 IBGE Contagem da populaccedilatildeo 2007 Rio de Janeiro Instituto Brasileiro deGeografia e Estatiacutestica ndash IBGE 2007

38 Biernacki P Waldorf D Snowball sampling problems and techniques ofchain referral sampling Sociol Methods and Res 1981 10(2)141ndash163

39 BRASIL Portal da transparecircncia do Governo Federal 2011 httptransparenciagovbrPortalTransparenciaListaAcoesaspExercicio=2007ampSelecaoUF=1ampSiglaUF=AMampNomeUF=AMAZONASampCodMun=0279ampNomeMun=TAPAUAampValorMun=1288641216

40 Isaac VJ Cerdeira RGP Avaliaccedilatildeo e monitoramento de impactos dos acordosde pesca na regiatildeo do Meacutedio Amazonas IbamaProacuteVaacuterzea Manaus 2004

41 Fabreacute NN Alonso JC Recursos Iacutecticos no Alto Amazonas Sua Importacircnciapara as populaccedilotildees ribeirinhas Bol Mus Para Emiacutelio Goeldi seacuter Zool 1998119ndash55

42 Rodrigues MJJ Cardoso EC Cintra IHA Morfometria e rendimento decarcaccedila da tartaruga-da-Amazocircnia Podocnemis expansa (Schweigger1812) capturada em ambiente natural Bol Teacutec Cient CEPNOR 20044(1)67ndash75

43 Ferreira-Luz VL Stringhini JH Bataus YSL Fernandes ES Paula WA NovaisMN Reis IJ Rendimento e composiccedilatildeo quiacutemica de carcaccedila datartaruga-da-Amazocircnia (Podocnemis expansa) em Sistema ComercialR Bras Zootec 2003 32(1)1ndash9

44 Paacutedua LFM Alho CJR Carvalho AG Conservaccedilatildeo e manejo da tartaruga-da-amazocircnia Podocnemis expansa na Reserva Bioloacutegica Rio Trombetas(Testudines Pelomedusidae) Brasil Florestal 1983 5443ndash53

45 Redford KH Robinson JG The game of choice patterns of indian andcolonist hunting in the neotropics Am Anthropolist 1987 89650ndash667

46 Moll DL Moll EO The Ecology Exploitation and Conservation of River TurtlesNew York Oxford University Press 2004

47 Scarlato RC Gaspar A Composiccedilatildeo nutricional do casco da tartaruga-da-Amazocircnia (Podocnemis expansa) criada em cativeiro e em idade deabate Ciecircnc Tecnol Aliment Camp 2007 27(supl)41ndash44

48 Portal RR Lima MAS Luz VLF Bataus YSL Reis IJ Espeacutecies vegetaisutilizadas na alimentaccedilatildeo de Podocnemis unifilis Troschel 1948 (ReptiliaTestudinae Pelomedusidae) na regiatildeo do Pracuuacuteba -Amapaacute-Brasil CiecircncAnim Bras 2002 3(1)11ndash19

49 Gaspar A Silva TSP Composiccedilatildeo nutricional da carne da tartaruga-da-Amazocircnia (Podocnemis expansa) criada em cativeiro e em idade deabate Rev Inst Adolfo Lutz 2009 68(3)419ndash425

50 USDA - United States Departament of Agriculture Composition of FoodPoultry Products Volume 8 Washington DC USA Agriculture Handbook19795ndash8

51 Alian AM Sallam YI Dessouki TM Atia AM Evaluation and utilization ofturtle meat physical and chemical properties of turtle meat Egypt J ofFood Sci 1986 14(2)341ndash350

52 Lowe-Macconnell RH Ecological studies in tropical fish communitiesCambridge Cambridge University Press 1997

53 Batista VS Petrere M Characterization of the commercial fish productionlanded at Manaus The state of Amazonas Brazil Acta Amazon 200333(1)53ndash66

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Pantoja-Lima et al Journal of Ethnobiology and Ethnomedicine 2014 108 0 of 10httpwwwethnobiomedcomcontent1018

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doi1011861746-4269-10-8Cite this article as Pantoja-Lima et al Chain of commercialization ofPodocnemis spp turtles (Testudines Podocnemididae) in the PurusRiver Amazon basin Brazil current status and perspectives Journal ofEthnobiology and Ethnomedicine 2014 108

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Abstract

Background

Methods

Results

Conclusions

Background

Methods

Study site

Procedures

Results and discussion

Conclusion

Competing interests

Authorsrsquo contributions

Acknowledgments

Author details

References



RESEARCH Open Access

Chain of commercialization of Podocnemis sppturtles (Testudines Podocnemididae) in the PurusRiver Amazon basin Brazil current status andperspectivesJackson Pantoja-Lima1 Paulo HR Aride1 Adriano T de Oliveira1 Daniely Feacutelix-Silva2 Juarez CB Pezzuti2

and George H Rebecirclo3

Abstract

Background Consumption of turtles by natives and settlers in the Amazon and Orinoco has been widely studiedin scientific communities Accepted cultural customs and the local dietary and monetary needs need to be takeninto account in conservation programs and when implementing federal laws related to consumption and fishingmethods This study was conducted around the Purus River a region known for the consumption and illegal tradeof turtles The objective of this study was to quantify the illegal turtle trade in Tapauaacute and to understand its effecton the local economy

Methods This study was conducted in the municipality of Tapauaacute in the state of Amazonas Brazil To estimateturtle consumption interviews were conducted over 2 consecutive years (2006 and 2007) in urban areas andisolated communities The experimental design was randomized with respect to type of household To study theturtle fishery and trade chain we used snowball sampling methodology

Results During our study period 100 of respondents reported consuming at least three species of turtles(Podocnemis spp) Our estimates indicate that about 34 tons of animals are consumed annually in Tapauaacute along themargins of a major fishing river in the Amazon At least five components related to the chain of commercializationof turtles on the Purus River are identified Indigenous Apurinatilde and (2) residents of bordering villages(communities) (3) of local smugglers buy and sell turtles to the community in exchange for manufactured goodsand (4) regional smugglers buy in Tapauaacute Laacutebrea and Beruri to sell in Manaus and Manacapuru Finally (5) thereare professional fishermen

Conclusions We quantify the full impact of turtle consumption and advocate the conservation of the regionrsquosturtle populations The Brazilian government should initiate a new turtle consumption management program whichinvolves the opinions of consumers With these measures the conservation of freshwater turtles in the BrazilianAmazon is possible

Keywords Chelonian Amazon Turtle consumption Illegal trade Endangered species

Correspondence jacksonpantojagmailcom1Instituto Federal de Educaccedilatildeo Ciecircncia e Tecnologia do Amazonas (IFAM)Campus Presidente Figueiredo Av Onccedila Pintada 1308 Galo da SerraPresidente Figueiredo AM CEP 69735-000 BrazilFull list of author information is available at the end of the article

copy 2014 Pantoja-Lima et al licensee BioMed Central Ltd This is an Open Access article distributed under the terms of theCreative Commons Attribution License (httpcreativecommonsorglicensesby20) which permits unrestricted usedistribution and reproduction in any medium provided the original work is properly cited The Creative Commons PublicDomain Dedication waiver (httpcreativecommonsorgpublicdomainzero10) applies to the data made available in thisarticle unless otherwise stated

Pantoja-Lima et al Journal of Ethnobiology and Ethnomedicine 2014 108 of 10httpwwwethnobiomedcomcontent1018











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una

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Abstract

Background

Methods

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Conclusions

Background

Methods

Study site

Procedures


Conclusion

Competing interests


Acknowledgments

Author details

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Ipix

una

Riv

er

River

River

ReserveBiological

Beach


Abufari River


I L

Chapeacuteu Lake





















































P sextuberculata

Indigenous
































































































Abstract

Background

Methods

Results

Conclusions

Background

Methods

Study site

Procedures


Conclusion

Competing interests


Acknowledgments

Author details

References













































P sextuberculata

Indigenous
































































































Abstract

Background

Methods

Results

Conclusions

Background

Methods

Study site

Procedures


Conclusion

Competing interests


Acknowledgments

Author details

References




















































































Abstract

Background

Methods

Results

Conclusions

Background

Methods

Study site

Procedures


Conclusion

Competing interests


Acknowledgments

Author details

References

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