RESEARCH ARTICLE
Mul ispecies Fishe ies in he Lowe Amazon
Ri e and I s Rela ionship wi h he Regional
and Global Clima e Va iabili y
Wal e Hugo Diaz Pinaya
1☯¤
*, F ancisco Ja ie Lobon-Ce ia
3☯
, Pablo Pi a
4☯
,
Ronald Buss de Souza
2‡
, Juan F ei e
5‡
, Vic o ia Judi h Isaac
1‡
1Labo a o y o Fishe ies Biology and Managemen o Aqua ic Resou ces, Fede al Uni e si y o Pa á,
Belém, Pa á, B azil, 2Labo a o y o Me eo ology and Sa elli e Oceanog aphy, Sou he n Regional Cen e o
Space Resea ch, Na ional Ins i u e o Space Resea ch, San a Ma ia, Rio G ande do Sul, B azil,
3Depa men o E olu iona y Ecology, Na ional Museum o Na u al Sciences, Mad id, Spain, 4Depa men
o Applied Economics, Facul y o Economics and Business Adminis a ion, Uni e si y o San iago de
Compos ela, San iago de Compos ela, Galicia, Spain, 5G upo de Recu sos Ma inos y Pesque ías,
Uni e sidad de A Co uña, A Co uña, Galicia, Spain
☯These au ho s con ibu ed equally o his wo k.
¤Cu en Add ess: Labo a o y o Me eo ology and Sa elli e Oceanog aphy, Sou he n Regional Cen e o
Space Resea ch, Na ional Ins i u e o Space Resea ch, San a Ma ia, Rio G ande do Sul, B azil
‡These au ho s also con ibu ed equally o his wo k.
*[email p o ec ed]
Abs ac
This pape aims o desc ibe he spa ial- empo al a iabili y in ca ch o he main ishe y
esou ces o he Amazon Ri e and loodplain lakes o he Lowe Amazon, as well as ela -
ing he Ca ch pe Uni o E o wi h anomalies o some o he Amazon Ri e , a mosphe e
and A lan ic Ocean sys em a iables, de e mining he in luence o he en i onmen on he
Amazonian ishe y esou ces. Fin ish landings da a om he owns and illages o he
Lowe Amazon o he ishe ies o h ee si es (Óbidos, San a ém and Mon e Aleg e), we e
ob ained o he pe iod be ween Janua y 1993 and Decembe 2004. Analysis o a iance,
de ended co espondence analysis, edundancy analysis and mul iple eg ession ech-
niques we e used o he s a is ical analysis o he dis inc ime se ies. Fishe ies p oduc ion
in he Lowe Amazon p esen s di e ences be ween he Amazon Ri e and he loodplain
lakes. P oduc ion in he Amazon Ri e is app oxima ely hal o he one o he loodplain
lakes. This a iabili y occu s bo h along he Lowe Amazon Ri e egion (longi udinal g adi-
en ) and la e ally (la i udinal g adien ) o e e y ishing g ound s udied he e. The dis inc
en i onmen al a iables alone o in associa ion ac di e en ly on he ishe y s ocks and he
success o ca ches in each ishe y g oup s udied he e. Impo an a iables a e he looding
e en s; he soil he sea su ace empe a u es; he humidi y; he wind and he occu ence o
El Niño-Sou he n Oscilla ion e en s. Fishe y p oduc i i y p esen s a la ge di e ence in
quan i y and dis ibu ion pa e ns be ween he i e and loodplain lakes. This a iabili y
occu s in he egion o he Lowe Amazon as well as la e ally o each ishe y g oup s udied,
being dependen on he ecological cha ac e is ics and li e s a egies o each ish g oup con-
side ed he e.
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 1/29
a11111
OPEN ACCESS
Ci a ion: Pinaya WHD, Lobon-Ce ia FJ, Pi a P,
Buss de Souza R, F ei e J, Isaac VJ (2016)
Mul ispecies Fishe ies in he Lowe Amazon Ri e
and I s Rela ionship wi h he Regional and Global
Clima e Va iabili y. PLoS ONE 11(6): e0157050.
doi:10.1371/jou nal.pone.0157050
Edi o : Ma in Cas onguay, Ins i u Mau ice-
Lamon agne, CANADA
Recei ed: Sep embe 1, 2015
Accep ed: May 24, 2016
Published: June 17, 2016
Copy igh : © 2016 Pinaya e al. This is an open
access a icle dis ibu ed unde he e ms o he
C ea i e Commons A ibu ion License, which pe mi s
un es ic ed use, dis ibu ion, and ep oduc ion in any
medium, p o ided he o iginal au ho and sou ce a e
c edi ed.
Da a A ailabili y S a emen : The en i onmen al
da a and clima e indexes a e a ailable in public
eposi o ies as ollows: Me eo ological da a a e
a ailable in he websi e: www.es l.noaa.go /psd/da a/
g idded/. The sea su ace empe a u e da a a e
a ailable in he websi e: h ps://podaac.jpl.nasa.go /
da ase lis ?sea ch=Pa h inde . The hyd ological da a
a e a ailable in he websi e: h p://www.sni h.go .b /
hid oweb/. Clima e indexes a e a ailable in he
websi e: www.es l.noaa.go /psd/da a/clima eindices/
lis /. The se o aw ishing da a a e ob ained h ough
he B azilian Minis y o Fishe ies and he Chico
In oduc ion
Fishing is a majo ac i i y in he Amazon Ri e since he o igins o he ea lies na i e commu-
ni ies in he egion [1]. In he Lowe Amazon, his ac i i y is di e en om o he egions due
o he la ge amoun o species explo ed, hei p oduc ion and hei di e en impac s on each o
he human communi ies p esen in he egion [2]. The ishe y in his egion is essen ially a i-
sanal and based on a di e si y o ishing me hods, wi h di e en deg ees o echnological de el-
opmen . Di e en ishing ac ics a e equen ly applied, depending on he a ge species and
he local en i onmen [3], con ibu ing o inc ease he unce ain ies o ou unde s anding o
he ishe ies in he Amazon.
The es ima ed numbe o ish species in he Amazon anges om 1500–2000 o 8,000 spe-
cies acco ding o di e en au ho s [4–5]. Howe e , he comme cially exploi ed species a ies
wi hin a na ow ange o six o wel e species ha co espond o abou 80% o he o al ish
biomass landed [2]. The composi ion o he ca ch is ela ed o he speci ic en i onmen ha
p edomina es whe e he ishe y is made as well o he na u e and cos umes o he egional com-
muni ies. This is well exempli ied by he p edominance o scale ishes ela i e o ca ish in he
Cen al Amazon egion which is echoed in he ish supply o he local ma ke s [2].
Fish species exhibi adap a i e ac ics o cope wi h he seasonal changes in he hyd ological
cycle in he egions whe e hey occu : ei he he loodplain lakes and/o in he main cou se o
he Amazon Ri e [2]. In o de o unde s and he dynamics and composi ion o hese ish spe-
cies, i is c i ical o documen hei adap a i e ac ics and, he e o e, new esea ch is needed o
be e unde s and he biological cycles, eeding s a egies, me abolism, indi idual g ow h and
de elopmen and mig a ion beha iou o he Amazonian ish. [6–14].
The dis ibu ion and ecology o ishe y esou ces in he Amazon egion a e de e mined by
he na u al su oundings, a ailabili y o en i onmen s, me eo ological cha ac e is ics and a i-
abili y o he hyd ological cycle. Wi h a highe discha ge, he Amazon Ri e loods i s banks
and expand i sel o e he su ounding loodplains [2]. Thus, he looding dynamics is expec ed
o ac o e he ishe y dynamics. Ea ly wo ks show ha he e is a s ong ela ionship be ween
he Amazonian hyd ological cycle and he local ish ca ches h oughou he yea [15]. Flood-
plains and we land o es s a e ex emely aluable in ensu ing he success o Amazonian com-
me cial ishe ies, which leads o he consequen need o hei conse a ion [16–19].
To ensu e a sus ainable ishe y and i s long- e m conse a ion, he concep o managing
landscape uni s should be conside ed: we ough o unde s and he esou ces wi hin he en i-
onmen as a whole and hei a iabili y wi hin he i e - looding plains sys em. Likewise,
when conside ing he clima e a iabili y and changes, he ecological app oach aken o unde -
s and he ishe ies should conside he meso o mac o spa ial scales. This is pa amoun i we
aim o s eng hen ou public conse a ion policies and imp o e he managemen o he ishe -
ies esou ces in he Amazon Ri e Basin egion. These aspec s indica e he impo ance o
unde s anding he di ec in e ac ions be ween he li ing esou ces and hei en i onmen [2].
Some au ho s ha e s udied he a iabili y o he hyd ological cycle and i s ela ionship wi h
he dynamics, ec ui men and ca ch o comme cial species in inland wa e s, in di e se places
in he wo ld [20–32], bu no in he Amazon Ri e Basin. To con ibu e o his lack o knowl-
edge, his pape aims o s udy he spa ial- empo al a iabili y in ca ch o he main ishe ies
esou ces in he Lowe Amazon, conside ing he di e en aqua ic en i onmen s, i.e., he Ama-
zon Ri e and he loodplain lakes. This pape also aims o desc ibe he ela ionship be ween
ishe y p oduc i i y using he a iable CPUE (Ca ch pe Uni E o ) and anomalies o some
en i onmen al a iables o he i e -a mosphe e-ocean sys em, de e mining he in luence o
he en i onmen on he he success o he local ishe ies.
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 2/29
Mendes Ins i u e o Biodi e si y Conse a ion. The
ishing da a used he e we e p ocessed by he au ho s
o his pape as CPUE (ca ch pe uni e o ) and we e
made a ailable o PLOS ONE eade s in he
supplemen a y ile (S2 CPUE Ri e and S3 CPUE
Lake).
Funding: Funding o ansla ion and publishing was
p o ided by he P o-Rei o ia de Pesquisa e Pos-
G aduacao (www.p opesp.u pa.b ) and Fundacao de
Ampa o e Desen ol imen o da Pesquisa (www.
po al adesp.o g.b ) om Uni e sidade Fede al do
Pa a (www.po al.u pa.b ). WHDP was suppo ed by
B azilian Ph.D. Schola ships om he Coo denacao
de Ape eicoamen o de Pessoal de Ni el Supe io o
B azil (www.capes.go .b ). RBS was suppo ed by
Schola ship in Resea ch P oduc i i y PQ CNPq
308646/2013-4 om he B azilian Na ional Council o
Scien i ic and Technological De elopmen (www.
cnpq.b ). The unde s had no ole in s udy design,
da a collec ion and analysis, decision o publish, o
p epa a ion o he manusc ip . The speci ic ole o his
au ho is a icula ed in he 'au ho con ibu ions'
sec ion.
Compe ing In e es s: The au ho s ha e decla ed
ha no compe ing in e es s exis .
Ma e ials and Me hods
S udy a ea
The s udy a ea co e s he ishe ies g ounds o Óbidos, San a ém and Mon e Aleg e, in he
egion o he Lowe Amazon, be ween la i udes 1° 43’S–2° 37’S and longi udes 55°55’W–53°
46’W(Fig 1).
Ma e ials
Fishe ies da a. In o ma ion on ca ch pe species and ishing e o om Janua y 1993 o
Decembe 2004 was collec ed on a daily basis o each ishing ip by means o in e iews wi h
he skippe s o hose esponsible on he essels ha dock in he majo ca ch landing po s o
he s udy a ea [15]. The ime se ies o ishe ies da a included 163,546 iden i ica ion eco ds o
ishing uni s, whe e each eco d co esponds o a single ishing ip. Wi h he selec ion o a i-
bu es– ishing boa and gill ne – he se ies we e educed o 19,484 eco ds o he i e en i on-
men and 37,624 eco ds o he loodplain lakes, only conside ing he e he ishe ies in he
Lowe Amazon. This selec ion is jus i ied since i is known ha gill ne is he main ishing
me hod in he Lowe Amazon, and he ishing boa s (boa s wi h hei own c ew o ca ching
ish) a e he mos ep esen a i e uni s o his a isanal lee , accoun ing o o e 80% o all he
ishe ies p oduc ion in he egion [33]. A c i e ia o educing he numbe o species s udied
he e om all species caugh in he Lowe Amazon egion included he use o a mul i a ia e
analysis (discussed la e on his ex ). The analysis was pe o med o e a numbe o ish ami-
lies ha ep esen ed abou 80% o he local ish p oduc ion in each o he wo en i onmen s
s udied he e: i e and loodplain lakes.
Due o he low abundances and small impo ance on he egional ishe ies, some ish ami-
lies we e no conside ed he e. They a e: Anos omidae, Se asalmidae and Lo ica iidae a
Fig 1. S udy a ea. The Lowe Amazon and he subdi ision in h ee a eas: Óbidos, San a ém and Mon e
Aleg e.
doi:10.1371/jou nal.pone.0157050.g001
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 3/29
Óbidos ( o he i e en i onmen ); Lo ica iidae and Do adidae a Óbidos and Clupeidae a
Mon e Aleg e ( o he loodplain lakes). The mos ep esen a i e ish amilies o ou s udy a ea
we e he Pimelodidae (in he Amazon Ro e and especially du ing he d y season) and he
Hypoph halmidae (in he lakes and especially du ing he we season).
Hyd ological da a. The hyd ological da a o he Amazon Ri e used he e we e he dis-
cha ge (ARD) o Óbidos, wa e le el (WL) o San a ém and a spa ial a e age o ain all (RF)
o he Lowe Amazon egion we e ob ained om he B azilian Wa e Managemen Agency
(ANA, Agência Nacional de Águas–www.ana.go .b ). Time se ies a he mon hly empo al
esolu ion we e ob ained o he same pe iod o he ishe y da a, co e ing Janua y 1993 o
Decembe 2004. The ime se ies we e used o calcula ing he clima ology means o discha ge,
wa e le el and ain all o he Lowe Amazon Ri e egion du ing he pe iod analysed he e.
Me eo ological and oceanog aphic da a. O he me eo ological da a apa om ain all
we e ob ained om he NCEP/NCAR (Na ional Cen e s o En i onmen al P edic ion /
Na ional Cen e o A mosphe ic Resea ch) Reanalysis P ojec . We used da a om bo h N/N
Reanalysis [34] and Reanalysis 2 [35] da abanks. Mon hly a e ages we e used, dis ibu ed in a
Gaussian G id wi h a spa ial esolu ion o 1.8758 km x 1.9058 km (la i ude/longi ude). The a -
iables s udied he e we e zonal (u) and me idional ( ) wind su ace (10 m) anomalies, su ace (2
m) speci ic humidi y (SPFH), minimum ai empe a u e (TMP), soil empe a u e (TMPs c),
po en ial e apo a ion (PEVPR), la en hea lux (LHF) and uno (RUNOF). The me eo ologi-
cal da a is publicly a ailable on-line (h p://www.es l.noaa.go /psd/da a/g idded/).
Mon hly sea su ace empe a u e (SST) da a we e also ob ained in a 4 × 4 km g id along he
coas o Pa á and Amapá s a es in he B azilian Amazonia, as well as o he mou h o he Ama-
zon Ri e . This oceanog aphic a iable was ob ained om he “Op imum In e pola ion Sea
Su ace Tempe a u e Ve sion 2—Fi s Guess SST Field”da ase , p ocessed wi h he NLSST
(Non Linea Sea Su ace Tempe a u e) algo i hm, a ailable on he da abase o he Pa h inde
p ojec .5. (PV5) de eloped by he NODC (Na ional Oceanog aphic Da a Cen e - h ps://
podaac.jpl.nasa.go /da ase lis ?sea ch=Pa h inde ) and RSMAS (Rosens iel School o Ma ine
and A mosphe ic Science,—Uni e si y o Miami)
Clima ological indices. In o de o ime co ela e he oscilla ions ound in he ishe ies
ime se ies wi h clima ological e en s possibly a ec ing he s udy egion, we used ime se ies o
some known clima ic indices. Owing o known linkages o clima ic e en s such as he El Niño-
Sou he n Oscilla ion (ENSO) and he a iabili y o he SST ields in he A lan ic Ocean [36–
40], we used he Mul i a ia e ENSO Index (MEI), he No h A lan ic Oscilla ion Index (NAO)
and he In e -Hemisphe ic SST G adien o he A lan ic (GITA). The ime se ies o MEI and
NAO indexes we e ob ained om www.es l.noaa.go /psd/da a/clima eindices/lis /. The GITA
index was calcula ed by he di e ence be ween SST anomalies in he No h and he Sou h
A lan ic Ocean [41].
Me hods
CPUE (Ca ch pe Uni o E o ) es ima ion. In o de o measu e p oduc i i y, ca ch pe
uni o e o (CPUE) was es ima ed he e o each ishe y and species. CPUE is de ined as he
amoun o ishe ies esou ce caugh by an e o uni employed. The CPUE was es ima ed by
using ca ch in onnes di ided by he e o (numbe o ishe men x ishing days). The CPUE
es ima e was made by using he Jackkni e me hod, desc ibed as [42]:
CPUE ¼Pn
i¼1CiEi
Pn
i¼1E2
i
ð1Þ
whe e C
1
is he ca ch in a specific mon h and fishe y, and E
1
is he e o o he same mon h
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 4/29
and fishe y. The Jackkni e me hod was selec ed since i is ecommended o si ua ions in which
he e is a lack o knowledge on he beha iou o he choosen a iables, as is he case in he
majo i y o fishe ies s udies [43].
The CPUE, on he o he hand, will be conside ed as being ela ed no only o ca ching he
esou ce, bu also o he a ailabili y o he ishe y en i onmen , i.e., bo h i s ca chabili y (Q)
and i s abundance (A), as shown below:
CPUE  ðA;QÞ;
CPUE /Q!Q ðen i onmen Þð2Þ
Ou Amazonian ishe ies da a we e g ouped acco ding o he axonomic amily and he
mon hly alue o he CPUE was es ima ed o each ishe y si e (Óbidos, San a ém and Mon e
Aleg e) and ishe y en i onmen ( i e and loodplain lakes).
Ma ke Index. The e a e wo di e en ish ma ke s in ou s udy egion. Indus ial ish
p ocessing companies a e loca ed in Óbidos and San a ém while local consump ion ma ke s
a e mainly loca ed in San a ém and Mon e Aleg e. This ac con ibu es o he ishe ies
dynamics in he Lowe Amazon egion. In o de o imp o e ou u u e mul i a ia e s a is ical
analysis, we ook in o accoun he ish ma ke as well as he di e en ish si es and he en i on-
men al a iables. A ish ma ke index was p oduced he e in o de o accoun o he ishe ies
des ina ion, aiming o ake in o conside a ion he economical d i e s o he Lowe Amazon
ishe ies. The ma ke index is se o be 1 (one) when he mon hly ish p oduc ion was des ined
owa d he indus ial p ocessing companies and 0 (ze o) when i was des ined owa d he local
consump ion ma ke s. The es ima e o he ma ke index was made using he ollowing equa-
ions:
MKTR ¼PI ca ch= o al ishing ð3Þ
MKTLk ¼HY ca ch= o al ishing ð4Þ
whe e, MKT
R
is he ma ked index o he Ri e Amazon en i onmen ; MKT
Lk
is he ma ked
index o he lake en i onmen ; PI is he ca ch o Pimelodidae and HY is he ca ch o
Hypoph halmidae, he wo mo e ep esen a i e amilies in he wo s udied en i onmen s. Ma -
ke indexes we e compu ed o he wo di e en en i onmen s and also o he di e en fishe y
locals.
Collinea i y es s be ween he biological and en in onmen al a iables. In o de o
a oid possible dis o ions on ou in e ences as well as weak conclusions all ou biological and
en i onmen al da a we e subjec o a obus s a is ical me hod o es o he collinea i y
among all a iables s udied he e. The me hod is desc ibed in [44]. When some o ou a iables
a e highly co ela ed we can op on despise one o some o hem aiming o no epea ou in e -
p e a ions. Following [45], we used he e he Pea son co ela ion me hod and used dispe sion
diag ams o analize he collinea i y among ou da a.
The esul s om he Pea son co ela ion analysis a e seen in Table 1 and Fig 2. As expec ed,
he analysis indica es ha he looding pulse o he Amazon Ri e loodplains is e y co ela ed
wi h he i e 's discha ge (co ela ion coe icien , cc = 0.79). A he same ime, he su ace (soil)
empe a u e is co ela ed o he ai empe a u e (cc = 0.80) and wi h ENSO e en s (cc = 0.59).
The SST anomalies o he con inen al shel o Amapá, Amazon Ri e mou h and Pa á a e
highly co ela ed among hem (cc >0.90).
A e he collinea i y es s, he en i onmen al a iables used he e we e educed o he ol-
lowing: Discha ge Anomaly o he Amazon Ri e (ARD); Rain all (RF); Wa e Le el (WL);
zonal (u) and me idional ( ) componen s o he wind; Su ace Tempe a u e (TEMP); Ai
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 5/29

Table 1. Pea son’s co ela ion coe icien s. Pea son’s co ela ion coe icien s be ween en i onmen al a iables. (p <0.05).
ARD WL RF u TMPs c TMIN2M SPFH2M SWSoilM PEVPR RUNOF LHF SSTA_AP SSTA_AZ SSTA_PA MEI GITA NAO
ARD 1.00
WL 0.63 1.00
RF 0.24 0.20 1.00
u 0.02 -0.12 0.36 1.00
-0.11 0.16 0.12 0.27 1.00
TMPs c -0.35 -0.26 -0.50 -0.40 -0.02 1.00
TMIN2M -0.44 -0.23 -0.34 -0.27 0.03 0.76 1.00
SPFH2M -0.45 -0.37 -0.12 0.31 0.21 0.07 0.43 1.00
SWSoilM 0.17 0.21 0.41 0.49 0.09 -0.54 -0.18 0.25 1.00
PEVPR -0.04 -0.03 -0.39 -0.61 -0.12 0.69 0.30 -0.50 -0.76 1.00
RUNOF 0.15 0.31 0.28 0.36 0.25 -0.23 0.06 0.14 0.63 -0.42 1.00
LHF -0.04 -0.29 -0.11 -0.01 -0.27 -0.28 -0.22 0.28 -0.05 -0.18 -0.22 1.00
SSTA_AP -0.25 -0.02 -0.05 0.00 0.39 0.32 0.35 0.29 -0.26 0.16 -0.08 -0.08 1.00
SSTA_AZ -0.35 -0.02 -0.15 -0.03 0.35 0.35 0.40 0.33 -0.24 0.18 -0.08 -0.06 0.89 1.00
SSTA_PA -0.34 0.05 -0.07 0.00 0.42 0.30 0.39 0.32 -0.16 0.12 0.00 -0.14 0.82 0.93 1.00
MEI -0.20 -0.45 -0.38 -0.34 -0.26 0.59 0.42 0.16 -0.49 0.45 -0.45 0.20 -0.05 -0.08 -0.12 1.00
GITA -0.28 -0.13 -0.20 -0.06 0.14 0.13 0.05 0.02 -0.19 0.16 -0.19 -0.03 0.20 0.24 0.12 -0.03 1.00
NAO 0.06 0.10 0.03 0.01 -0.03 -0.19 -0.07 0.08 0.17 -0.16 0.14 0.18 -0.06 -0.01 -0.04 -0.06 -0.22 1.00
(ARD) Amazon Ri e Discha ge, (WL) Wa e Le el, (RF) Rain all, (u) Zonal Wind Componen , ( ) Me idional Wind Componen , (TMPs c) Su ace Tempe a u e, (TMIN2m) Ai
Tempe a u e, (SPFH2m) Specific Humidi y a 2 m heigh , (SWSoilM) Wa e Con en o he Soil, (PEVPR) Po en ial E apo a ion, (RUNOF) Runo , (LHF) La en Hea Flux, (SSTA)
Sea Su ace Tempe a u e, (MEI) Mul i a ia e ENSO Index, (GITA) A lan ic In e -Hemisphe ic Sea Su ace Tempe a u e G adien , (NAO) No h A lan ic Oscilla ion, (AP) Con inen al
Shel o Amapá, (AZ) Con inen al Shel o he Amazon, (PA) Con inen al Shel o Pa á.
doi:10.1371/jou nal.pone.0157050. 001
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 6/29
Humidi y (SPFH); Runo (RUNOF); La en Hea Flux (LHF); sea Su ace Tempe a u e
(SSTA); Clima ic indexes MEI, GITA and NAO.
Mul i a ia e s a is ical analysis
Many dis inc ma hema ical and s a is ical models ha e been applied in o ishe ies da a.
Among hem, he mul i a ia e eg ession analysis like he Au o eg essi e In eg a ed Mo ing
A e age (ARIMA) and he Gene al Linea model (GLM) a e highly ecommended [46–53].
Some au ho s also employ e iciency models ela ing ish p oduc ion wi h some en i onmen al
a iables [54–56]. The Redundancy Analysis (RDA) is also a model la gely employed in eco-
logical s udies o analyse da a ime se ies. This me hod when applyed o ishe ies s udies empi -
ically assums ha he se e al en i onmen al a iables egula e he ishe y esou ces' dinamics
as much as he ishe y e o do [45]. This kind o analysis assumes a linea beha io o he
a iables s udied allowing ha he unkown a iables i in o a linea eg ession model.
Fo all he a iables analysed he e, es s o no mali y we e conduc ed and he da a homoce-
das ici y was analysed using he Shapi o-Wilk and Ba le es s, espec i ely, accep ed o he
signi ican le el o p <0.05. The Analysis o Va iance (ANOVA) es was applied aiming o
es he a iance in he mon hly a e age CPUE acco ding o he axonomic amily o he mos
abundan ish species in he Lowe Amazon egion. Fo he ANOVA, he ac o s es ablished
we e he axonomic amilies, he ishe ies egion, he mon hs and he yea s o he ishe ies.
O dina ion was made o he h ee ishing g ounds s udies he e (Óbidos, San a ém and
Mon e Aleg e) as well as o hei espec i e ishe y en i onmen s ( i e and loodplain lakes)
using he De ended Co espondence Analysis (DCA) o he mon hly a e aged CPUE [57].
The CPUE alues analysed he e we e loga i hmically ans o med be o e p oceeding wi h he
analysis [58]. DCA is a s a is ical ool mainly used o explo e he da a and show ini ial ela ion-
ships in one sou ce o da a, al hough i can also be used o choose be ween linea o unimodal
o dina ion me hods [59]. This analysis made possible o g aphically isualize he a ia ion in
he associa ions be ween ou a iables.
The ela ionships be ween he mon hly a e aged CPUE ela ed o he axonomic amily and
he en i onmen al a iables we e analyzed using he RDA and he mul iple eg ession. RDA
Fig 2. Dispe sion diag am and co ela ions among he en i onmen al a iables. (ARD) Amazon Ri e
Discha ge, (WL) Wa e Le el, (RF) Rain all, (u) Zonal Wind Componen , ( ) Me idional Wind Componen ,
(TMPs c) Su ace Tempe a u e, (TMIN2m) Ai Tempe a u e, (SPFH2m) Speci ic Humidi y a 2 m heigh ,
(SWSoilM) Wa e Con en o he Soil, (PEVPR) Po en ial E apo a ion, (RUNOF) Runo , (LHF) La en Hea
Flux, (SSTA) Sea Su ace Tempe a u e, (MEI) Mul i a ia e ENSO Index, (GITA) A lan ic In e -Hemisphe ic
Sea Su ace Tempe a u e G adien , (NAO) No h A lan ic Oscilla ion, (AP) Con inen al Shel o Amapá, (AZ)
Con inen al Shel o he Amazon, (PA) Con inen al Shel o Pa á.
doi:10.1371/jou nal.pone.0157050.g002
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 7/29
was also employed using a ma ix o explana o y a iables (en i onmen al a iables) o quan-
i y he a ia ion in a ma ix o esponse a iables (CPUE), assuming linea ela ionships
be ween all a iables [60]. RDA is a ool ha has been ex ensi ely used o analyze ecological
ela ionships, e.g. be ween abundance da a and en i onmen a iables. En i onmen al da a a e
used o ex ac pa e ns om he explained a ia ion only. RDA was he linea g adien analysis
me hod. The ocus scaling was on in e -species co ela ions and species sco e was di ided by
s anda d de ia ion. We also applied a ou h oo ans o ma ion in o ou species da a which
we e p e iously no malized and s anda dized. The o wa d selec ion o en i onmen a iables
was made by manual selec ion wi h he bes K o 24 a iables and using Mon e Ca lo pe mu a-
ion es s wi h 9999 un es ic pe mu a ions. The da a se was hen andomized and each a i-
able was analyzed on i s own.
The mul iple eg ession me hod used he e was he Backwa d S epwise Me hod applied o a
con idence le el o 2 (F Fishe -Snedeco alue). The dependen a iables we e he CPUE while
he independen a iables we e he en i onmen al a iables and he ma ke index. The ishe ies
da a we e ans o med h ough he ou h oo ans o ma ion. All eg essions signi ican o
p<0.05 we e conside ed he e o u u e analysis. All he s a is ical analysis om he ANOVA
and he mul iple eg ession es s we e made using he STATISTICA7.0
1
so wa e esul ing in
se e al s a is ical models which ela e CPUE wi h he en i onmen al a iables and he ma ke
index. When pe o ming he DCA we used he PCORD so wa e un a he Na u al Sciences
Museum in Mad id, Spain. The RDA was un using he Canoco p og am o Windows 4.54 [60].
Resul s
Fishing in he Lowe Amazon and speci ic composi ion
Fishe ies p oduc ion. Fo he pe iod 1993–2004, he es ima ed o al ishe ies p oduc ion
in he Lowe Amazon egion was 17,482 , wi h a mon hly mean o 122 (s d = 49 ). Augus
and Sep embe o 1994, 1995, 2001 and 2002 we e he mon hs wi h he highes ca ches. These
mon hs we e pa o in e annual pe iods o ebb-d ough in he Amazon Ri e Basin. Decembe
2002 and 2003, Janua y and Feb ua y 2000 and 2004 we e he mon hs wi h he lowes ca ches
in he s udy egion. These pe iods coincide wi h he we pe iod o he s udy egion. The mos
caugh species (81.4% o o al) we e Hypoph halmus ma gina us and H.eden a us (26.9%),
B achypla ys oma ousseauxii (11.6%), P ochilodus nig icans (8.6%), Plagioscion sp. and Pachy-
pops sp. (5.4%), Pseudopla ys oma ascia um and P. ig inum (5.3%), Liposa cus pa dalis
(5.0%), Semap ochiloduns aeniu us and S.insignis (4.5%), Pimelodina la ipinnis (3.8%), Schi-
zodon ascia um and Lepo inus i ascia us (3.4%) and B achypla ys oma aillan i (3.2%). Each
ishing ip p esen ed a mean ishing e o o 6 ishe men (s d = 2 ishe men) and 4 ishing
days (s d = 1 day).
As expec ed, ou esul s show ha he ishe ies p oduc ion in he lo ic en i onmen o he
Lowe Amazon Ri e was cyclic in na u e. The annual peak p oduc ion happened in he pe iod
om Augus o Oc obe (d ough - lood season), wi h less exp essi e alues om Decembe o
Feb ua y (we season). The yea s 1995, 1999, 2001 and 2002 s ood ou o ha ing highe
ca ches, while he yea s 1997, 2000 and 2003 p esen ed he lowe ca ch alues (Fig 3). Ou o all
he species caugh in he lo ic en i onmen , he mos exp essi e ones du ing he s udied pe iod
we e: B achypla ys oma ousseauxii (28.0%), P ochilodus nig icans (11.1%), Semap ochiloduns
aeniu us and S.insignis (8.7%), B achypla ys oma aillan i (7.6%), B achypla ys oma ilamen-
osum (7.0%), Pseudopla ys oma ascia um and P. ig inum (5.6%), Hypoph halmus ma gina us
and H.eden a us (5.5%), Mylossoma du i en e,Myleus schombu gki and Me ynnis a gen eus
(4.2%) and Liposa cus pa dalis (3.8%). These species accoun ed o 81.4% o he ca ches in he
analyzed pe iod, accoun ing o a o al o 4,700 wi h a mon hly mean o 33 (s d = 28 ).
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 8/29
In he len ic en i onmen associa ed o he Amazon Ri e , a ising end was no ed in o al
ish p oduc ion, con a y o wha commonly occu s in i e s. The yea s om 2001 o 2003 had
he highes ish p oduc ion, while he lowes p oduc ions we e eco ded in 1993 and om 1997
o 1999 (Fig 4). The we pe iod be ween Feb ua y and Ma ch p esen ed he highes alues
while he lowes alues we e ela ed o he Amazonian d ough - lood pe iod, om Oc obe o
Decembe . The a ge species mos caugh in loodplain lakes du ing he s udy pe iod we e
Hypoph halmus ma gina us and H.eden a us (50.1%), Plagioscion spp. and Pachypops spp.
(7.3%), Pimelodina la ipinnis (7.1%), Liposa cus pa dalis (6.1%) and P ochilodus nig icans
(4.7%), Colossoma mac opomum (3.5%) and Pseudopla ys oma ascia um and P. ig inum
(3.2%). These species accoun ed o 82.2% o he o al p oduc ion o 12,782 in he s udy
pe iod. The ish p oduc ion mon hly mean was 89 (s d = 43 ).
When we g oup he species caugh in o hei axonomic amilies, he p esence o 20 amilies
o i e o de s a e no ed. The mos impo an amilies a e he Hypoph halmidae, Pimelodidae,
Sciaenidae, P ochilodon idae, Lo ica iidae, Anos omidae, Cichlidae, Clupeidae and Do adidae.
The e olu ion o he CPUE by axonomic amily caugh in he Lowe Amazon indica es an
in e annual a ia ion and speci ici ies ha a y acco ding o he ishe y en i onmen . The am-
ilies Pimelodidae a e mos ly caugh in he i e (Fig 5A) while Hypoph halmidae a e mos ly
caugh in loodplain lakes (Fig 5B). These wo axonomic g oups accoun o a highe CPUE
obse ed in 1996 and 1999.
Du ing he pe iod o his s udy, he ca ch and CPUE a ied acco ding o he en i onmen
and he ishing a ea no always being di ec ly p opo ional (Table 2). To illus a e his, in he
i e en i onmen o San a ém, he mos caugh amily was Pimelodidae wi h a mon hly a e -
age o 12.16 , while he amily wi h he highes CPUE was Hypoph halmidae, wi h, 10.44
kg ishe man
-1
day
-1
and a ca ch mean o only 787 kg pe mon h. In he case o loodplain
Fig 3. Mon hly ishe y p oduc ion by species in he Amazon Ri e . Mon hly ishe y p oduc ion by species
in he Amazon Ri e nea he ishe y g ounds o Óbidos, San a ém and Mon e Aleg e, om Janua y 1993 o
Decembe 2004. (BRV) B achypla ys oma aillan i, (BRA) B achypla ys oma ousseauxii, (SEM)
Semap ochiloduns aeniu us and S.insignis, (BFI) B achypla ys oma ilamen osum, (HYP) Hypoph halmus
ma gina us and H.eden a us, (MYL) Mylossoma du i en e,Myleus schombu gki and Me ynnis a gen eus,
(LIP) Liposa cus pa dalis, (PRO) P ochilodus nig icans, (PSE) Pseudopla ys oma ascia um and P. ig inum.
doi:10.1371/jou nal.pone.0157050.g003
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
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Fig 9. RDA o he CPUE in ela ion o he en i onmen al a iables. G aphic illus a ion o he RDA
analysis o he mon hly a e age CPUE in he i e (a) and loodplain lakes (b) o he Lowe Amazon egion o
all axonomic amilies wi h espec o he en i onmen al a iables. Black a ows a e ela ed o he axonomic
amilies while he ed a ows ep esen he se e al en i onmen al a iables conside ed he e. (HY)
Hypoph halmidae, (PI) Pimelodidae, (SC) Sciaenidae, (PC) P ochilodon idae, (LR) Lo ica iidae, (SR)
Se asalmidae, (AN) Anos omidae, (CI) Cichlidae, (CL) Clupeidae, (DR) Do adidae, (ARD) he Amazon Ri e
discha ge, (WL) he Amazon Ri e le el, (u, ) zonal and me idional componen s o he wind, (TEMP) su ace
empe a u e, (SPFH) speci ic humidi y o he ai , (RUNOF) su ace uno , (LHF) la en hea lux, (GITA) In e -
Hemisphe ic SST G adien o he A lan ic, (NAO) No h A lan ic Oscilla ion Index, (MEI) Mul i a ia e Clima ic
Index o ENSO e en s.
doi:10.1371/jou nal.pone.0157050.g009
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 16 / 29

Table 4. Mul iple eg ession model. Bes signi ican esul s o he CPUE o each axnomic amily, ishing g ound and ishing en i onmen om mul iple
eg ession. Signi ican alues p <0.05 and 2 deg ees o eedom.
RIVER
R
2
pεs d o
Es ima e
In e cep ion Model Equa ion
OBIDOS SR 0.2669 0.00000 2.11580 2.0878 SR = 2.0878 + 0.275*MEI—0.41*MKT
HY 0.2654 0.00000 2.50530 2.4609 HY = 2.4609 + 0.361*ARD + 0.195*SSTA + 0.287*RUNOF—0.38*MKT
PI 0.2348 0.00001 1.97816 2.9799 PI = 2.9799–0.25*WL + 0.207*RF—0.20* + 0.261*MKT
PC 0.1807 0.00144 4.92976 4.5017 PC = 4.5017–0.22*MKT
SC 0.2307 0.00016 1.40274 1.1752 SC = 1.1752–0.26*ARD + 0.284*WL + 0.369*u + 0.256*MEI—0.33*MKT
DR 0.1092 0.01761 0.51768 0.3036 DR = 0.3036–0.26*TEMP + 0.306*MEI -0.20*MKT
CL 0.2493 0.00001 1.22029 1.1025 CL = 1.1025 + 0.169*SSTA—0.36*MEI—0.27*RUNOF—0.25*MKT
SANTAREM AN 0.1313 0.00147 1.12772 1.1578 AN = 1.1578–0.23*TEMP—0.20SPFH + 0.267*SSTA
HY 0.1291 0.00067 5.13092 6.1742 HY = 6.1742–0.29*MKT
LR 0.1605 0.00047 2.03290 2.6633 LR = 2.6633 + 0.265*TEMP + 0.190*SPFH—0.37*MEI—0.25*MKT
PI 0.6481 0.00000 1.07017 0.3926 PI = 0.3926 + 0.161*ARD—0.26*WL—0.18*RF -0.13*SPFH + 0.223*SSTA
—0.25*MEI + 0.706*MKT
PC 0.0897 0.04213 2.43577 2.8433 PC = 2.8433–0.21*MKT
SC 0.1147 0.01825 0.67738 1.1215 SC = 1.1215–0.28*WL—0.19*MKT
MONTE
ALEGRE
AN 0.2895 0.00000 1.21969 0.2493 AN = 0.2493–0.23*u—0.43*LHF
SR 0.1018 0.10478 1.15839 1.2407 SR = 1.2407–0.29*WL—0.19*LHF
CI 0.2027 0.00002 0.60253 0.6249 CI = 0.6249–0.37*ARD + 0.233*WL—0.21*MKT
HY 0.1961 0.00003 3.17750 3.5757 HY = 3.5757–0.21*SSTA + 0.210*GITA—0.27*MKT
LR 0.1383 0.00090 1.95819 1.9148 LR = 1.9148 + 0.214*MEI—0.22*MKT
PI 0.5920 0.00000 1.19065 0.8520 PI = 0.8520–0.29*WL—0.22*u—0.21*TEMP—0.26*LHF—0.15*RUNOF
+ 0.753*MKT
PC 0.0935 0.03399 1.68062 1.5994 PC = 1.5995–0.29*WL—0.23*TEMP
SC 0.1313 0.00332 0.86496 0.8101 SC = 0.8101–0.25*TEMP + 0.355*SPFH—0.25*LHF
DR 0.1408 0.00731 1.59834 0.4593 DR = 0.4593 + 0.259*MEI
CL 0.0738 0.02968 1.02307 0.2611 CL = 0.2611–0.18*LHF
R
2
pεs d o
Es ima e
In e cep ion Model Equa ion
OBIDOS AN 0.1801 0.0002 1.1836 0.5663 AN = 0.5663–0.41*u—0.27*TEMP + 0.267*SSTA
SR 0.1402 0.1058 1.5357 1.7031 SR = 1.7031–0.27*WL + 0.202*RF—0.23*u—0.28*MEI
CI 0.0963 0.0202 1.3893 0.5563 CI = 0.5563 + 0.293*WL + 0.196*LHF
HY 0.1787 0.0002 3.4437 3.5962 HY = 3.5962 + 0.256*ARD + 0.215*RF + 0.414*TEMP
LR 0.2713 0.0000 1.7490 0.2788 LR = 0.2788–0.55*ARD + 0.518*WL—0.29*TEMP -0.32*SPFH + 0.310*MEI
—0.25*GITA
PC 0.1253 0.0133 2.5474 1.0287 PC = 1.0287 + 0.271*ARD—0.33*WL—0.29*u—0.42*TEMP
SC 0.1467 0.0037 0.9441 1.3580 SC = 1.3580 + 0.277*ARD + 0.380*TEMP + 0.228*LHF
DR 0.1764 0.0046 0.8924 0.4870 DR = 0.4870–0.31*ARD + 0.365*WL—0.21*u
SANTAREM AN 0.1678 0.0003 0.7664 1.1736 AN = 1.1736–0.23* + 0.237*SSTA—0.20*GITA + 0.197*MKT
SR 0.1573 0.0027 0.5457 1.0539 SR = 1.0539 + 0.244*ARD—0.28*WL + 0.234*TEMP + 0.286*RUNOF
CI 0.2106 0.0000 0.3291 0.7476 CI = 0.7476–0.35*WL—0.19*
HY 0.1457 0.0027 2.5188 2.8879 HY = 2.8879–0.26*WL + 0.188*MKT
PI 0.0824 0.0171 0.7994 1.6174 PI = 1.6174–0.22*ARD—0.17* —0.23*MEI
SC 0.1891 0.0003 0.5361 1.1842 SC = 1.1842–0.19* —0.24*GITA
DR 0.1639 0.0018 0.6842 0.3724 DR = 0.3724 + 0.210*TEMP
MONTE
ALEGRE
AN 0.1546 0.0069 0.9814 0.8905 AN = 0.8905 + 0.192*ARD—0.24*u
(Con inued)
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 17 / 29
We migh expec ha he e ec s o he looding pulse should be s onge du ing he we sea-
son, bu [53] obse ed ha he e ec s o he d y season on he mul ispecies ishe ies in he
Amazon a e equally impo an . The au ho s indica ed ha he ishe ies dynamics in he i e
and loodplains a eas o he Amazon is no simply dependen on he inunda ion pulse.
In he Amazon a he s a o he looding, he le el o he i e is p ac ically s able. The
aqua ic en i onmen s on he loodplain p edomina e whe e a subs an ial pa o he ich hyo-
auna is dispe sed in sea ch o ood [10,19,33–34,66–70]. Du ing his pe iod, ishing is mo e
di icul and he ca chabili y o a ge species is educed because o he conside able dispe sion
o he indi iduals, a ising om he inc ease o habi a s and hidden a eas. Du ing ebb, ish
begin o g oup oge he due o he con ac ion o he aqua ic en i onmen [2,9]. In his pe iod,
ca ching is in ense in he loodplain lakes and i e s. Bo h he loodplains and he o es a e
used by species o he amilies Pimelodidae and Sciaenidae since such ishes p eda e on o he
species ha a e lea ing hese a eas du ing his pe iod [7]. Du ing he d y season, ish a e o ced
o mo e o a eas whe e wa e is abundan in he i e channels [71]. Howe e , no all Amazo-
nian ishing boa s a e able o ope a e in his en i onmen . Du ing his pe iod, he e is a con-
cen a ion o Pimelodidae ca ches in he i e . A he end o he d y season, ishe ies
p oduc ion o Se asalmidae (genus Colossoma) and P ochilodon idae (genus P ochilodus) a e
in ensi ied. A we season, ca ch is concen a ed in o a ge amilies o lake-li ing species ha
ha e a li e cycle mainly associa ed o he loodplain lakes o lake sys ems [72] such as Pimelodi-
dae (genuses Pimelodina and Pseudopla ys oma), Sciaenidae (genus Plagioscion), Lo ica iidae
(genus Liposa cus).
The complexi y o he dynamical p ocesses associa ed o he mul ispecies ishe ies oge he
wi h he lack o ishe ies p oduc ion da a se ies inc ease ou di icul y on e alua ing he impac
o ishing on he na u al s ocks o he Amazon [73–74]. In mul ispecies ishe y, ca ch le els
end o inc ease wi h he inc ease o he ishing e o , un il a s abilizing poin whe e one can-
no inc ease he p oduc ion wi h an inc ease in e o [75]. I is also known ha , con a y o
wha is obse ed in ishe ies wi h a single a ge species which shows a linea d op p opo ional
o he CPUE wi h an inc eased e o , he mul ispecies ishe ies CPUE beha es in a non-linea
manne [76]. The same occu ed in ou esul s: al hough he annual a e age o ishing e o
(numbe o ishe men imes ishing days) was kep p ac ically s able o was educed in he
pe iod om 1993 o 2003 in San a ém, he CPUE inc eased p obably due o o he ac o s.
These ac o s may be ela ed o echnological ad ancemen s in he ishing lee , such as he
inc ease in he a e age size and engine powe o he boa s and/o a be e ice s o age capaci y
Table 4. (Con inued)
SR 0.1317 0.0125 1.3418 1.2193 SR = 1.2193 + 0.209*RUNOF
HY 0.0936 0.0081 3.8455 3.7127 HY = 3.7127 + 0.272*ARD + 0.170*LHF
LR 0.1436 0.0006 1.5032 2.7674 LR = 2.7673 + 0.268*MEI + 0.178*GITA
PI 0.1280 0.0155 1.4128 1.2851 PI = 1.2851–0.41*TEMP—0.22*SPFH—0.22*LHF + 0.234*SSTA
+ 0.281*MEI—0.18*GITA
DR 0.1777 0.0001 0.7176 0.5794 DR = 0.5794–0.22*WL + 0.331*SPFH—0.22*LHF
(AN) Anos omidae, (CI) Cichlidae, (CL) Clupeidae, (DR) Do adidae, (HY) Hypoph halmidae, (LR) Lo ica iidae, (PC) P ochilodon idae, (PI) Pimelodidae,
(SC) Sciaenidae, (SR) Se asalmidae, (ARD) he Amazon Ri e discha ge, (WL) he Amazon Ri e le el, (u, ) zonal and me idional componen s o he
wind, (TEMP) su ace empe a u e, (SPFH) specific humidi y o he ai , (RUNOF) su ace uno , (LHF) la en hea flux, (GITA) In e -Hemisphe ic SST
G adien o he A lan ic, (NAO) No h A lan ic Oscilla ion Index, (MEI) Mul i a ia e Clima ic Index o ENSO e en s, (MKT) ma ke index.
(R
2
) eg ession coe ficien , (p) confidence le el, (ε) s anda d e o o he es ima i e.
doi:10.1371/jou nal.pone.0157050. 004
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 18 / 29
o ish ca ch p ese a ion [71]. These ac o s inc ease he ishing powe and a e no accoun ed
o in his pape .
Some species o he amilies Se asalmidae, Pimelodidae and Scianidae a e known o ha e
being caugh in he Lowe Amazon egion in sizes below he a e age leng h o he i s sexual
ma u a ion—L
50
[76–78], a p ac ice agains he cu en B azilian law ha may comp omise
he main enance o hese ish s ocks in he egion. A subs an ial h ea o he sus ainabili y o
he ishe ies esou ces in he egion is he excessi e concen a ion o ishing e o on jus some
ew a ge species [76]. In his ega d, e o s o di e si y he composi ion o he species caugh
may educe he p essu e on he species al eady highly exploi ed. Meanwhile, despi e hese con-
side a ions, he esul s o ou analyses indica e ha he ishe ies esou ces in he Lowe Ama-
zon appea o be mode a ely exploi ed, ha is, below he maximum expec ed yield [76].
The ishing ac i i y pe o med in i e s is mo e complex ha he one pe o med in lakes in
he Amazon. The Pimelodidae p oduc ion, o ins ance, is p ac ically en i ely di ec ed o he
indus y o p ocessing and is conside ed he mos p o essional ishing ac i i y o he Lowe
Amazon egion. As a consequence, he Pimelodidae ishing is mo e in luenced by he ma ke
han by he en i onmen al ac o s. The mul iple eg ession models used he e a e consis en
wi h his eali y showing ha he e is an inc ease o he Pimelodidae p oduc ion associa ed
wi h he ma ke index inc ease. The opposi e happens wi h he o he ishing amilies ha
a end he local ma ke : when he ma ke index inc eases hei p oduc ion dec eases.
Al hough local ishing in lakes nea Óbidos is mo e oppo unis and di e se, he local ish-
ing ma ke o Ódibos is e y small in compa ison o San a ém and Mon e Aleg e. The ishing
p oduc ion o lake en i onmen s in Óbidos e Mon e Aleg e do no depend on he o e all ma -
ke (indus y ela ed) o being ypically di ec ed o local consump ion. Ou esul s showed
ha he ma ke index was only impo an o he Hypoph halmidae and Anos omidae amilies.
The co ela ions we e low wi h he excep ion o he ishing o Pimelodidae in i e en i on-
men s. We conclude ha he mo e a isanal he ishe ies a e, he highe a e he e o s associ-
a ed o ou s a is ics o co ela e ishing p oduc i i y wi h he en i onmen al a iables.
The ela i e impo ance o he ish p ocessing indus ies in Óbidos and San a ém, as well as
he ish s ocks composi ion in hose si es we e p e iously s udied by [49]. The au ho s used
bo h P incipal Componen s Analysis and a Gene al Linea Model and conclude ha he ishe -
ies in hose wo si es is highly condi ioned o he ca ches o ca ish (Pimemolidae and
Hypoph halmidae). Mo eo e , he ishe ies o hose axonomic amilies o eed he indus y
con ibu e o he o e all ishe ies a iabili y especially in he i e en i onmen . These esul s
a e in ag eemen wi h ou indings when we add he (economic a iable) ma ke index in ou
analysis.
The ishe ies in he Lowe Amazon egion can be di ided in o wo dis inc ishe y ca ego-
ies: (1) pe manen ishe ies in he i e en i onmen ha occu s along he en i e yea and (2)
cyclic ishe ies di ec ed owa ds he lake en i onmen ha is no accessible o he ishing lee
du ing he d y season [61]. Fishing in loodplain lakes, as opposed o ishing in he i e ,
in ol es a low deg ee o specializa ion and occu s h oughou he yea [71]. The species caugh
in he i e a e ex emely ulne able, wi h a high isk o o e exploi a ion since ishing is mo e
specialized and ishe ies p oduc ion a ge s a small numbe o amilies and a ge species. In
addi ion o his, since he main ishing explo a ion a ea is he i e a he han he lakes, i e
species a e no bene i ed by ishe y ag eemen s held by he coas al communi ies o p o ec
loodplain lakes and looded a eas [79]. Fu he mo e, ish species ha mo e be ween looded
a eas and i e s depending on he hyd ological cycle phase ha e a g ea e plas ici y and a e less
ulne able o he isk o o e exploi a ion [71]. These species end o be be e p o ec ed unde
communi y ishe y ag eemen s. Thus, new ishing managemen policies should conside hese
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 19 / 29
wo ca ego ies in o de o p omo e di e en ia ed solu ions o he o dinance and sus ainabili y
o he ishing ac i i y in he Amazon.
Howe e , i is e iden ha only ishe ies egula ion policies a e no su icien o ob ain be e
yields in he ac i i y. Al e a ions in he Amazonian landscape, especially close o he i e
banks and loodplains, ha e impac s on he clima ic cha ac e is ics o he egion a ec ing he
hyd ological cycle. In his ega d, de o es a ion causes di ec and di ec ha m o he ish popu-
la ions due o he educ ion in he amoun and di e si y o ood a ailable and due o he al e -
a ion o he hyd ological cycle. Scien i ic esea ch demons a es ha an inc ease in o es
biomass leads o an inc ease in ish biomass, wi h some species inc easing hei p edominance
in he ish communi ies [80–84]. So, o example, he subs i u ion o o es o g azing land
should cause changes in ish ea ing habi s due o he educ ion in he supply o ui s, seeds and
o he o ms o o ganic ma e o igina ing in he o es . The impac o de o es a ion on he s a-
bili y o he aqua ic ecosys em is g ea e han ha o ishing, e en on ich hyo auna species ha
do no depend di ec ly on he o es , such as hose in he amily Pimelodidae [85]. The ex en
o deg ada ion and modi ica ion o he plain landscape should wo sen wi h he ci ies g ow h
and he economic de elopmen in he Amazon. This can become a conside able h ea o he
Amazonian en i onmen in he long e m, comp omising he aqua ic and ish ecosys ems in
he egion [86–88].
Fishe ies in he Lowe Amazon a e cha ac e ized o co e la ge a eas o lo ic en i onmen s,
such as he Lago G ande o Mon e Aleg e, he G ande de Cu uaí Lake and he Pa ú Lake (Fig
1). The kinema ics o he low and he dynamics o he looding pulse play impo an oles in
he li e cycle o he ich hyo auna in he Lowe Amazon, egula ing he a ailabili y o ood and
shel e , in luencing he ep oduc ion, ood and g ow h o many ish species [69,81–82,89].
Cons an , inc easing modi ica ions o he landscape, change in he i e low due o he con-
s uc ion o ba ie s and o he al e a ions in he aqua ic habi a a e poin ed ou as conside able
h ea s, in he long e m, o he ich hyo auna and o he ishe ies ac i i y in he Lowe Amazon
egion [41,81–83]. In addi ion o he impac s o he landscape and hyd ological al e a ions in
he en i onmen , [53] desc ibe ha side e ec s on he ish popula ions include he in ensi ica-
ion o na u al dea h p ocesses caused by he diminu ion o he body g ow h and he o e all
ec ui men p ocess.
The di e si ica ion o he ac o s esponsible o he clima e egula ion in he Amazon d o e
his esea ch o make use o he highes numbe o possible a iables in o de o unde s and
he clima e dynamics o ou s udy egion as well as he e ec s o hose on he aqua ic sys em
and ishe ies a iabili y. The sola ene gy a ailabili y d i ing he local ene gy balance is known
as an impo an ac o egula ing he clima e o he Amazonian egion [90]. The ene gy ha
a i es a he Ea h's su ace is deli e ed back o he a mosphe e in he o m o sensible and
la en hea lux. While he i s is esponsible o he hea ing, he second one is ela ed o he
e apo anspi a ion p ocess. Ano he impo an a iable o all opical egions o he plane is
he p ecipi a ion o ain all. This a iable d i es he a iabili y o o he me eo ological a i-
ables such as he empe a u e and he ela i e humidi y, being e y he e ogeneous in he Ama-
zon [90].
Pas s udies es ima e ha abou 50% o he wa e apo condensed and p ecipi a ed by he
ain all in he Amazon is locally ecycled h ough he e apo anspi a ion p ocess while he
o he 50% is d i en in o he egion om he A lan ic Ocean [90–92]. The in e annual a iabil-
i y o he ain all and he i e s discha ge a e ela ed o clima ic e en s such as he ENSO. Du -
ing he El Niño (posi i e ENOS phase), he ain all in he Amazon dec eases leading
some imes o se e al d ough s. Du ing hese pe iods he posi ion o he In e opical con e -
gence Zone (ITCZ) in he A lan ic Ocean leads o a weakening o he T ade Winds blowing
owa ds he con inen [93–96].
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 20 / 29
As desc ibed be o e, he hyd ological cycle in he Lowe Amazon is e y much de e mined
by he clima e, and ice e sa [97]. This cycle includes ene gy exchanges, anspo o wa e
apo , ain all, d ainage, in il a ion and di e se wa e s o age mechanisms. All hese p ocesses
depend on he clima e and a e de e minan o he main cha ac e is ics o ecosys ems which, in
u n, a ec he dynamics o he ich hyo auna. Clima ic a iabili y and he dynamics o he
hyd ological cycle in he Lowe Amazon, as well as he cha ac e is ics o he landscape and he
amoun o aqua ic en i onmen s and ood a ailable a ec he dis ibu ion and ecology o he
ishe ies esou ces and, hus, he beha io o he ishe man and he ish. Howe e , his beha io
is also a ec ed by local cul u e and he g ow h o he mac o economy. These a e dynamic
aspec s, which p esen ma ked empo al a ia ions. [98–99] desc ibe ha one mus conside
he empo al and spa ial associa ions o all he a iables in o de o be e de e mine he ela-
ionships be ween he en i onmen al a iables and he ishe ies. In he case o his pape , di id-
ing ou s udy egion in he Lowe Amazon in o h ee di e en si es (Óbidos, San a ém and
Mon e Aleg e) ied o espec he conside a ions abo e men ioned.
Fluc ua ions in ain all in he Amazon a e pa ially associa ed wi h ENOS e en s. Du ing El
Niño yea s he e is a endency o p oduce d ough o accen ua ed ebb while in La Niña yea s
a e associa ed o in ense looding [37,75,96,100–102]. The du a ion and in ensi y o each
pe iod in he hyd ological cycle a e de e mining ac o s o he ich hyo auna o hey use he
loodplains o achie ing success o ec ui men and consequen species su i al [103]. [76,89,
104] desc ibe ha he composi ion o ish communi ies in he Amazon loodplain each yea is
ela ed o he du a ion and in ensi y o he hyd ological cycle in p e ious yea s, sugges ing an
in e annual dependence be ween ecological and en i onmen al a iables. The success o ailu e
o a ep oduc i e s a egy (seasonal, balanced o oppo unis ) and he su i al o young indi-
iduals in he popula ion o ish in he ebb depends on he adap a ion capaci y o each species
o adap o he seasonal luc ua ions o en i onmen al a iables [61,105].
The clima ic a iabili y o he Lowe Amazon egion has a di ec e ec on ish ca ch and
consequen p oduc i i y as i allows o supp esses he ishe man's access o ideal ishing loca-
ions o a ge he di e en ish species. The esul s o all analysis made in his pape indica es
ha he i e -a mosphe e-ocean sys em e ec s he mul ispecies ishe ies in a di e en way o
each s udied egion o he Lowe Amazon, as well o each ish axonomic amily and o each
a ge species. [106] desc ibe ha he empe a u e ac s on he ish g ow h; he winds, humidi y,
ege a ion co e age and he ENSO e en s p omo e o supp esses he a ailabili y o ood, while
he hyd og aphic ca chmen , yield in he Amazon Ri e and he su ace uno d i e he ex en
o he looded a ea. So, due o he ecological and beha io al complexi y o he Amazonian ish
esou ces, he en i onmen al a iables can indi idually o collec i ely a ec hei li e cycles.
A es ed by ou en i onmen al da a ( ime se ies no shown), 1995 was an a ypical yea du -
ing he pe iod o ou s udy. The yea o 1995 was cha ac e ized by an in ense d ough in he
Amazon basin, leading o a conside able educ ion o he aqua ic en i onmen a ea. This mus
ha e le he ich hyo auna indi iduals mo e ulne able. In 1995, ENSO was in i s posi i e
phase (El Niño) bu he e en was conside ed weak p og essing o a La Niña in he nex yea .
Du ing ha yea hough, ou da a (no shown) indica e ha he e was an a ypical inc ease in
sea su ace empe a u e in he A lan ic Ocean, a dec ease in he T ade Winds in ensi y and a
consequen educ ion in he wa e apo anspo in he eas e n po ion o he Amazon Basin
[97,106]. Du ing 1995, a lowe ing in he annual a e aged CPUE occu ed in he loodplain
lakes.
We assume ha du ing 1995 in he d ough e en , he accessibili y o he loodplain lakes
o ishe y was mo e di icul , consequen ly s imula ing he ish ac i i y and an inc ease in p o-
duc i i y in he i e en i onmen . This ac is e idenced in ou da a by he a iabili y in he
CPUE o he axonomic amily Hypoph halmidae. To esume hese ideas, we acknowledge ha
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 21 / 29

he e ec s o he clima ic (en i onmen al) a iabili y on he Lowe Amazon ishe ies a e
impo an and ollow a logic based upon s a is ical dependence. These e ec s can be exp essed
by many logical ways. In Fig 10 we p esen a logical schema ic diag am o illus a e and esume
he indings o his pape wi h espec o he dependence ela ions be ween he CPUE o all
species, he en i onmen al a iables s udied he e and he pe sis ence o posi i e o nega i e
ENSO phenomena. These ela ions a e shown in espec o he di e en seasons (d y o we )
and he ishing en i onmen s ( i e o lakes and loodplains) o ou s udy a ea. This simple,
classic diag am p esen s he a iables and hei di ec o in e se ela ions o dependence indi-
ca ed by he up o down, espec i ely, di ec ion o a ows.
A he p esen we know ha o e he ime he amoun o wa e e ained in he Amazon
Basin has been al e ed, as well as he g ea e pa o i s su ace ege a ion co e age due o long
e m geophysical ac o s [107]. In e annual a iabili y o he lood pulse and o he en i on-
men al pa ame e s, such as ai and su ace empe a u e, ha e a conside able e ec on he di e -
si y o local auna [108] and, as a esul , on he ishe ies ac i i y and p oduc ion [89]. Highe
empe a u es educe he solubili y o oxygen in wa e , which may inc ease he demand o oxy-
gen and ood consump ion o ish due o hei inc eased me abolic a e. The inc ease o he
empe a u e in he su ace laye o he wa e may also p omo e he de elopmen and su i al
o pa asi es and bac e ia. These ac s combined oge he can educe he su i al, g ow h and
ep oduc i e success o ish popula ions [109].
We also know ha he ich hyo auna in he loodplain lakes o he Lowe Amazon ha e a
complex beha io al dynamic. Du ing he we pe iod, ollowing ep oduc ion, la ae and/o
young ish o many ish species a e ca ied ou by he i e cu en in o he looded a eas [19,
61,66,110–111], a ee aqua ic en i onmen whe e hey should sea ch o ood and shel e
agains a ious ypes o p eda o . E en du ing he d y season, ish adul s y o mo e in o he
Fig 10. Logical schema ic diag am illus a ing he dependence ela ions be ween he CPUE, ENSO phenomena and
en i onmen a iables. Logical schema ic diag am illus a ing he dependence ela ions be ween he CPUE o all amilies,
he en i onmen al a iables s udied he e and he pe sis ence o posi i e o nega i e ENSO phenomena. (AN) Anos omidae,
(CI) Cichlidae, (CL) Clupeidae, (DR) Do adidae, (HY) Hypoph halmidae, (LR) Lo ica iidae, (PC) P ochilodon idae, (PI)
Pimelodidae, (SC) Sciaenidae, (SR) Se asalmidae.
doi:10.1371/jou nal.pone.0157050.g010
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 22 / 29
i e s since he aqua ic en i onmen s a e concen a ed in he main channels [61]. This pa icu-
la dynamic is echoed in ish p oduc i i y and in he beha io o he ishe men. The p edicable
e ec s o d ough in he Amazon in global clima e change scena ios include an es ima ed loss
o 7 o 12% o ish species by 2070 in he Amazon Ri e Basin [111].
Conclusion
En i onmen al a iables such as he ai , wa e and soil empe a u es, a mosphe ic humidi y,
he wa e le el, he local winds as well as clima ic a iables measu ed indexes such as he MEI,
NOA and GITA ac a dis inc empo al scales p omo ing an clea e ec on he mul ispecies
ishe ies o he Lowe Amazon egion;
The ela ionship be ween he mon hly a e age CPUE o di e en axonomic amily o a ge
ish p esen s di e en beha io depending on he en i onmen al o clima ic a iable
conside ed;
The ishe y p oduc i i y in he s udy a ea p esen s di e en pa e ns in espec o he en i-
onmen and clima e depending i i is o igina ed om he i e o om he loodplain lakes. A
clea a iabili y occu s bo h along he Ri e Amazon ex end in he Lowe Amazon (longi udi-
nal g adien ) and la e ally ac oss he i e (la i udinal g adien ) o each kind o ishe y s udied
he e. This depends on he ecological cha ac e is ics and li e s a egies o each a ge axonomic
amily conside ed in he ishe y;
The in ensi y o ish explo a ion in he Lowe Amazon egion is appa en ly s ill mode a e;
The p ese a ion o he landscape and he equilib ium o he ene gy and hyd ic balances
should be conside ed o u u e ish managemen policies;
New p og ams aiming he long e m collec ion and p ocessing o ishe y s a is ics da a in
he Amazon Ri e Basin should be pu o wa d and incen i ized. In a Global Change scena io
wi h pe cei ed changes in he ege a ion co e o he Amazon egion we belie e ha he
s eng hening o ou knowledge abou he ela ionship o he en i onmen al and clima ic a i-
ables wi h he ishe ies is c ucial o any u u e en i onmen al modeling o he egion;
Fu u e esea ch should also d i e a en ion owa ds he iden i ica ion o new a iables o be
included in o he mul i a ia e models. Possible new en i onmen al a iables should include
he posi ioning and equency o he ins abili y lines o clouds in he a mosphe e esponsible
o he egion's ain all pa e ns, he In e T opical Con e gence Zone and he Boli ian Heigh
posi ioning and pe sis ence, he lu ial b eeze, wa e quali y a iables ( o example he phy o-
planck on, nu ien s, pollu an s and dissol ed oxigen concen a ions). Ideally, new ishe ies
da a should be p oduced in a be e geo e e ing in e ace such as a Geog aphical In o ma ion
Sys em.
Suppo ing In o ma ion
S1 Da ase . CPUE i e da ase . Da ase o CPUE in he i e o ishing g ounds in Óbidos,
San a ém and Mon e Aleg e and axonomic amilies o ish. (AN) Anos omidae, (SR) Se asal-
midae, (CI) Cichlidae, (HY) Hypoph halmidae, (LR) Lo ica iidae, (PI) Pimelodidae, (PC) P o-
chilodon idae, (SC) Sciaenidae, (DR) Do adidae, (CL) Clupeidae.
(XLSX)
S2 Da ase . CPUE lake da ase . Da ase o CPUE in he loodplain lakes o ishing g ounds in
Óbidos, San a ém and Mon e Aleg e and axonomic amilies o ish. (AN) Anos omidae, (SR)
Se asalmidae, (CI) Cichlidae, (HY) Hypoph halmidae, (LR) Lo ica iidae, (PI) Pimelodidae,
(PC) P ochilodon idae, (SC) Sciaenidae, (DR) Do adidae, (CL) Clupeidae.
(XLSX)
Mul ispecies Fishe ies in he Lowe Amazon and I s Rela ionship Clima e Va iabili y
PLOS ONE | DOI:10.1371/jou nal.pone.0157050 June 17, 2016 23 / 29
S3 Da ase . Ma ke index o each ishing g ound. Ma ke index conside ing i e and lood-
plain lakes o Óbidos, San a ém and Mon e Aleg e ishing g ounds.
(XLSX)
S4 Da ase . CPUE lake da ase . Time se ies o en i onmen al a iables and clima e indeces.
(ARD) Amazon Ri e Discha ge, (WL) Wa e Le el, (RF) Rain all, (u) Zonal Wind Compo-
nen , ( ) Me idional Wind Componen , (TEMP) Su ace Tempe a u e, (SPFH) Speci ic
Humidi y, (RUNOF) Runo , (LHF) La en Hea Flux, (SSTA) Sea Su ace Tempe a u e, (MEI)
Mul i a ia e ENSO Index, (GITA) A lan ic In e -Hemisphe ic Sea Su ace Tempe a u e G adi-
en , (NAO) No h A lan ic Oscilla ion.
(XLSX)
Acknowledgmen s
The au ho s hank he Minis y o Fishe ies and Aquacul u e o B azil o eleasing he ish
da a used he e. The en i onmen al da a was ob ained om B azilian Na ional Wa e Agency
(ANA) and NOAA/NCEP. WDHP wish o hank he Pos -G adua e P og amme in Aqua ic
and Fishing Ecology o he Fede al Uni e si y o Pa á (UFPA), he g oup o Ma ine Resou ces
and Fishe ies a he Facul y o Science in he Uni e si y o A Co uña and he Depa men o
E olu ional Ecology a he Na ional Museum o Na u al Sciences o he oppo uni y o con-
duc pa o his PhD s udies in Spain. Ou hanks a e also di ec ed o Ian Emme who p o-
duced he i s English e sion o his pape .
Au ho Con ibu ions
Concei ed and designed he expe imen s: WHDP VJI. Analyzed he da a: WHDP FJLC PP
VJI. Con ibu ed eagen s/ma e ials/analysis ools: WHDP FJLC PP VJI. W o e he pape :
WHDP RBS VJI PP FJLC JF. Ob ained pe mission o use o ishing da a: WHDP VJI.
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