The bycatch of piramutaba, Brachyplatystoma vaillantii industrial fishing in a salinity and depth gradient in the Amazon estuary, Brazil

ABSTRACT

The piramutaba, Brachyplatystoma vaillantii is a freshwater catfish that is the most abundant fishery resource in the Amazon estuary. Piramutaba trawling is done on industrial fishing scale and is characterized by the presence of many freshwater and marine bycatch species, with and without commercial value. Here we describe the bycatch of the industrial fishery of piramutaba in the Amazon estuary and evaluate the relationship of two important environmental factors, depth and salinity, with the accidental capture of freshwater and marine fishes in the Amazon estuary in the rainy and dry seasons. We identified 21 cartilaginous fish species (19.1% freshwater and 80.9% marine) and 125 bony fish species (25.6% freshwater and 74.4% marine). The bycatch included 64 species without commercial value (43% of all bycatch species), which are always discarded. Freshwater and estuarine fishes exhibited significantly higher abundances in shallower environments, while marine fishes were similarly abundant along the entire depth gradient. On the contrary, the abundance of freshwater fishes significantly decreased, and that of estuarine and marine fishes significantly increased with increasing salinity. Regarding the conservation status of the bycatch species, one is classified as vulnerable (VU), and seven as critically endangered (CR). The information on the bycatch of piramutaba fishery in the Amazon estuary is important to subsidize regional fisheries policies and the management of protected areas.

KEYWORDS:
freshwater; marine; environmental factors

RESUMO

A piramutaba, Brachyplatystoma vaillantii é um bagre de água doce que representa o recurso pesqueiro mais abundante no estuário amazônico. O arrasto da piramutaba é feito em escala industrial, caracterizado pela presença de muitas espécies de água doce e marinha capturadas de forma incidental, com e sem valor comercial. Aqui descrevemos a captura incidental da pesca industrial de piramutaba no estuário amazônico e avaliamos a relação de dois fatores ambientais, profundidade e salinidade, com a captura incidental de espécies de água doce e marinhas nas estações chuvosa e seca. Identificamos 21 espécies de peixes cartilaginosos (19,1% de água doce e 80,9% marinhos) e 125 espécies de peixes ósseos (25,6% de água doce e 74,4% marinhos). A captura incidental incluiu 64 espécies sem valor comercial (43% de todas as espécies capturadas) que sempre são descartadas. Os peixes de água doce e estuarinos exibiram abundâncias significativamente maiores em ambientes mais rasos, enquanto os peixes marinhos foram igualmente abundantes ao longo de todo o gradiente de profundidade. Inversamente, a abundância de peixes de água doce diminuiu significativamente, e a de peixes estuarinos e marinhos aumentou significativamente em salinidades maiores. Em relação ao estado de conservação das espécies capturadas, uma é reconhecida como vulnerável (VU) e sete como criticamente ameaçadas (CR). As informações sobre a captura incidental da pesca da piramutaba no estuário amazônico são fundaentais para subsidiar políticas pesqueiras regionais e gestão de áreas protegidas.

PALAVRA-CHAVE:
água doce; marinho; fatores ambientais

INTRODUCTION

The piramutaba, Brachyplatystoma vaillantii (Siluriformes: Pimelodidae) is a freshwater catfish that is the most abundant fishery resource of the Amazon estuary, formed by a panmitic population along the Solimões-Amazonas River (Barthem and Goulding 1997; Formiga et al. 2021). This catfish is explored by artisanal fisheries using gillnets and long lines and industrial fisheries using pair or triple trawling (Barthem, and Goulding 1997; Ruffino 2003). The industrial fishery of the piramutaba began in 1971 with the use of adapted shrimp boats (Silva et al. 2016), reached the largest landing (22,486 tonnes) in 1977, and occupied the ninth place on the list of exportation goods from Pará state, Brazil by 1980 (Dias-Neto et al. 1985; Barthem 1990; Dias-Neto 1991; Prestes et al. 2022). The piramutaba trawl fishery is limited to the Amazon estuary facing the Marajó Island and the coast of state of Amapá coast, Brazil (Prestes et al. 2022), a region characterized by the extensive input of sediments by the Amazon River (Geyer et al. 1996), with enormous oscillation in the discharge of the Amazon River, which, at its peak in May-June, more than doubles the minimum discharge, which occurs in November (Guimberteau et al. 2012). The region is located between the North Cape (01º42’S and 49º55’W) and the Maguari Cape (00º15’S and 48º25’W) (Figure 1), encompassing a 80-mile coastline stretch with a depth range between 3 and 20 m (Santos et al. 1984; Dias-Neto et al. 1985).

Figure 1
Location of the Amazon estuary (small map, in red) and detailment of the study area between North Cape (one asterisk) and Maguari Cape (two asterisks) by the mouth of the Amazon River. This figure is in color in the electronic version.

The great economic importance of the piramutaba fishery led to many scientific studies on the species, including topics such as migration (Godoy 1979; Barthem and Goulding 1997; Duponchelle et al. 2021), age and growth determination (Barthem and Petrere 1995; Alonso and Pirker 2005), genetic variability (Rodrigues 2009; Batista et al. 2005), fishing stock (Barthem 1990; Barthem and Petrere 1995; Chaves et al. 2003; Alonso and Pirker 2005; Barthem et al. 2015), gear selectivity (Barthem 1998; Furtado Junior et al. 2013), and fisheries management (Klautau et al. 2016a; Prestes et al. 2022). The knowledge on the biodiversity of the bycatch produced during the paired trawling, however, is still poor and marred by dubious species identifications (Barthem 1985; Jimenez et al. 2013; Silva et al. 2016; Klautau et al. 2016b) which is further complicated by the absence of voucher material from bycatch surveys (AP Marceniuk, personal observation).

Trawling has low selectivity, therefore producing a high proportion of accidental captures (Perez and Pezzuto 1998; Diamond et al. 2000) of species with and without commercial value, the latter being discarded (Alverson et al. 1994; Clucas 1998). Accidental captures may have a significant impact on local biodiversity (Clucas 1997) by altering the community structure and food webs (Anderson et al. 2013), which makes trawling management challenging (Davies et al. 2009). The correct identification of the bycatch is fundamental for establishing the guidelines for fisheries zonation, which should be based on all the populations affected by the activity (sensu Manthey and Fridley 2009). Therefore, the incomplete knowledge of the fish diversity of the bycatch of the piramutaba industrial fishery hampers the development of effective protection measures for the local fauna and the management of the ecosystems affected by the activity (Thrush et al. 1998; Greenstreet and Rogers 2004; Juan and Demestres 2012).

In this study, we describe the bycatch of the industrial fishery of the piramutaba in the Amazon estuary by integrating secondary data from the literature with primary data from the Japan International Cooperation Agency (JICA), the Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Norte (CEPNOR-ICMBIO), and personal databases from collaborators. Considering that salinity and depth were the main forces that structured the distribution patterns of species in the Ariidae family in the Amazon estuary (Soares et al. 2021), we analyzed the influence of these two factors considering the abundance of all fish captured by trawls in the same area. For this, we grouped the fish into three groups, marine, estuarine and freshwater, and tested the abundance of these groups in response to salinity and depth in the periods of the year when the discharge of the Amazon River is maximum and minimum.

MATERIAL AND METHODS

Study area

The study area was undertaken in the inner estuary of the Amazon River mouth, in the fishing area of the Brazilian bottom pair trawler fleet (Figure 1). The area is characterized by the shallow muddy bottom and the dynamism of the mixture of the freshwater of the Amazon River and the marine water (Curtin and Legeckis 1986; Eisma and Marel 1971). The annual discharge cycle of the Amazon River ranges from 230×103 m³ s⁻¹ in the first half of the year to 103×103 m³ s⁻¹ in the second half (Guimberteau et al. 2012) and causes the displacement of wedge salt along the shelf of the Amazon mouth, being the most critical force acting on the salinity structure of the plume (Geyer et al. 1996). The dry season is marked by the arrival of brackish waters to the coast in May, and by the predominance of fresh waters from December (Barthem and Schwassmann 1994).

Database

We compiled a species list of bycatch from available data of published studies on the bycatch of the industrial outrigger trawling fleet of the North coast do Brazil (Barthem 1985; Jimenez et al. 2013; Silva et al. 2016; Klautau et al. 2016), primary data from the Japan International Cooperation Agency (JICA) from 1996 to 1997, and Research and Conservation National Center of Northern Marine Biodiversity (CEPNOR, Brazil) from 2016 to 2020.

The collections by JICA, Museu Paraense Emilio Goeldi (MPEG), and Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) were performed between 1996 and 1997, sampling in an area divided into 1330 blocks of 3′ latitude by 3′ longitude each and nearly nine square nautical miles in total. Samplings were carried out during three trawling expeditions in the dry period of 1996 (August to September), the rainy period of 1997 (March to April), and the dry period of 1997 (August to September). Each seasonal survey comprised 120 trawling stations distributed randomly and proportionally to the area of three strata of isobaths: 5-10 m, 10-20 m, and 20-50 m. In each station, fishes were sampled by bottom trawling conducted by a pair of vessels operating for 30 min along the current direction at a constant 2-3 knots speed. Standardized trawls were carried out at daytime by trawlers equipped with bottom trawl nets of 58.2 m length and 14 cm between opposite knots, with all collected specimens identified and counted.

The collections by CEPNOR were carried out under SISBIO license # 44915-7 and all species collected by CEPNOR are represented by voucher specimens in the ichthyological collection of Museu Paraense Emílio Goeldi (MPEG) in Belém (Pará, Brazil), the zoological collection of Universidade Santa Cecília at Santos (AZUSC) in Santos (São Paulo, Brazil), and the Laboratory of Fish Biology and Genetics (LBP) at Universidade Estadual Paulista Júlio de Mesquita in Botucatu (São Paulo, Brazil). Images and voucher numbers of all marine species captured by CEPNOR are available in Marceniuk et al. (2020; 2021a).

Species were identified using the descriptions and collection keys provided by Van Der Sleen and Albert (2017) and Marceniuk et al. (2021a). Species were further classified as primary marine, estuarine, or freshwater following Nelson (2016) and as pelagic, demersal, or benthonic following Marceniuk et al. (2021b). The market value for the piramutaba and all other bycatch was obtained at Ver-o-Peso Market (Belém, Pará state, Brazil) by WSRS, APM and JPRJ. The conservation status of the species followed the Red Book of the Brazilian Fauna Threatened with Extinction (ICMBio, 2018), and its updates (MMA 2022).

Depth and salinity information were obtained during the sea-borne survey in the Amazon River Mouth by JICA, concomitantly with the collection of the primary data on fish composition. Salinity was measured from the surface to the bottom with an STD (Alec Denshi AST200PK STD, salinity measuring capability 0-40 ‰, depth range 0-200 m, measurement distance 0.2 m).

Statistical analysis

We evaluated the importance of seasonality and two environmental variables (depth and salinity) to the abundance of freshwater, estuarine, and marine fish using the data sampled by JICA between 1996 and 1997. As the data distribution was heteroscedastic (according to Levene’s test), we used the Kruskal-Wallis H test to evaluate differences in the abundance of freshwater, estuarine, and marine fish between the rainy and dry seasons. We then evaluated the importance of depth (average depth at hauling) and salinity (average salinity at hauling) to the average abundance of freshwater, estuarine, and marine fishes by fitting generalized additive models (GAMs) integrating a smoothing parameter to consider the nonlinear relationship of the variables. GAMs were performed using the default gam function from the mgcv package (Wood 2011) in the R environment (R Core Team 2021). All analyses considered a 5% level of significance.

RESULTS

Bycatch species composition

We identified 21 sharks and batoids from 10 taxonomic families and five orders (Table 1; Figure 2a), with four freshwater species (19.1%), and 17 marine species (80.9%). The richest order among the elasmobranchs was Myliobatiformes, with 11 species, four associated with freshwater, and seven with marine environments (Table 1). The richest family among cartilaginous fishes was Potamotrygonidae, including five species, four associated with freshwater (Table 1). Regarding habitat use, 12 cartilaginous species were benthonic (i.e., associated with the substrate), and nine were pelagic or demersal (i.e., actively swimming in the water column) (Table 1). Isogomphodon oxyrhynchus, Fontitrygon geijskesi, Plesiotrygon iwamae (Figure 3a), Potamotrygon humerosa (Figure 3b), Potamotrygon scobina (Figure 3d) and Styracura schmardae are endemic to the area of influence of the Amazon-Orinoco plume and its drainages (Table 1).

Table 1
Sharks, batoids and bone fishes caught as bycatch of piramutaba fishery in the Amazon estuary, on the northern coast of Brazil. Orders and families are ordered alphabetically. Figure = in Marceniuk et al. (2019) (*), in Marceniuk et al. (2021a) (**), or in present study (without asterisk). Species list = published and unpublished species surveys where the soecies is listed: Barthem (1985) (A), Jimenez et al. (2013) (B), Silva et al. (2016) (C), Klautau et al. (2016) (D), JICA (E), CEPNOR onboard observers (F). Comm value = commercial value: target species (A), commercial value higher than target species (>), commercial value lower than target species (<), equal commercial value equal to target species (=), no commercial value (*). Habitat: freshwater (FW), brackish water (BW), marine and estuarine (M). Habit: pelagic (I), demersal (J), benthic (K). End = endemic to the influence area of the Amazonian-Orinoco plume and its drainages. Status = conservation status in the Brazilian List of Endangered Fauna (ICMBio 2018): CR = critically endangered (CR), vulnerable (V), near threatened (NT), least concern (LC), data deficient (DD), not evaluated (X) .

Order	Family	Species	Figure	Species list						Comm value	Habitat	Habit			End	Status
				A	B	C	D	E	F			I	J	K
Carcharhiniformes	Carcharhinidae	Carcharhinus leucas (Valenciennes, 1839)		X				X		<	M	X	X			NT
Carcharhiniformes	Carcharhinidae	Carcharhinus limbatus (Valenciennes, 1839)	*Fig. 3e	X				X	X	<	M	X	X			NT
Carcharhiniformes	Carcharhinidae	Carcharhinus porosus (Ranzani, 1839)		X				X	X	<	M	X	X			CR
Carcharhiniformes	Carcharhinidae	Isogomphodon oxyrhynchus (Müller & Henle, 1839)	*Fig. 4a	X				X	X	*	M		X		X	CR
Carcharhiniformes	Sphyrnidae	Sphyrna lewini (Griffith & Smith, 1834)	*Fig. 4d						X	<	M	X	X			CR
Carcharhiniformes	Sphyrnidae	Sphyrna tiburo (Linnaeus, 1758)	*Fig. 4f					X	X	<	M	X	X			CR
Carcharhiniformes	Sphyrnidae	Sphyrna tudes (Valenciennes, 1822)		X				X	X	<	M	X	X			CR
Torpediniformes	Narcinidae	Narcine brasiliensis (Olfers, 1831)	*Fig. 5c					X	X	*	M			X		DD
Rhinopristiformes	Pristidae	Pristis pristis (Linnaeus, 1758)	*Fig. 2a	X					X	<	M			X		CR
Myliobatiformes	Dasyatidae	Fontitrygon geijskesi (Boeseman, 1948)	*Fig. 2f		X			X	X	<	M/BW			X	X	DD
Myliobatiformes	Dasyatidae	Hypanus berthalutzae Petean, Naylor & Lima, 2020	*Fig. 5j							<	M			X		DD
Myliobatiformes	Dasyatidae	Hypanus guttatus (Bloch & Schneider, 1801)	*Fig. 5k	X		X	X	X	X	<	M			X		LC
Myliobatiformes	Gymnuridae	Gymnura micrura (Bloch & Schneider, 1801)	*Fig. 6e-f					X	X	*	M			X		NT
Myliobatiformes	Myliobatidae	Aetobatus narinari (Euphrasen, 1790)	*Fig. 6g					X	X	<	M	X	X			DD
Myliobatiformes	Potamotrygonidae	Plesiotrygon iwamae Rosa, Castello & Thorson, 1987	Fig. 3a						X	<	FW			X	X	NT
Myliobatiformes	Potamotrygonidae	Potamotrygon humerosa Garman, 1913	Fig. 3b						X	<	FW			X	X	DD
Myliobatiformes	Potamotrygonidae	Potamotrygon orbignyi (Castelnau, 1855)	Fig. 3c						X	<	FW			X		LC
Myliobatiformes	Potamotrygonidae	Potamotrygon scobina Garman, 1913	Fig. 3d			X	X		X	<	FW			X	X	LC
Myliobatiformes	Potamotrygonidae	Styracura schmardae (Werner, 1904)	*Fig. 6d						X	<	M/BW			X	X	DD
Myliobatiformes	Urotrygonidae	Urotrygon microphthalmum Delsman, 1941	*Fig. 5i						X	<	M			X		DD
Rajiformes	Rhinopteridae	Rhinoptera bonasus (Mitchill, 1815)	*Fig. 6i					X	X	<	M	X				DD
Elopiformes	Elopidae	Elops smithi McBride et al. 2010	** pg. 81	X				X	X	<	M	X	X			LC
Elopiformes	Megalopidae	Megalops atlanticus Valenciennes, 1847	** pg. 83	X			X	X		<	M/BW	X				VU
Anguilliformes	Ophichthidae	Ahlia egmontis (Jordan, 1884)						X	X	*	M			X		LC
Anguilliformes	Muraenesocidae	Cynoponticus savanna (Bancroft, 1831)	**pg. 117						X	*	M		X			LC
Anguilliformes	Moringuide	Neoconger sp.	**pg. 127						X	*	M		X		X	X
Clupeiformes	Pristigasteridae	Chirocentrodon bleekerianus (Poey, 1867)	**pg. 131						X	*	M	X				LC
Clupeiformes	Pristigasteridae	Odontognathus mucronatus Lacepède, 1800	**pg. 132					X	X	*	M	X				LC
Clupeiformes	Pristigasteridae	Pellona castelnaeana Valenciennes, 1847	Fig. 3e						X	<	FW	X			X	LC
Clupeiformes	Pristigasteridae	Pellona flavipinnis (Valenciennes, 1837)	Fig. 3f	X	X	X	X	X	X	<	FW	X				LC
Clupeiformes	Pristigasteridae	Pellona harroweri (Fowler, 1917)	**pg. 133					X	X	<	M	X				LC
Clupeiformes	Engraulidae	Anchoa januaria (Steindachner, 1879)	**pg. 137						X	*	M/BW	X				LC
Clupeiformes	Engraulidae	Anchoa spinifer (Valenciennes, 1848)	**pg. 140	X				X	X	*	M/BW	X				LC
Clupeiformes	Engraulidae	Anchovia clupeoides (Swainson, 1839)	**pg. 141				X			*	M/BW	X				LC
Clupeiformes	Engraulidae	Anchoviella cayennensis (Puyo, 1945)	**pg. 144	X						*	M/BW	X				LC
Clupeiformes	Engraulidae	Anchoviella lepidentostole (Fowler, 1911)	**pg. 147					X		*	M/BW	X				LC
Clupeiformes	Engraulidae	Lycengraulis batesii (Günther, 1868)	**pg. 149	X				X		*	FW/BW	X			X	LC
Clupeiformes	Engraulidae	Lycengraulis grossidens (Spix & Agassiz, 1829)	**pg. 150							*	M/BW	X				LC
Clupeiformes	Clupeidae	Opisthonema oglinum (Lesueur, 1818)	**pg. 156					X	X	*	M	X				LC
Clupeiformes	Clupeidae	Sardinella aurita Valenciennes, 1847							X	*	M	X				DD
Siluriformes	Loricariidae	Aphanotorulus emarginatus (Valenciennes, 1840)	Fig. 3g	X					X	*	FW			X		X
Siluriformes	Loricariidae	Hypostomus punctatus Valenciennes, 1840			X					*	FW			X		LC
Siluriformes	Ariidae	Amphiarius rugispinis (Valenciennes, 1840)	**pg. 162	X		X	X	X		<	M				X	LC
Siluriformes	Ariidae	Amphiarius phrygiatus (Valenciennes, 1840)	**pg. 163	X	X			X	X	<	M/BW		X		X	LC
Siluriformes	Ariidae	Aspistor quadriscutis (Valenciennes, 1840)	**pg. 164		X	X	X	X	X	<	M/BW		X		X	LC
Siluriformes	Ariidae	Bagre bagre (Linnaeus, 1766)	**pg. 165	X	X	X		X	X	<	M		X			NT
Siluriformes	Ariidae	Cathorops arenatus (Valenciennes, 1840)	**pg. 167					X	X	<	M		X		X	LC
Siluriformes	Ariidae	Cathorops spixii (Agassiz, 1829)	**pg. 168	X	X		X		X	<	M/BW		X			LC
Siluriformes	Ariidae	Notarius grandicassis (Valenciennes, 1840)	**pg. 169	X	X		X	X	X	<	M		X		X	LC
Siluriformes	Ariidae	Sciades couma (Valenciennes, 1840)	**pg. 170	X				X	X	<	M/BW		X		X	DD
Siluriformes	Ariidae	Sciades herzbergii (Bloch, 1794)	**pg. 171		X					<	M		X		X	LC
Siluriformes	Ariidae	Sciades parkeri (Trail, 1832)	**pg. 172	X	X	X	X	X	X	>	M		X		X	LC
Siluriformes	Ariidae	Sciades proops (Valenciennes, 1840)	**pg. 174	X	X	X	X	X	X	<	M		X		X	DD
Siluriformes	Aspredinidae	Aspredinichthys filamentosus (Valenciennes, 1840)	Fig. 3h	X				X	X	*	FW			X	X	LC
Siluriformes	Aspredinidae	Aspredo aspredo (Linnaeus, 1758)	Fig. 3i	X	X	X	X		X	*	FW			X	X	LC
Siluriformes	Doradidae	Centrodoras brachiatus (Cope, 1872)	Fig. 3j	X				X	X	<	FW		X		X	LC
Siluriformes	Doradidae	Lithodoras dorsalis (Valenciennes, 1840)	Fig. 3k	X	X	X	X		X	<	FW		X		X	LC
Siluriformes	Doradidae	Pterodoras granulosus (Valenciennes, 1821)			X		X			<	FW		X			LC
Siluriformes	Auchenipteridae	Trachelyopterus galeatus (Linnaeus, 1766)	Fig. 3l						X	<	FW	X				LC
Siluriformes	Auchenipteridae	Ageneiosus inermis (Linnaeus, 1766)			X					<	FW	X				LC
Siluriformes	Auchenipteridae	Ageneiosus ucayalensis Castelnau, 1855	Fig. 3m	X		X	X	X	X	*	FW	X			X	LC
Siluriformes	Auchenipteridae	Pseudauchenipterus nodosus (Bloch, 1794)	Fig. 3n					X	X	*	FW		X		X	LC
Siluriformes	Heptapteridae	Pimelodella altipinnis (Steindachner, 1864)				X	X			*	FW		X		X	X
Siluriformes	Heptapteridae	Pimelodella cristata (Müller & Troschel, 1849)			X					*	FW		X		X	LC
Siluriformes	Pimelodidae	Brachyplatystoma filamentosum (Lichtenstein, 1819)	Fig. 3o	X	X	X	X	X	X	>	FW		X		X	LC
Siluriformes	Pimelodidae	Brachyplatystoma platynemum Boulenger, 1898	Fig. 3p	X	X	X	X		X	<	FW		X		X	LC
Siluriformes	Pimelodidae	Brachyplatystoma rousseauxii (Castelnau, 1855)	Fig. 3q		X	X	X		X	>	FW		X		X	LC
Siluriformes	Pimelodidae	Brachyplatystoma vaillantii (Valenciennes, 1840)	Fig. 3r	X				X	X	A	FW		X		X	LC
Siluriformes	Pimelodidae	Hypophthalmus edentatus Spix & Agassiz, 1829	Fig. 3s			X	X		X	*	FW		X		X	LC
Siluriformes	Pimelodidae	Hypophthalmus marginatus Valenciennes, 1840			X					*	FW		X		X	LC
Siluriformes	Pimelodidae	Pimelodus blochii Valenciennes, 1840		X			X			*	FW		X		X	LC
Siluriformes	Pimelodidae	Pinirampus pirinampu (Spix & Agassiz, 1829			X					*	FW		X			LC
Siluriformes	Pimelodidae	Propimelodus eigenmanni (van der Stigchel, 1946)	Fig. 3t				X		X	*	FW		X		X	LC
Siluriformes	Pimelodidae	Zungaro zungaro (Humboldt, 1821)		X				X		=	FW		X		X	LC
Gymnotiformes	Apteronotidae	Sternarchella schotti (Steindachner, 1868)	Fig. 3u						X	*	FW		X			LC
Gymnotiformes	Apteronotidae	Sternarchella sima Starks, 1913	Fig. 3v						X	*	FW		X			LC
Gymnotiformes	Apteronotidae	Sternarchorhamphus muelleri (Steindachner, 1881)	Fig. 3w						X	*	FW		X		X	LC
Gymnotiformes	Sternopygidae	Eigenmannia virescens (Valenciennes, 1836)			X					*	FW		X			LC
Batrachoidiformes	Batrachoididae	Batrachoides surinamensis (Bloch & Schneider, 1801)	**pg. 203	X	X	X	X	X	X	<	M/BW			X		LC
Batrachoidiformes	Batrachoididae	Porichthys plectrodon Jordan & Gilbert, 1882	**pg. 208						X	*	M			X		LC
Gobiiformes	Gobiidae	Awaous flavus (Valenciennes, 1837)	**pg. 231	X						*	M			X		DD
Gobiiformes	Gobiidae	Bathygobius soporator (Valenciennes, 1837)	**pg. 233	X						*	M			X		LC
Gobiiformes	Gobiidae	Gobioides broussonnetii Lacepède, 1800	**pg. 243						X	*	M			X		LC
Gobiiformes	Gobiidae	Gobioides grahamae Palmer & Wheeler, 1955	**pg.244	X				X	X	*	M/BW			X	X	LC
Mugiliformes	Mugilidae	Mugil brevirostris Miranda Ribeiro, 1915	**pg. 269						X	=	M	X				X
Mugiliformes	Mugilidae	Mugil curema Valenciennes, 1836	**pg. 270	X		X	X		X	=	M	X				DD
Mugiliformes	Mugilidae	Mugil incilis Hancock, 1830	**pg. 272		X					=	M	X				LC
Cyprinodontiformes	Anablepidae	Anableps microlepis Müller & Troschel, 1844	**pg. 324	X						*	M	X				LC
Carangiformes	Echeneidae	Echeneis naucrates Linnaeus, 1758	**pg. 330				X	X	*	M	X				LC
Carangiformes	Carangidae	Caranx hippos (Linnaeus, 1766)	**pg. 341	X						<	M	X	X			LC
Carangiformes	Carangidae	Chloroscombrus chrysurus (Linnaeus, 1766)	**pg. 344						X	*	M	X				LC
Carangiformes	Carangidae	Hemicaranx amblyrhynchus (Cuvier, 1833)	**pg. 349					X	X	<	M	X				LC
Carangiformes	Carangidae	Oligoplites palometa (Cuvier, 1832)	**pg. 350	X	X			X	X	<	M	X				LC
Carangiformes	Carangidae	Oligoplites saliens (Bloch, 1793)	**pg. 351		X			X		<	M	X				LC
Carangiformes	Carangidae	Oligoplites saurus (Bloch & Schneider, 1801)	**pg. 352		X			X		<	M	X				LC
Carangiformes	Carangidae	Selene setapinnis (Mitchill, 1815)	**pg. 354					X	X	<	M	X				LC
Carangiformes	Carangidae	Selene vomer (Linnaeus, 1758)	**pg. 356					X	X	<	M	X				LC
Carangiformes	Carangidae	Trachinotus carolinus (Linnaeus, 1766)	**pg. 359					X	X	=	M	X				LC
Carangiformes	Carangidae	Trachinotus cayennensis Cuvier, 1832	**pg. 360					X	X	=	M	X			X	DD
Istiophoriformes	Sphyraenidae	Sphyraena guachancho Cuvier, 1829	**pg. 365					X	X	*	M	X				LC
Pleuronectiformes	Paralichthyidae	Citharichthys macrops Dresel, 1885	**pg. 381	X					X	*	M			X		LC
Pleuronectiformes	Bothidae	Bothus robinsi Topp & Hoff, 1972	**pg. 394					X	X	*	M/BW			X		LC
Pleuronectiformes	Achiridae	Achirus achirus (Linnaeus, 1758)	**pg. 397	X	X			X	X	*	M/BW			X		LC
Pleuronectiformes	Achiridae	Achirus lineatus (Linnaeus, 1758)	**pg. 399	X	X	X	X			*	M			X		LC
Pleuronectiformes	Achiridae	Apionichthys dumerili Kaup, 1858.	**pg. 400		X			X	X	*	M/BW			X	X	LC
Pleuronectiformes	Achiridae	Trinectes paulistanus (Miranda Ribeiro, 1915)	**pg. 403		X				X	*	M			X		LC
Scombriformes	Trichiuridae	Trichiurus lepturus Linnaeus, 1758	**pg. 431		X			X	X	<	M	X	X	X		LC
Scombriformes	Scombridae	Acanthocybium solandri (Cuvier, 1832)	**pg. 434		X					<	M	X				LC
Scombriformes	Scombridae	Scomberomorus brasiliensis Collette et al. 1978	**pg. 439	X	X			X		=	M	X				LC
Scombriformes	Scombridae	Scomberomorus cavalla (Cuvier, 1829)	**pg. 440						X	>	M	X				LC
Scombriformes	Stromateidae	Peprilus crenulatus Cuvier, 1829	**pg. 447	X				X	X	<	M	X				X
Perciformes	Centropomidae	Centropomus irae Carvalho-Filho et al. 2019	**pg. 482		X				X	>	M		X		X	X
Perciformes	Centropomidae	Centropomus parallelus Poey, 1860	**pg. 483	X	X				X	>	M		X			LC
Perciformes	Centropomidae	Centropomus pectinatus Poey, 1860	**pg. 484		X			X	X	>	M		X			LC
Perciformes	Centropomidae	Centropomus undecimalis (Bloch, 1792)	**pg. 485		X		X		X	>	M		X			LC
Perciformes	Serranidae	Epinephelus itajara (Lichtenstein, 1822)	**pg. 548				X		X	*	M		X			CR
Perciformes	Serranidae	Serranus atrobranchus (Cuvier, 1829)	**pg. 535					X	X	*	M		X			LC
Perciformes	Haemulidae	Genyatremus luteus (Bloch, 1790)	**pg. 565	X	X			X	X	=	M		X			LC
Perciformes	Haemulidae	Orthopristis scapularis Fowler, 1915	**pg. 574					X		*	M		X			X
Perciformes	Polynemidae	Polydactylus virginicus (Linnaeus, 1758)	**pg. 596		X				X	*	M		X			LC
Ephippiformes	Ephippidae	Chaetodipterus faber (Broussonet, 1782)	**pg. 619	X	X			X	X	*	M	X	X			LC
Acanthuriformes	Sciaenidae	Bairdiella goeldi Marceniuk et al, 2019	**pg. 625				X			*	M		X			X
Acanthuriformes	Sciaenidae	Ctenosciaena gracilicirrhus (Metzelaar, 1919)	**pg. 626		X			X		*	M		X			LC
Acanthuriformes	Sciaenidae	Cynoscion acoupa (Lacepède, 1801)	**pg. 627	X	X	X	X		X	>	M		X			NT
Acanthuriformes	Sciaenidae	Cynoscion jamaicensis (Vaillant & Bocourt, 1883)	**pg. 628						X	<	M		X			LC
Acanthuriformes	Sciaenidae	Cynoscion leiarchus (Cuvier, 1830)	**pg. 629					X		<	M		X			LC
Acanthuriformes	Sciaenidae	Cynoscion microlepidotus (Cuvier, 1830)	**pg. 630	X						<	M		X			LC
Acanthuriformes	Sciaenidae	Cynoscion similis Randall & Cervigón, 1968	**pg. 631						X	<	M		X			X
Acanthuriformes	Sciaenidae	Cynoscion steindachneri (Jordan, 1889)	**pg. 632						X	<	M		X			LC
Acanthuriformes	Sciaenidae	Cynoscion virescens (Cuvier, 1830)	**pg. 633				X		X	<	M		X			LC
Acanthuriformes	Sciaenidae	Isopisthus parvipinnis (Cuvier, 1830)	**pg. 635					X	X	<	M		X			LC
Acanthuriformes	Sciaenidae	Larimus breviceps Cuvier, 1830	**pg. 636						X	*	M		X			LC
Acanthuriformes	Sciaenidae	Lonchurus lanceolatus (Bloch, 1788)	**pg. 638					X	X	*	M		X		X	LC
Acanthuriformes	Sciaenidae	Macrodon ancylodon (Bloch & Schneider, 1801)	**pg. 639	X	X	X	X	X	X	=	M		X			LC
Acanthuriformes	Sciaenidae	Micropogonias furnieri (Desmarest, 1823)	**pg. 642		X		X	X	X	<	M		X			LC
Acanthuriformes	Sciaenidae	Nebris microps Cuvier, 1830	**pg. 643		X			X	X	<	M		X			LC
Acanthuriformes	Sciaenidae	Paralonchurus brasiliensis (Steindachner, 1875)	**pg. 645					X	X	<	M		X			LC
Acanthuriformes	Sciaenidae	Plagioscion auratus (Castelnau, 1855)	Fig. 3x	X	X			X	X	=	FW		X		X	LC
Acanthuriformes	Sciaenidae	Plagioscion squamosissimus (Heckel, 1840)	Fig. 3y	X	X	X	X		X	=	FW		X			LC
Acanthuriformes	Sciaenidae	Stellifer microps (Steindachner, 1864)	**pg. 652	X	X			X	X	*	M		X			LC
Acanthuriformes	Sciaenidae	Stellifer rastrifer (Jordan, 1889)	**pg. 656	X	X			X	X	*	M		X			LC
Lobotiformes	Lobotidae	Lobotes surinamensis (Bloch, 1790)	**pg. 665	X				X	X	<	M	X	X			LC
Lophiiformes	Ogcocephalidae	Ogcocephalus nasutus (Cuvier, 1829)	**pg. 681						X	*	M			X		LC
Tetraodontiformes	Tetraodontidae	Colomesus psittacus (Bloch & Schneider, 1801)	**pg. 710	X	X			X	X	*	M/BW		X	X	X	LC
Tetraodontiformes	Tetraodontidae	Lagocephalus laevigatus (Linnaeus, 1766)	**pg. 711					X		*	M	X	X			LC
Tetraodontiformes	Diodontidae	Chilomycterus antillarum Jordan & Rutter, 1897	**pg. 720					X	X	*	M		X			LC

Figure 2
Composition of the bycatch of piramutaba fisheries in the Amazon estuary, northern coast of Brazil. A - Taxonomic and marine-estuarine/freshwater composition (%) of Elasmobranchii; B - Taxonomic and marine-estuarine/freshwater composition (%) of Teleostei; C - Economic value of the by-catch species: higher than Brachyplatystoma vaillantii (red), equal to B. vaillantii (orange), lower than B. vaillantii (yellow), no commercial value (grey); D - Conservation status: critically endangered (CR), vulnerable (VU), near threatened (NT), data deficient (DD), not evaluated (NE), least concern (LC). This figure is in color in the electronic version.

Figure 3
Freshwater batoids and bony fishes captured as bycatch of piramutaba fisheries in the Amazon estuary, northern coast of Brazil. Order Myliobatiformes, family Potamotrygonidae: A - Plesiotrygon iwamae (broken caudal fin); B - Potamotrygon humerosa; C - Potamotrygon orbignyi; D - Potamotrygon scobina. Order Clupeiformes, family Pristigasteridae: E - Pellona castelnaeana; F - Pellona flavipinnis. Order Siluriformes, family Loricariidae: G - Aphanotorulus emarginatus; family Aspredinidae: H - Aspredinichthys filamentosus; I - Aspredo aspredo; family Doradidae: J - Centrodoras brachiatus; K - Lithodoras dorsalis; family Auchenipteridae: L - Trachelyopterus galeatus; M - Ageneiosus ucayalensis; N - Pseudauchenipterus nodosus; family Pimelodidae: O - Brachyplatystoma filamentosum; P - Brachyplatystoma platynemum; Q - Brachyplatystoma rousseauxii; R - Brachyplatystoma vaillantii; S - Hypophthalmus edentatus; T - Propimelodus eigenmanni. Order Gymnotiformes, family Apteronotidae: U - Sternarchella schotti; V - Sternarchella sima; W - Sternarchorhamphus muelleri. Order Acanthuriformes, family Sciaenidae: X - Plagioscion auratus; Y - Plagioscion squamosissimus. This figure is in color in the electronic version.

Regarding bony fishes, we identified 125 species (Table 1; Figure 2b) of 40 families and 18 orders. Thirty-two species were from freshwater (25.6%), and 93 were marine (74.4%) (Table 1). The richest order of Teleostei was Siluriformes, with 34 species, 23 of them associated with freshwater, belonging to the families Aspredinidae (Figure 3h,i), Auchenipteridae (Figure 3l-n), Doradidae (Figure 3j,k), Heptapteridae and Pimelodidae (Figure 3o-t), and 11 associated with marine environments belonging to the family Ariidae. The second richest taxonomic order of bony fishes was Acanthuriformes, including 20 species of Sciaenidae, mainly associated with marine environments (18 vs. two freshwater species, Table 1). Most of the captured teleosteans were pelagic or demersal (112 species), and only 19 were benthonic, primarily Gobiiformes and Pleuronectiformes (Table 1). Thirty-three (26.4%) of the captured bony fish species were endemic (Table 1).

The bycatch included 64 species (43% of all bycatch species) with no commercial value (Figure 2c), which are always discarded, and 81 species (57%) with some commercial value (Table 1). Among the latter, nine were more valuable than piramutaba, 11 had similar value to piramutaba, and 61 had lower value than piramutaba and were only occasionally traded (Table 1). Regarding the conservation status of the bycatch species (Figure 2d), 109 (74.7%) were classified as safe or least concern (LC), six as near threatened (NT), one as vulnerable (VU), and seven as critically endangered (CR) (Table 1). Among the critically endangered species, six were cartilaginous fishes, including the endemic Isogomphodon oxyrhynchus, the sawfish Pristis pristis and three species of hammerhead sharks (Sphyrna), and only one was a bony fish, the Atlantic goliath grouper, Epinephelus itajara. We highlight that 23 of the identified species were not evaluated (NE) or data deficient (DD), eight of them endemic to the area (Table 1).

Effect of depth and salinity

The standardized samples obtained by JICA occurred in sites with depth ranging from 6 to 50 m, and salinity near the substrate ranging from 0.05 to 36 ppm. The occurrence and abundance of freshwater, estuarine, and marine fishes between the seasons and along the depth and salinity gradients was not random. While estuarine fishes did not differ in abundance between the dry and rainy season (H₍₁₎ = 0.851; p = 0.356), the abundance of both freshwater (H₍₁₎ = 20.712; p < 0.001) and marine fishes (H₍₁₎ = 6.462; p = 0.011) was significantly higher during the rainy season. Depth and salinity affected the abundance of freshwater, estuarine, and marine fishes differently (Figure 4). Freshwater (GAM; R² = 0.132; p < 0.001) and estuarine fishes (R² = 0.024; p = 0.002) exhibited significantly higher abundance in shallower environments, while marine fishes had similar abundance along the entire depth gradient (R² = 0.001; p = 0.221). On the contrary, the abundance of freshwater fishes significantly decreased (R² = 0.444; p < 0.001), and that of estuarine (R² = 0.067; p < 0.001) and marine fishes (R² = 0.211; p < 0.001) significantly increased with increasing salinity.

Figure 4
Generalized additive models (GAM) with smoothing parameters describing the relationship of depth (upper) and salinity (bottom) with the average abundance of freshwater (left), estuarine (middle), and marine fishes (right) of the bycatch of the piramutaba fisheries in the Amazon estuary. This figure is in color in the electronic version.

DISCUSSION

The bycatch of piramutaba fishery is composed of species with and without commercial value, being that 20 to 30% of the total capture is discarded (Dias-Neto et al. 1985; Ruffino 2003; Jimenez et al. 2013). We showed that almost 45% of all captured species in the bycatch have no commercial value, while the remaining species range from lower to higher market value than that of the piramutaba. This information is crucial for optimizing management criteria for the use of the bycatch of piramutaba. Some bycatch species are already overexploited fishery resources, such as Brachyplatystoma rousseauxii (Garcia-Vasquez et al. 2009; Agudelo-Córdoba et al. 2013).

The bycatch of the industrial fishery that targets piramutaba, a primary freshwater species, is mainly composed of marine fishes, while about 25% of the species are freshwater fishes (see Table 1). This association between freshwater and marine species in the Amazonian estuary is unique compared to other oceanic basins worldwide, due to the enormous oscillation in the discharge of the Amazon River (Guimberteau et al. 2012).

The abundance of estuarine fishes did not vary significantly between the dry and the rainy seasons (minimum and maximum discharge of the Amazon River), while freshwater species were more abundant during the rainy season and marine species were more abundant during the dry seasons. Seasonal variation in rainfall is a major environmental factor determining the taxonomic and functional composition of fish communities in estuaries (Barletta et al. 2005; Castillo-Rivera 2013; Molina et al. 2020). The composition turnover is usually associated to: (i) life-history traits by species using different habitats for reproduction (Dantas et al. 2010; Fontoura et al. 2019) and (ii) physiological constraints due to changes in salinity level (Lisboa et al. 2015; Smyth and Elliott 2016).

The seasonal variation in salinity is more important for primary marine or primary freshwater species than for estuarine species, because the latter display higher osmoregulatory efficiency and can better cope with this environmental variation (Becker et al. 2011; Marshall 2012; Park et al. 2020). Consequently, the abundance of estuarine fishes tends to be stable between seasons, while abundance of marine and freshwater fishes is higher in the season when salinity levels are lower (rainy season) or higher (dry season), respectively, as corroborated by our GAM results.

The association of fish species with depth is more complex than with salinity, depending on habitat use and osmoregulation. Freshwater fishes have lower osmoregulatory efficiency and might occupy the shallower waters along the coastline both because of lower salinity levels and of adequate habitat structure. Estuarine fishes can better cope with salinity variation, but are usually inhabit or migrate seasonally to shallower areas and more structured environments (Akin et al. 2003; Barletta et al. 2005; Dantas et al. 2010). Marine species might use shallower areas with lower salinity levels in specific periods of their life cycle (Smyth and Elliott 2016). Therefore, the spatial pattern of variation in salinity levels in the Amazon estuary, where lower salinity is frequently associated with shallower areas, is important in shaping the distribution of fishes and the turnover of species with different affinity levels (Soares et al. 2021).

The majority (90%) of threatened species in the bycatch are elasmobranchs, six of them critically endangered and three vulnerable. Other threatened elasmobranch species that occur in the area, but were not reported in the piramutaba bycatch, include the stingrays Fontitrygon colarensis (VU), Paratrygon aiereba (CR) and Pseudobatos percellens (VU) (ICMBio 2018; MMA 2022). The potential negative impact of the fishery on the populations of these endangered species has not yet been assessed.

CONCLUSIONS

The present study poses an important advance on the knowledge of the fauna captured during piramutaba trawling in the mouth of the Amazon River and the influence of the hydrological cycle of the river on the structure of this community. This information will support the establishment of criteria for management for the use of the bycatch of the piramutaba fishery in order to improve the definition of areas and periods allowed for the operation of this fishing fleet. Given the observed gaps in the knowledge of the ichthyofauna in the region, we highlight the importance to increase the knowledge on the biology and fishery stocks of the endemic fauna, especially sharks and batoids.

ACKNOWLEDGMENTS

We thank Projeto Áreas Marinhas e Costeiras Protegidas - GEF Mar of the Brazilian Federal Government, responsible for supporting the collection of the specimens examined. APM is grateful to Programa de Capacitação Institucional (Ministério da Ciência, Tecnologia e Inovação - MCTIC/ Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, proc. # 444338/2018-7 and 300675/2019-4) and to the postdoctoral fellowship at Universidade Federal da Paraiba (Fundação de Apoio à Pesquisa do Estado da Paraíba - FAPESQ proc. # 1262/2021).

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• CITE AS:

  Marceniuk, A.P.; Soares, B.E.; Rotundo, M.M.; Caires, R.A.; Rosa, R.S.; Santos, W.C.R.; Cordeiro, A.P.B. et al. 2023. The bycatch of piramutaba, Brachyplatystoma vaillantii industrial fishing in a salinity and depth gradient in the Amazon estuary, Brazil. Acta Amazonica 53: 93-106.

Edited by

ASSOCIATE EDITOR:

David Santana

Publication Dates

• Publication in this collection
  28 Apr 2023
• Date of issue
  Apr-Jun 2023

History

• Received
  14 Feb 2022
• Accepted
  07 Jan 2023