Feeding habits and behaviour of Bagre bagre and Genidens barbus, two ariid catfishes (Pisces: Siluriformes) from southeastern Brazil

Communication

INTRODUCTION

Catfish are Siluriformes with a wide distribution throughout tropical, subtropical and temperate waters in lagoons, rivers, estuaries and marine coastal areas (Diogo 2004). The family Ariidae inhabits marine waters and is abundant in coastal areas associated with muddy or sandy bottoms (Marceniuk 2005; Silva et al. 2016), seeking out rivers and coastal lagoons during the spawning period (Ferraris 2007).

Marine catfish are generalist benthophagous feeders, consuming vertebrates and invertebrates such as fish, crustaceans, molluscs and polychaetes (Mishima & Tanji 1982; Froese & Pauly 2017). The mouth width and tooth-plate arrangements of Ariidae species are suitable for dealing with broad classes of prey, allowing them dietary flexibility (Blaber et al. 1994).

The family Ariidae is an important fish group in commercial fisheries worldwide (Marceniuk 2005; Froese & Pauly 2017). Bagre bagre and Genidens barbus occur along the southwest Atlantic coast, being sympatric from northern to southern Brazil, where they provide resources to artisanal coastal fisheries (Froese & Pauly 2017). Genidens barbus is of conservation concern in Brazilian waters, since it is considered to be an endangered species of economic interest (MMA 2014).

In the present study, we analyse the feeding habits and behaviour of B. bagre and G. barbus from a coastal area in Rio de Janeiro State, southeastern Brazil, to evaluate how adult specimens use available resources. Both species are important targets of artisanal commercial fisheries in this region (FIPERJ 2015), but information about their biology, including their feeding habits, is locally non-existent.

MATERIALS AND METHODS

The sampling site is a marine coastal area in Rio de Janeiro State, southeastern Brazil (Fig. 1). B. bagre and G. barbus (Image 1) are targets of commercial gillnet fishing occurring between -21.6268 S, -41.0208 W and -21.9833 S, -40.9833 W from less than one to 10 nautical miles from shore and at depths varying from 10–30 m. The specimens captured by these fisheries are adults based on their total length: the asymptotic or maximum length recorded for B. bagre is 55.0cm (Marceniuk et al. 2015), while for G. barbus, it is 120cm, with first maturity reached at approximately 40.0cm (Froese & Pauly 2017).

In 2016 (January and August), 29 specimens of B. bagre (49.8±4.7 cm mean total length; 1,003.4±255.6 g mean total weight) and 33 of G. barbus (51.9±4.1 cm mean total length; 1,393.9±273.1 g mean total weight) were obtained for stomach content analysis. The sampling included only adult specimens captured by commercial fisheries in the same location during the same time period, providing fish specimens in the same ontogenetic phase and sharing the same local habitat.

The stomach of each specimen was removed from the abdominal cavity, and the contents were washed in running water using a 500-µm mesh-size sieve and preserved in 70% ethanol. The items recovered from the stomach contents were analysed using a stereomicroscope. Partially digested fish, fish bones (e.g., spines, vertebrae, heads/skulls), scales and crystalline lenses, partially digested crustaceans and crustacean carapaces were recorded and identified whenever possible. The supraoccipital bone of Trichiurus lepturus and otoliths of Porichthys porosissimus, Conodon nobilis and Paralonchurus brasiliensis were removed from the fish skulls to back-calculate the original size of the ingested prey using the regression equations proposed by Di Beneditto et al. (2001).

The representation of the consumed food items was calculated using the percentage of frequency of occurrence (FO%): the number of stomachs with a given food item divided by the total number of stomachs with food items. The biomasses of prey were not calculated, since most recovered food items were fish or crustacean remains without any taxonomic features. Bias in the interpretation of feeding habits is expected when only one variable is examined, such as FO%, because the presence or absence of a given food item in the stomach contents does not consider the amount of food taken in (Wetherbee & Corte´s 2004). This measure, however, represents population-wide food habits, allowing a general assessment of food ingestion (Cortés 1997).

 

 

RESULTS AND DISCUSSION

 

Twenty-two B. bagre (75.8%) and 27 G. barbus (87.8%) specimens had food remains inside their stomachs. Teleost fish remains (partially digested fish, spines, vertebrae, scales and crystalline lenses) occurred in 18 stomachs of B. bagre, and prey taxonomic identification was possible for 10 stomachs. Crustacean remains (partially digested shrimps and shrimp and crab carapaces) occurred in eight stomachs, but prey identification was conducted for only two. For G. barbus, teleost fish remains occurred in 22 stomachs, and prey identification was possible for only three. Crustacean remains occurred in nine stomachs, with prey identification conducted for seven stomachs. Fishes were the more frequent prey species (82% in B. bagre and 81% in G. barbus), followed by crustaceans (36% in B. bagre and 33% in G. barbus). Table 1 shows the food items recovered from the stomach contents and their FO%.

The analysis of the stomach contents of both catfishes corroborated previous studies describing them as generalist benthophagous feeders (Mishima & Tanji 1982). All food items are bottom-associated resources and common year-round along the coast of northern Rio de Janeiro State (Di Beneditto et al. 2001; Gomes et al. 2003; Fernandes et al. 2011). The fish Trichiurus lepturus is the target of gillnet fishing in the study area (FIPERJ 2015), as well as the shrimp Xiphopenaeus kroyeri, which is the species most captured by local shrimp fisheries (Fernandes et al. 2011; 2014). The fishes P. porosissimus, C. nobilis, Gymnothorax ocellatus and P. brasiliensis are by-catch in local shrimp fisheries (Di Beneditto et al. 2001; Di Beneditto & Lima 2003). Moreover, T. lepturus and P. porosissimus are also important prey species for a coastal dolphin that inhabits the study area (Di Beneditto & Ramos 2004; Di Beneditto et al. 2017). Thus, the local availability of these prey species to consumers is high.

The feeding guilds of marine catfishes are related to their dentition. Piscivorous groups have large mouths with relatively large multiple palatine tooth plates armed with sharp, recurved teeth (Blaber et al. 1994). This description matches the oral apparatuses of B. bagre and G. barbus. Indeed, fish were the most frequent item in the stomach contents of both catfishes, although the importance of crustaceans as prey is not negligible in the study area.

The stomach content analysis also allowed inferences to be made regarding the consumer feeding behaviour, revealing an unusual pattern of predation in B. bagre. Some of the ingested prey had an estimated length that was close to that of the consumer, as in G. ocellatus, or even longer, as in T. lepturus (1.5 times longer) (Table 1). Meanwhile, for T. lepturus, only partially digested fish heads or supraoccipital bones were recovered from most of the stomach contents (Image 3). These records represent an unusual feeding behaviour, in which only the head of larger prey is ingested during predation; the position of these fish heads in the stomach, as illustrated in Image 1, suggests this kind of feeding behaviour.

Larger prey species, such as T. lepturus and G. ocellatus, are voracious consumers (Froese & Pauly 2017). Both species have a higher activity pattern during the night. During the day, T. lepturus remains close to the sea bottom, resting (Martins & Haimovici 1997; Froese & Pauly 2017), while G. ocellatus remains buried in the sand or muddy bottom with only the head above the sea bottom (Santos & Castro 2003). Prey behaviour likely influences catfish catch strategies during the day, reducing the chances of agonistic behaviour among prey during predation. Additionally, the shrimps recorded as catfish prey also remain buried in the sea bottom during the day, moving vertically in the water column in the night period (Simões et al. 2010). Thus, B. bagre and G. barbus are mainly daytime consumers.

The present study provides the first information about the feeding preferences of adult B. bagre and G. barbus in southeastern Brazil, where they are important targets in local artisanal fisheries. The results point to fish and crustaceans as the main prey species. Previous studies have mainly focused on the feeding habits of juveniles, showing ontogenetic changes from a crustacean-based diet to a fish-based diet (Mendoza-Carranza & Vieira 2009; Denadai et al. 2012) or even highlighting the presence of both prey groups (Pinheiro-Souza et al. 2015).

Although the sample size of both catfishes was too low to describe their local feeding habits accurately, it is evident from the data that they prey upon the most available resources. Since the conservation status of G. barbus in Brazil deserves attention (Endangered), data regarding its ecology, including its feeding demands and feeding strategies, are relevant to future management practices.

REFERENCES

 

Blaber, S.J.M., D.T. Brewer & J.P. Salini (1994). Diet and dentition in tropical ariid catfishes from Australia. Environmental Biology of Fishes 40(2): 159–174; https://doi.org/10.1007/BF00002543

Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Science 54(3): 726–738; https://doi.org/10.1139/f96-316

Denadai, M.R., E. Bessa, F.B. Santos, W.S. Fernandez, F.M.C. Santos, M.M. Feijó, A.C.D. Arcuri & A. Turra (2012).  The population and dietary biology of Genidens  genidens  Valenciennes, 1839, Genidens  barbus (Lacépède, 1803), and Aspistor  luniscutis  (Valenciennes, 1840) (Siluriformes: Ariidae) from Caraguatatuba Bay, Southeastern Brazil. Biota neotropica 12(4); http://www.biotaneotropica.org.br/v12n4/pt/abstract?article+bn01912042012

Di Beneditto, A.P.M. & N.R.W. Lima (2003). Biometria de teleósteos da costa norte do Estado do Rio de Janeiro para estudos sobre piscivoria. Biotemas 16(1): 135–144.

Di Beneditto, A.P.M. & R.M.A. Ramos (2004). Biology of the marine tucuxi dolphin (Sotalia fluviatilis) in south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 84(6): 1245–1250; http://doi.org/10.1017/S0025315404010744h

Di Beneditto, A.P.M, C.C.V. Badia & S. Siciliano (2017). On the feeding habit of the Guiana Dolphin Sotalia guianensis (van Bénedèn, 1864) (Mammalia: Cetartiodactyla: Delphinidae) in southeastern Brazil (~22ºS): has there been any change in more than two decades? Journal of Threatened Taxa 9(2): 9840–9843; http://doi.org/10.11609/jott.2745.9.2.9840-984

Di Beneditto, A.P.M., R.M.A. Ramos & N.R.W. Lima (2001). Os Golfinhos: Origem, Classificação, Captura Acidental, Hábito Alimentar. Editora Cinco Continentes, Porto Alegre, 148pp.

Diogo, R. (2004). Morphological Evolution, Adaptations, Homoplasies, Constraints, and Evolutionary Trends: Catfishes as a Case Study on General Phylogeny and Macroevolution. Taylor & Francis Inc, Enfield, 502pp.

Fernandes, L.P., A.C. Silva, L.P. Jardim, K.A. Keunecke & A.P.M. Di Beneditto (2011). Growth and recruitment of the Atlantic Seabob Shrimp, Xiphopenaeus kroyeri (Heller, 1862) (Decapoda, Penaeidae), on the coast of Rio de Janeiro, southeastern Brazil. Crustaceana 84(12–13): 1465–1480.

Fernandes, L.P., K.A. Keunecke & A.P.M. Di Beneditto (2014). Produção e socioeconomia da pesca do camarão sete-barbas no norte do estado do Rio de Janeiro. Boletim do Instituto de Pesca 40(4): 541–555.

Ferraris, Jr. C.J. (2007). Checklist of catfishes, recent and fossil (Osteichthyes: Siluriformes), and catalogue of siluriform primary types. Zootaxa 1418: 1–628.

FIPERJ - Fundação Instituto de Pesca do Estado do Rio de Janeiro (2015). Relatório 2015. Available at: <http://www.fiperj.rj.gov.br/fiperj_imagens/arquivos/revistarelatorios2015.pdf.

Froese, R. & D. Pauly (2017). FishBase. http://www.fishbase.org. Accessed in 20 April 2017.

Gomes, M.P., M.S. Cunha & I.R. Zalmon (2003). Spatial and temporal variations of diurnal ichthyofauna on surf-zone of São Francisco do Itabapoana beaches, Rio de Janeiro State, Brazil. Brazilian Archives of Biology and Technology 46(4): 653–664.

Marceniuk, A.P. (2005). Chave para identificação das espécies de bagres marinhos (Siluruformes, Ariidae) da costa brasileira. Boletim do Instituto de Pesca 31(2): 89–101.

Marceniuk, A.P., R. Betancur, T. Giarrizzo, F.L. Fredou & S. Knudsen (2015). Bagre bagre. The IUCN Red List of Threatened Species 2015: e.T190228A1945010. Downloaded on 16 October 2017. http://dx.doi.org/10.2305/IUCN.UK.2015-2.RLTS.T190228A1945010.en

Martins, A.S. & M. Haimovici (1997). Distribution, abundance and biological interactions of the cutlassfish Trichiurus lepturus in the southern Brazil suptropical convergence ecosystem. Fisheries Research 30: 217–227; http://doi.org/10.1016/S0165-7836(96)00566-8

Mendoza-Carranza, M. & J.P. Vieira (2009). Ontogenetic niche feeding partitioning in juvenile of White Sea Catfish Genidens barbus in estuarine environments, southern Brazil. Journal of the Marine Biological Association of the United Kingdom 89(4): 839–848; https://doi.org/10.1017/S0025315408002403

MMA - Ministério do Meio Ambiente (2014). Portaria MMA nº 445 de 17/12/2014. Available at http://www.icmbio.gov.br/portal/images/stories/biodiversidade/fauna-brasileira/avaliacao-do-risco/PORTARIA_N%C2%BA_445_DE_17_DE_DEZEMBRO_DE_2014.pdf.

Mishima, M. & S. Tanji (1982). Nicho alimentar de bagres marinhos (Teleostei; Ariidae) no complexo estuarino lagunar da Cananéia (25ºS, 48ºW). Boletim do Instituto de Pesca 9: 131–140.

Pinheiro-Sousa, D.B., N.K. Silva, N.M. Pioski, A.C.G. Rocha, R.N.F. Carvalho-Neta & Z.S. Almeida (2015). Aspectos alimentares e reprodutivos de Bagre bagre (Pisces, Ariidae) em um estuário da ilha de São Luís, Maranhão, Brasil. Revista Brasileira de Engenharia de Pesca 8: 1–12.

Santos, F.B. & R.M.C. Castro (2003). Activity, habitat utilization, feeding behaviour, and diet of the Sandy moray Gymnothorax ocellatus (Anguilliformes, Muraenidae) in the southwestern Atlantic. Biotaneotropica 3(1); http://www.biotaneotropica.org.br/v3n1/pt/abstract?article+BN00103012003

Silva, W.C., A.P. Marceniuk, J.B.L. Sales & J. Araripe (2016). Early Pleistocene lineages of Bagre bagre (Linnaeus, 1766) (Siluriformes: Ariidae), from the Atlantic coast of South America, with insights into demography and biogeography of the species. Neotropical Ichthyology 14(2): e150184; http://doi.org/10.1590/1982-0224-20150184

Simões, S.M., R.C. Costa & A. Fransozo (2010). Diel variation in abundance and size of the seabob shrimp Xiphopenaeus kroyeri (Crustacea, Penaeoidea) in the Ubatuba region, southeastern Brazil. Anais da Academia Brasileira de Ciências 82(2): 369–378; http://doi.org/10.1590/S0001-37652010000200013

Wetherbee, B.M. & E. Cortés (2004). Food consumption and feeding habits, pp. 223–244. In: Carrier, J.C., J.A. Musick & M.R. Heithaus (eds). Biology of Sharks and Their Relatives. CRC Press, Boca Raton, 596pp.