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Foraging Behavior Interactions Between the Invasive Nile Tilapia (Cichliformes: Cichlidae) and Three Large Native Predators

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Foraging Behavior Interactions Between the Invasive Nile Tilapia (Cichliformes: Cichlidae) and Three Large Native Predators Neotropical Ichthyology, 17(3): e180116, 2019 Journal homepage: www.scielo.br/ni DOI: 10.1590/1982-0224-20180116 Published online: 30 September 2019 (ISSN 1982-0224) Copyright © 2019 Sociedade Brasileira de Ictiologia Printed: 30 September 2019 (ISSN 1679-6225) Original article Foraging behavior interactions between the invasive Nile Tilapia (Cichliformes: Cichlidae) and three large native predators Tiago Birck1, Hugo José Message1,2, Gilmar Baumgartner2,3, Nyamien Yahaut Sebastien1,2 and Dirceu Baumgartner1,2 The predator-prey relationships between juvenile Nile Tilapia Oreochromis niloticus and native fish species of the Paraná River basin, Brazil, were experimentally examined. Juveniles of O. niloticus were offered to three native predator species (Salminus brasiliensis, Pseudoplatystoma corruscans, and Brycon orbignyanus) in 2,000-L tanks with four levels of habitat complexity (0%, 50%, 100% and RD (rocks and driftwood)). Predator efficiency was more variable among species (S. brasiliensis consumed 86.6% of the prey, P. corruscans 22.5% and B. orbignyanus 18.3%) than among levels of habitat complexity, and S. brasiliensis was faster than the others in detecting and consuming the prey. The higher predatory efficiency observed for S. brasiliensis can be partially explained by its more aggressive behavior (it fed earlier and for longer) and its presence in the surface layer. Here, the presence of predators led to O. niloticus juveniles spending more time at the surface or remaining in schools to coexist at the bottom with the predators, as expected for cichlids under predatory pressure in natural environments. Our results suggest that preserving and restoring populations of S. brasiliensis (and also to some extent P. corruscans and B. orbignyanus) might help to control O. niloticus in the Paraná River basin. Keywords: Invasion, Management, Oreochromis niloticus, Predation, Prey. As relações predador-presa entre alevinos de Tilápia-do-Nilo Oreochromis niloticus e espécies de peixes nativos da bacia do rio Paraná, Brasil, foram examinadas experimentalmente. Dez alevinos de O. niloticus foram oferecidos a três espécies nativas de predadores (Salminus brasiliensis, Pseudoplatystoma corruscans e Brycon orbignyanus) em tanques de 2000L com quatro níveis de complexidade ambiental (0%, 50%, 100% e RD (rochas e galhos)). A eficiência predatória foi mais variável entre espécies (S. brasiliensis consumiu 86,6%, P. corruscans 22,5% e B. orbignyanus 18,3% dos alevinos) do que para complexidade ambiental, e S. brasiliensis foi mais rápido do que os outros em detectar e consumir a presa. A eficiência predatória de S. brasiliensis pode ser parcialmente explicada pelo seu comportamento mais agressivo (alimentou-se mais cedo e por mais tempo de experimento) e pela presença na área de superfície. A presença de predadores levou os alevinos de O. niloticus a passar mais tempo na superfície ou formar cardume para coexistir no fundo com os predadores, como o esperado para ciclídeos sob pressão predatória no campo. Nossos resultados sugerem que preservar e restaurar as populações de S. brasiliensis (principalmente, mas também P. corruscans e B. orbignyanus) podem ajudar no controle de O. niloticus na bacia do rio Paraná. Palavras-chave: Invasão, Manejo, Oreochromis niloticus, Predação, Presa. Introduction Daga et al., 2016; Agostinho et al., 2018) and, against this backdrop, there is the paradigmatic issue that biological Aquaculture is an important economic activity; however, invasions are a major cause of biodiversity loss (Dirzo et al., it is also a major pathway for the introduction of aquatic 2014). Non-native species may prey upon native species or non-native species (Naylor et al., 2001; Ortega et al., 2015; compete with them, catalyze ecosystem alteration and biotic Padial et al., 2017; Alves et al., 2018). Escapes from fish homogenization (Olden, Poff, 2004), spread diseases, cause farms and invasions of non-native aquatic species into the reductions in wild stocks, (e.g., Latini, Petrere Júnior, 2004) wild are frequently associated with ecological and economic and decrease the economic value of rivers and lakes (Pimentel damages (Chandra, Gerhardt, 2008; Leprieur et al., 2008; et al., 2005; Ellender, Weyl, 2014; Lima et al., 2018). 1Programa de Pós-Graduação em Ciências Ambientais, Universidade Estadual do Oeste do Paraná, R. da Faculdade, 645 - Jardim La Salle, 85903-000 Toledo, PR, Brazil. (TB) [email protected], https://orcid.org/0000-0002-1042-4697; (HJM) [email protected], https://orcid.org/0000-0002-6031-8577 (corresponding author). 2Grupo de Pesquisas em Recursos Pesqueiros e Limnologia (Gerpel), Universidade Estadual do Oeste do Paraná, Toledo, Paraná, Brazil. (NYS) [email protected], https://orcid.org/0000-0002-5288-7593; (DB) [email protected], https://orcid.org/0000-0001-9943-6290. 3Programa de Pós-Graduação em Recursos Pesqueiros e Engenharia de Pesca, Universidade Estadual do Oeste do Paraná, Toledo, Paraná, Brazil. (GB) [email protected], https://orcid.org/0000-0003-0912-482X. e180116[1] Neotropical Ichthyology, 17(3): e180116, 2019 2 Oreochromis niloticus versus native predators There is some evidence that the Nile Tilapia gaps (the remaining issues listed above) in knowledge of Oreochromis niloticus (Linnaeus, 1758), introduced the Nile Tilapia as an invasive species, this study aimed for aquaculture purposes, has established populations to assess the predatory behavior of dourado, Salminus worldwide outside its native ranges and become invasive brasiliensis (Cuvier, 1816), pintado, Pseudoplatystoma (Lowe et al., 2000; Naylor et al., 2001; Vicente, Fonseca- corruscans (Spix, Agassiz, 1829) and piracanjuba, Brycon Alves, 2013; Padial et al., 2017). The negative effects orbignyanus (Valenciennes, 1850), on Nile Tilapia under of Nile Tilapia invasions on native biodiversity (Ogutu- standardized laboratory conditions, together with the Ohwayo, 1990; Canonico et al., 2005), on the ecosystem behavioral interactions between the non-native and native services (Vitule, 2009; Vitule et al., 2009; Njiru et al., species. This study comprised four parts: 1) investigation 2010) and on ecosystem features (Zaret, Paine, 1973; of the time required to start prey consumption and the Attayde et al., 2007), are well documented, and follow feeding rates over time, 2) predatory efficiency trials, expected patterns of biological invasions in aquatic 3) investigation of the behavior of the native predators ecosystems (Mollot et al., 2017; Agostinho et al., and the Nile Tilapia and 4) investigation of the use of 2018). However, whereas we know that the Nile Tilapia microhabitats by native predators and Nile Tilapia. The is a very invasive species, the interaction with native following hypotheses were tested: (i) the Nile Tilapia is predators, which may possibly feed on Nile Tilapia, preyed upon by each species of native predator and (ii) remains unknown. In summary, the following questions the level of habitat complexity has an influence on the remain unanswered: whether native predators consume behavior of native predators and Nile Tilapia. Hence, we Nile Tilapia, under what environmental conditions this aimed to assess whether the native predators’ behavior occurs and, finally, whether native predators are capable and the habitat complexity could reveal their potential to of reducing the effects of Nile Tilapia invasion. Our study control the Nile Tilapia, which are invasive in the Paraná aimed to answer these questions. River basin. The Nile Tilapia, Oreochromis niloticus, is an omnivorous species native to northern and eastern Africa. Material and Methods Oreochromis niloticus is one of the top ten species in the world (Lowe et al., 2000; Picker, Griffiths, 2011) most Experimental procedures and design. Juveniles of Nile frequently introduced through aquaculture. The rearing of Tilapia, Oreochromis niloticus, and adults of Salminus Nile Tilapia can be traced back to ancient Egyptian times brasiliensis, Pseudoplatystoma corruscans, and Brycon (4,000 years ago), and the species was first introduced to orbignyanus, were obtained from local fish farms. These African countries in the 1940s and 1950s and to Asian native predator species were selected for testing because and South, Central and North American countries in the they are abundant in areas where Nile Tilapia escapes have 1960s and 1970s. Market development and processing been observed (Buitrago-Suaréz, Burr, 2007; Lima, 2007; advances have led to a rapid expansion of the cultured Daga et al., 2016), giving rise to the inference that they Nile Tilapia since the mid-1980s. Oreochromis niloticus might prey upon Nile Tilapia. All animals were transferred is the most cultivated fish species in the world (FAO, to the wet laboratory at the Instituto de Pesquisas em 2016) due to their desirable features for aquaculture, Aquicultura Ambiental (InPAA), Universidade Estadual including rapid growth rates, high feed conversion rates, do Oeste do Paraná (UNIOESTE), Toledo campus, in high disease resistance at high densities and high market Paraná State, for acclimatization and use in laboratory acceptability (Welcomme, 1967; Hassanien et al., 2004). experiments. Conspecific individuals were kept together Nevertheless, the same characteristics that increased for acclimatization in 2,000-L circular tanks for 15 days interest in the Nile Tilapia for aquaculture are responsible before the experiment started. During this period, the fish for turning this species into a potentially
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