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Feeding strategy of the introduced Astronotus crassipinnis (Cichlidae) in upper Paraná river floodplain

Estratégia alimentar do introduzido Astronotus crassipinnis (Cichlidae) na planície de inundação do alto rio Paraná

ABSTRACT

The cichlid Astronotus crassipinnis (Heckel, 1840) known as “oscar” or “apaiari” is native to the Amazon basin and presents an omnivorous feeding habit, with a tendency to carnivory. The species was introduced in the upper Paraná River floodplain, where the trophic strategies adopted by the species are not well-known. The objective of this study was to characterize the diet of A. crassipinnis in different size classes to identify ontogenetic differences in diet composition and to determine its feeding behavior in the invaded floodplain. In addition, we experimentally compared the feeding behavior of A. crassipinnis with Hoplias sp. 2, a native piscivorous. We evaluated the predation rate of the two species with different prey (fish and shrimp). Astronotus crassipinnis consumed items from several trophic levels in the juvenile stage, characterizing an omnivore feeding. In the adult stage, A. crassipinnis displayed a specialist strategy in which fish and mollusks dominated the diet. Under controlled conditions, A. crassipinnis consumed more shrimp than Hoplias sp. 2. The preference for shrimp during the experiment contrasted to its feeding in natural environments, showing the potential trophic plasticity of A. crassipinnis. The piscivorous habit in the invaded environment can be considered a trophic strategy of A. crassipinnis, which feeds on an abundant resource in the upper Paraná River floodplain. In conclusion, the ontogenetic diet shifts and the trophic opportunism of the carnivore adults can be the strategies used by the species to invade and settle the floodplain. The piscivorous strategy of A. crassipinnis may impact fish biodiversity, altering ecosystem functioning.

KEYWORDS
Ontogenetic variations; diet; freshwater fish; predation behavior; upper Paraná River Floodplain

RESUMO

Astronotus crassipinnis (Heckel, 1840), conhecido como “oscar” ou “apaiari”, é nativo da bacia Amazônica e apresenta hábito alimentar onívoro, com tendência à carnivoria. A espécie foi introduzida na planície de inundação do alto rio Paraná, onde as estratégias tróficas adotadas pela espécie não são bem conhecidas. O objetivo deste estudo foi caracterizar a dieta de A. crassipinis em diferentes classes de comprimento para identificar diferenças ontogenéticas na composição da dieta e determinar seu comportamento alimentar na planície de inundação invadida. Em adição, nós comparamos experimentalmente o comportamento alimentar de A. crassipinnis com Hoplias sp. 2, um piscívoro nativo. Avaliamos a taxa de predação das duas espécies com presas diferentes (peixes e camarões). Astronotus crassipinnis consumiu itens de diferentes níveis tróficos no estágio juvenil, caracterizando uma alimentação onívora. No estágio adulto, A. crassipinnis apresentou uma estratégia especialista em que peixes e moluscos dominaram a dieta. Em condições controladas, A. crassipinnis consumiu mais camarões que Hoplias sp. 2. A preferência por camarão durante o experimento em contraste com sua alimentação em ambientes naturais evidencia a alta plasticidade trófica de A. crassipinnis. O hábito piscívoro no ambiente invadido pode ser considerado uma estratégia trófica de A. crassipinnis, que se alimenta de um recurso abundante na planície do alto Rio Paraná. Em conclusão, as mudanças ontogenéticas na dieta e o oportunismo trófico dos adultos podem ser as estratégias utilizadas pela espécie para invadir e colonizar a planície de inundação. A estratégia piscívora de A. crassipinnis pode impactar a biodiversidade de peixes, alterando o funcionamento do ecossistema.

PALAVRAS-CHAVE
Variação ontogenética; dieta; peixes de água doce; comportamento de predação; planície de inundação do alto Rio Paraná

The introduction of freshwater fish species is amongst the major threats to aquatic biodiversity (Dudgeon et al., 2006Dudgeon, D.; Arthington, A. H.; Gessner, M. O.; Kawabata, Z.; Knowler, D. J.; Lévêque, C.; Naiman, R. J.; Prieur-Richard, A. H.; Soto, D.; Stiassny, M. L. J. & Sullivan, C. A. 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81(2):163-182.; Olden et al., 2010Olden, J. D.; Kennard, M. J.; Leprieur, F.; Tedesco, P. A.; Winemiller, K. O. & Garcia-Berthou, E. 2010. Conservation biogeography of freshwater fishes: recent progress and future challenges. Diversity and Distribution 16(3):496-513.; Vitule et al., 2017Vitule, J. R. S.; Agostinho, A. A.; Azevedo-Santos, V. M.; Daga, V. S.; Darwall, W. R. T.; Fitzgerald, D. B.; Padial, A. A.; Pelicice, F. M.; Petrere Jr, M.; Pompeu, P. S. & Winemiller, K. O. 2017. We need better understanding about functional diversity and vulnerability of tropical freshwater fishes. Biodiversity and Conservation 26:757-762.). The success of invasion is commonly determined by the isolated and synergetic effects of several factors, such as low local species richness (Elton, 1958Elton, C. S. 1958. The ecology of invasions by animals and plants. London, Methuen. 196p.; Fitzgerald et al., 2016Fitzgerald, D. B.; Tobler, M. & Winemiller, K. O. 2016. From richer to poorer successful invasion by freshwater depends on species richness of donor and recipient basins. Global Change Biology 22(7):2440-2450.), local characteristics of the recipient river basin (Duncan et al., 2003Duncan, R. P.; Blackburn, T. M. & Sol, D. 2003. The ecology of bird introductions. Annual Review of Ecology, Evolution, and Systematics 34:71-98.), global changes (Dukes & Mooney, 1999Dukes, J. S. & Mooney, H. A. 1999. Does global change increase the success of biological invaders? Trends Ecology and Evolution 14(4):135-139.; Hellmann et al., 2008Hellmann, J. J.; Byers, J. E.; Bierwagen, B. G.; & Dukes, J. S. 2008. Five potential consequences of climate change for invasive species. Conservation Biology 22(3):534-543.), propagules pressure (Vitule et al., 2009Vitule, J. R. S.; Freire, C. A. & Simberloff, D. 2009. Introduction of nonnative freshwater fish can certainly be bad. Fish and Fisheries 10:98-108.), facilitation for establishment provided by other invasive species (Invasional Meltdown; Simberloff & Von Holle, 1999Simberloff, D. & Von Holle, B. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasion 1:21-32.; Ricciardi, 2001Ricciardi, A. 2001. Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Canadian Journal of Fisheries and Aquatic Science 58:2513-2525.) and the biological traits of the invasive species (Kolar & Lodge, 2002Kolar, C. S. & Lodge, D. M. 2002. Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233-1236.).

The recognition of invasive fish traits allows predicting their potential impacts on the structure and functioning of a native community (Comte et al., 2017Comte, L.; Cucherousset, J. & Olden, J. O. 2017. Global test of Eltonian niche conservatism of nonnative freshwater fish species between their native and introduced ranges. Ecography 40(3):384-392.). Among such traits are those that facilitate dispersion (e.g., ability to overcome natural barriers, high fecundity, and high survival rates of eggs and larvae) and population growth (e.g., high growth rates, high competitive ability; Catford et al., 2009Catford, J. A.; Jansson, R. & Nilsson, C. 2009. Reducing redundancy in invasion ecology by integrating hypothesis into a single theoretical framework. Diversity and Distribution 15:22-40.; Côté et al., 2013Côté, I. M.; Green, S. J. & Hixon, M. A. 2013. Predatory fish invaders: Insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biological Conservation 164:50-61.). Moreover, the feeding strategy is a key mechanism that facilitates growth and may increase the invasion success of a species (Bohn et al., 2004Bohn, T.; Sandlund, O. T.; Amundsen, P. A. & Primicerio, R. 2004. Rapidly changing life history during invasion. Oikos 106:138-150.; Ruesink, 2005Ruesink, J. L. 2005. Global analysis of factors affecting the outcome of freshwater fish introductions. Conservation Biology 19:1883-1893. ; Tonella et al., 2017Tonella, L. H.; Fugi, R.; Vitorino Jr, O. B.; Suzuki, H. I.; Gomes, L. C. & Agostinho, A. A. 2017. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817:239-252.).

In the invaded environment, invasive species may consume the same food resources that they consumed in their native environment. However, some species can adjust their diet to consume different resources available in the new area (Hahn & Fugi, 2008Hahn, N. S. & Fugi, R. 2008. Environmental changes, habitat modifications and feeding ecology of freshwater fish. In: Cyrino, J. E. P.; Bureau, D. P. & Kapoor, B. G. eds. Feeding and Digestive Functions of Fishes. Enfield, Science Publishers, p.35-65.), using this feeding strategy to establish in the new environment. During invasion processes, trophic generalists are favored over specialists who demonstrate a more limited ability to explore different resources (Hahn & Fugi, 2008Hahn, N. S. & Fugi, R. 2008. Environmental changes, habitat modifications and feeding ecology of freshwater fish. In: Cyrino, J. E. P.; Bureau, D. P. & Kapoor, B. G. eds. Feeding and Digestive Functions of Fishes. Enfield, Science Publishers, p.35-65.). Species with omnivorous feeding habitats have high trophic plasticity and can adjust their diet according to the local availability of food resources (Gerking, 1994Gerking, S. D. 1994. Feeding Ecology of Fish. San Diego, Academic Press. 416p.).

Piscivorous fish are specialists and generally do not change their diets (Hahn & Fugi, 2008Hahn, N. S. & Fugi, R. 2008. Environmental changes, habitat modifications and feeding ecology of freshwater fish. In: Cyrino, J. E. P.; Bureau, D. P. & Kapoor, B. G. eds. Feeding and Digestive Functions of Fishes. Enfield, Science Publishers, p.35-65.). Specialist feeders are favored only if their primary resources are abundant in the invaded environment (Agostinho et al., 2015Agostinho, A. A.; Suzuki, H. I.; Fugi, R.; Alves, D. C.; Tonella, L. H. & Espindola, L. A. 2015. Ecological and life history traits of Hemiodus orthonops in the invasion process: looking for clues at home. Hydrobiologia 746:415-430.; Pereira et al., 2016Pereira, L. S.; Agostinho, A. A. & Delariva, R. L. 2016. Effects of river damming in Neotropical piscivorous and omnivorous fish: feeding, body condition and abundances. Neotropical Ichthyology 14(1):e150044.; Tonella et al., 2017Tonella, L. H.; Fugi, R.; Vitorino Jr, O. B.; Suzuki, H. I.; Gomes, L. C. & Agostinho, A. A. 2017. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817:239-252.). An additional mechanism for successful invasion is ontogenetic shifts in food preferences, that reduces intraspecific competition as immature individuals eat different food types than adults (Sánchez-Hernándes et al. 2019Sánchez-Hernández, J.; Nunn, A. D.; Adams, C. E. & Amundsen, P. A. 2019. Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models. Biological Reviews 94:539-554.; Alves et al., 2021Alves, G. H. Z.; Figueiredo, B. R. S.; Manetta, G. I. & Benedito, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências 93(4):e20190868.).

The cichlid Astronotus crassipinnis (Heckel, 1840), known as “oscar” or “apaiari”, is native to the Amazon basin and its distribution is restricted to the southwestern portion of the basin (Kullander, 2003Kullander, S. O. 2003. Family Cichlidae (Cichlids). In: Reis, R. E. & Kullander, S. O. & Ferraris Jr, C. J. eds. Check list of the freshwater fishes of South and Central America. Porto Alegre, Edipucs, p. 291-309. ). The species was introduced in the upper Paraná River floodplain by aquaculture and fish farming (Ortega et al., 2015Ortega, J. C. G.; Júlio Junior, H. F.; Gomes. L. C. & Agostinho, A. A. 2015. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746(1):147-158.) in the late 90s (Ota et al., 2018Ota, R. R.; Deprá, G. C.; Graça, W. J. & Pavanelli, C. S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotropical Ichthyology 16(2):e170094.). Previous studies have categorized its feeding strategy as piscivorous in the floodplain (Hahn et al., 2004Hahn, N. S.; Fugi, R. & Andrian, I. F. 2004. Trophic ecology of the fish assemblages. In: Thomaz, S. M.; Agostinho, A. A. & Hahn, N. S. eds. The Upper Paraná River and its Floodplain: physical aspects, ecology and conservation. Leiden, Backhuys Publishers, p. 247-269.; Abujanra et al., 2009Abujanra, F.; Agostinho, A. A. & Hahn, N. S. 2009. Effects of the flood regime on the body condition of fish of different trophic guilds in the Upper Paraná River floodplain. Brazilian Journal Biology 69(2, Suppl.):469-479.), but without evaluating its diet. On the other hand, A. crassipinnis was categorized as omnivorous with a carnivorous tendency in the Amazon and the São Francisco basins, feeding mainly on small fish and shrimps (Rebelo et al., 2010Rebelo, S. R. M.; Freitas, C. E. C. F. & Soares, M. G. M. 2010. Fish diet from Manacapuru Big Lake complex (Amazon): an approach starting from the traditional knowledge. Biota Neotropica 10(3).; Costa et al., 2018Costa, L. X.; Maciel Junior, L.; Silva, J. C.; Nascimento, L. S. & Maciel, C. M. R. R. 2018. Anatomia funcional do aparelho digestório e conteúdo estomacal de Astronotus crassipinnis (Perciformes, Cichlidae). Enciclopédia Biosfera 15(28):965-976.). Furthermore, the congeneric Astronotus ocellatus (Cuvier, 1829) displays a carnivorous diet, consuming a large amount of fish (Santos et al., 2009Santos, G. M.; Ferreira, E. J. G.; & Zuanon, J. A. S. 2009. Peixes comerciais de Manaus. Manaus, INPA. 144p.; Trindade & Queiroz, 2012Trindade, M. E. J. & Queiroz, H. L. 2012. Feeding ecology and morphometry of the digestive tract of Astronotus ocellatus. Uakari 8(1):45-57.).

Given the lack of empirical information on its local diet, this study aimed to characterize the diet of introduced A. crassipinnis in the upper Paraná River floodplain and identify potential ontogenetic shifts. We also experimentally compared its feeding behavior with Hoplias sp. 2 (sensuOta et al., 2018Ota, R. R.; Deprá, G. C.; Graça, W. J. & Pavanelli, C. S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotropical Ichthyology 16(2):e170094.), a native piscivorous (Pereira et al., 2017aPereira, L. S; Tencatt, L. F. C.; Dias, R. M.; Oliveira, A. G. & Agostinho, A. A. 2017a. Effects of long and short flooding years on the feeding ecology of piscivorous fish in floodplain river systems. Hydrobiologia 795(1):65-80.,bPereira, L. S.; Mise, F. T.; Tencatt, L. F. C.; Baumgartner, M. T. & Agostinho, A. A. 2017b. Is coexistence between non-native and native Erythrinidae species mediated by niche differentiation or environmental filtering? A case study in the upper Paraná River floodplain. Neotropical Ichthyology 15(2):e160142.). The objective here was to confirm if piscivory is a feeding strategy of A. crassipinnis in the invaded environment and to evaluate how plastic the diet of both species could be in front of other prey than fish. In the experiment, we evaluated the predation rates of the two species for different prey (fish and shrimp). We expected that A. crassipinnis would be able to consume both types of prey in high amounts, which may contribute to its invasion success in the floodplain.

MATERIAL AND METHODS

Study area. The upper Paraná River floodplain (Fig. 1) is located downstream from the Engenheiro Sérgio Motta dam (locally known as Porto Primavera) and upstream from the Itaipu Reservoir. The study area is 230 km long, covers 5,268 km2, and represents the last remnant stretch of floodplain along the Brazilian section of the Paraná River (Agostinho et al., 2004Agostinho, A. A.; Gomes, L. C.; Thomaz, S. M. & Hahn, N. S. 2004. The Upper Paraná River and its floodplain: main characteristics and perspectives for management and conservation. In: Thomaz, S. M.; Agostinho, A. A. & Hahn, N. S. eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden, Backhuys Publishers, p. 381-393.). Its waterscape is formed by the main channel of the Paraná River, the channel of two major tributaries (Ivinhema and Baía), and many adjacent lakes, small tributaries, backwaters, and channels, configuring a highly heterogeneous environment (Agostinho et al., 2004Agostinho, A. A.; Gomes, L. C.; Thomaz, S. M. & Hahn, N. S. 2004. The Upper Paraná River and its floodplain: main characteristics and perspectives for management and conservation. In: Thomaz, S. M.; Agostinho, A. A. & Hahn, N. S. eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden, Backhuys Publishers, p. 381-393.).

Fig. 1.
Upper Paraná River floodplain with Nupelia field laboratory in detail.

Fish sampling and diet of Astronotus crassipinnis. We sampled individuals of A. crassipinnis quarterly from March 2000 to March 2016 in three main rivers (Ivinhema, Baia and Paraná) and adjacent lakes in the upper Paraná River floodplain, as a part of the Long-Term Ecological Research (LTER - research site 6). Fish were sampled with sets of 10 m long gillnets (24, 30, 40, 50, 60, 70, 80, 90, 100, 120, 140, and 160 mm meshes) installed perpendicularly to the margins for 24 h and checked every 8 hours. We measured the standard length (SL; cm) for each captured fish and visually determined their gonadal maturation stage (Vazzoler et al., 1996Vazzoler, A. E. A. M. 1996. Biologia da reprodução de peixes teleósteos: teoria e prática. Notas de estudo de Ciências Biológicas. Universidade Estadual Paulista - Unesp. 171p.). Individuals were separated into size classes (Class I = 0 - 10 cm, Class II = 11 - 19 cm, Class III = 20 - 30 cm). Class I corresponds to individuals in the juvenile stage and classes II - III in the adult stage. Stomachs with food contents were preserved in 4% formaldehyde for further laboratory analysis under a stereoscopic microscope. The identification of food items followed specific literature (e.g., McCafferty, 1983McCafferty, W. P. 1983. Aquatic Entomology. Boston, Jones & Barlett. 448p.; Pes et al., 2005Pes, A. M. O.; Hamada, N. & Nessimian, J. L. 2005. Chaves de identificação de larvas para famílias e gêneros de Trichoptera (Insecta) da Amazônia Central, Brasil. Revista Brasileira de Entomologia 49:181-204.; Graça & Pavanelli, 2007Graça, W. J. & Pavanelli, C. S. 2007. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Maringá, EDUEM. 241p.; Trivinho-Strixino, 2011Trivinho-Strixino, S. 2011. Larvas de Chironomidae: Guia de identificação. São Carlos , Departamento de Hidrobiologia, Laboratório de Entomologia Aquática da UFSCar.) and experts’ opinions for each group, and the items were classified to the lowest possible taxonomic level. For analysis, food items were grouped into the following categories: aquatic insects, terrestrial insects, microcrustaceans, other invertebrates, mollusks, fishes, plants, and detritus.

The diet composition was determined by analyzing stomach contents, and results were expressed following the volumetric percentage of the items (Hyslop, 1980Hyslop, E. J. 1980. Stomach contents analysis - a review of methods and their application. Journal of Fish Biology 17:411-429.). The volumetric percentage represents the volume of a given item over the total volume of all items recorded in the stomach contents. For smaller food items (e.g., insects, microcrustaceans, detritus) millimeter petri dishes with known depth were used, where the volume was obtained in mm3 and later converted to ml (Hellawel & Abel, 1971Hellawell, J. & Abel, R. 1971. A rapid volumetric method for the analysis of the food of fishes. Journal of fish Biology 3:29-37.). For larger food items (e.g., fish, shrimp) graduated test tubes with known liquid volume were used. After the insertion of each food item, the difference between the initial volume and the final volume caused by the displacement of the item in the test tubes was verified, indicating the volume in ml of the item.

To evaluate the differences in diet between size classes (factor) a resemblance matrix was generated based on the volume data matrix of the food items identified in the stomachs, using the Gower similarity coefficient (Gower, 1971Gower, J. C. 1971. A general coefficient of similarity and some of its properties. Biometrics 27(4):857-871.). Each individual was considered a replica within the matrix (lines), food items (columns), and the size classes was the factor. The differences were determined using the Permutational Analysis of Variance (PERMANOVA) applied to the resemblance matrix (Anderson et al., 2008Anderson, M. J.; Gorley, R. N. & Clarke, K. R. 2008. Permanova+ for Primer: Guide to software and statistical methods. Plymouth, Primer-e. 218p.). The patterns of similarity in diet composition were summarized for the size classes by a Principal Coordinates Analysis (PCoA; Gower, 1966Gower, J. C. 1966. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325-338.). Pearson’s correlations between each PCoA axis and the original variables (matrix of the food items) were performed to assess the association between food resources and PCoA axes. Correlations with r > 0.70 and significant p-value were considered. Significances were conducted using 4.999 Monte Carlo permutations (p < 0.05). Analyses were performed in the R environment (R Core Team, 2018) using package vegan (Oksanen et al., 2019Oksanen, J.; Blanchet, F. G.; Friendly, M.; Kindt, R.; Legendre, P.; McGlinn, D.; Minchin, P. R.; O’Hara, R. B.; Gavin, L.; Solymos, P.; Stevens, M. R. H.; Szoecs, E. & Wagner, H. 2019. vegan: Community Ecology Package. R package version 2.5-6 [Internet]. Available from: https://CRAN.R-project.org/package=vegan
https://CRAN.R-project.org/package=vegan...
).

Laboratory experiment. We conducted an experiment to evaluate the feeding strategy of the introduced A. crassipinnis compared to the native Hoplias sp. 2 (sensuOta et al., 2018Ota, R. R.; Deprá, G. C.; Graça, W. J. & Pavanelli, C. S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotropical Ichthyology 16(2):e170094.). This native species belongs to the Hoplias malabaricus group and it is currently being described since it has a well-defined morphotype (A. G. Bifi, unpubl. data). Hoplias sp. 2 is described as primarily piscivorous, with the diet dominated by fish and some consumption of insects, crustaceans, and plants (Pereira et al., 2017Pereira, L. S.; Mise, F. T.; Tencatt, L. F. C.; Baumgartner, M. T. & Agostinho, A. A. 2017b. Is coexistence between non-native and native Erythrinidae species mediated by niche differentiation or environmental filtering? A case study in the upper Paraná River floodplain. Neotropical Ichthyology 15(2):e160142.a,b).

Adults of A. crassipinnis (SL: 20.5 ± 1.09, n = 4) and Hoplias sp. 2 (SL: 18.23 cm ± 2.07, n = 4) were sampled using rods in Baía River (22°47’S, 53°22’W). Although both species co-occur in structured environments by macrophytes, they display different predatory behaviors. The introduced species is a diurnal, active predator and stays close to the surface, near or inside the macrophytes patches (Poulin et al., 1987Poulin, R.; Wolf, N. G. & Kramer, D. L. 1987. The effects of hypoxia on the vulnerability of guppies (Poecilia reticulata, Poecilliidae) to an aquatic predator (Astronotus ocellatus, Cichlidae). Environmental Biology of Fishes 20(4):285-292.). On the other hand, the native species is a nocturnal sit-and-wait ambush predator that often sits on the bottom facing upwards and waits for a prey to pounce abruptly (Figueiredo et al., 2018Figueiredo, B. R. S.; Fiori, L. F.; Keppeler, F. W.; Mormul, R. P. & Benedito, E. 2018. Non-lethal effects of a native and a non-native piscivorous fish on the interaction between a mesopredator and benthic and pelagic invertebrates. Aquatic Invasions 13(4):553-563.).

To perform as prey in the experiment, we used the small native Characidae Moenkhausia sanctaefilomenae Benine, Mariguela, Oliveira, 2009 (Total Length - TL: 3.34 ± 0.54 cm) and the introduced shrimp Macrobrachium amazonicum (Heller, 1862) (TL: 4.17 ± 0.58 cm), both dip netted from the same habitats as the predators. Both species are abundant in the floodplain and play important roles as prey for several fish. After capture, predators and prey were separately transported into 250 L flow-through tanks to acclimation to laboratory light (12 - 12 h day-light cycle) and temperature (air = 30°C and water = 27ºC) conditions for ten days (sensuPetry et al., 2007Petry, A. C.; Agostinho, A. A.; Piana, P. A. & Gomes, L. C. 2007. Effects of temperature on prey consumption and growth in mass of juvenile trahira Hoplias aff. malabaricus (Bloch, 1974). Journal of Fish Biology 70:1855-1864.) before running the experiment. Predators were fed with smaller fish to satiation during the first two days and then were left starving to standardize starvation time, while prey was daily fed with commercial pellets to satiation.

The experiment was performed at the research station “Base de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia)” from the State University of Maringá (UEM), municipality of Porto Rico, Paraná State, Brazil. The experiment was conducted in aerated aquariums (100 x 50 x 40 cm) filled with 200 L of river water and submerged macrophytes branches (Hydrilla verticillata (L.f.) Royle and Egeria najas Planch) to provide shelter and minimize stress. The back and both sides of each aquarium were covered with black fabric to prevent visual disturbance, while the front and right sides were left open to allow observation. Experimental conditions were the same during the acclimatization period.

At the beginning of the experiment, we added six prey species to the aquarium 30 minutes before predators, allowing prey to acclimatize. Each treatment corresponded to a shoal of either M. sanctaefilomenae or M. amazonicum with the same size class. After the acclimatization, predators were randomly added to the aquariums, and the trials were carried out for 24 h. There were four independent experimental units for each of the two predator treatments, totalizing eight experimental units for each prey species. Each predator was used only in a single experimental unit, and each shoal was exposed only to a single predator.

The number of consumed prey (response variable) was evaluated using generalized linear models fitted with a Binomial negative distribution, considering prey type and predator species (predictor variables). The significance of the deviance captured by the fixed variables was analyzed using a deviance analysis (Type II test). The analysis was performed in the R environment (R Development Core Team, 2018R Development Core Team. 2019. R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. Available from: http://www.R-project.org/.
http://www.R-project.org/...
) using packages car (Fox & Weisberg, 2011Fox, J. & Weisberg, S. 2011. An R Companion to Applied Regression. Newbury Park, Sage Publishing. 474p.) and MASS (Venables & Ripley, 2002Venables, W. N. & Ripley, B. D. 2002. Modern Applied Statistics with S, Fourth edition. New York, Springer. Available from: <http://www.stats.ox.ac.uk/pub/MASS4>.
http://www.stats.ox.ac.uk/pub/MASS4...
).

RESULTS

Diet of Astronotus crassipinnis. In 16 years of PELD monitoring, we sampled 612 individuals of A. crassipinnis, which 50 individuals with stomach contents (Class I = 3.7 - 4.6 cm; Class II = 13.5 - 19.5 cm; Class III = 20.0 - 27.0 cm) (Tab. I). The diet composition expressed by percentage volumetric (V%) suggested that individuals of Class I had their diet mostly based on aquatic insects (V% = 45.01%) and microcrustaceans (V% = 51.58%). Class II and III primarily consumed fish (V% = 40.68% and 35.64%, respectively) and mollusks (V% = 33.23% and 57.31%, respectively) (Tab. I).

Tab. I
Food item consumed by the size classes of Astronotus crassipinnis (Heckel, 1840) estimated by the values of volume (V%) of the food items in the upper Paraná River floodplain (N, number of individuals; n.i., not indentified). Values in bold represent the calculated metrics for the food categories.

PERMANOVA indicated a significant difference in the diet composition between size classes of A. crassipinnis (Pseudo-F = 6.02, p = 0.001). Class I differed from classes II (t = 8.93, p < 0.001) and III (t = 5.63; p = 0.001), and Class II differed from Class III, but with a lower effect size (t = 2.18, p = 0.002). In the PCoA, Chironomidae larvae (r = -0.80), Ostracoda (r = -0.80) and Ephemeroptera (r = -0.74) were the items that most explained the patterns in Axis 1 (Tab. II). However, there was no clear pattern in Axis 2 (Fig. 2). Differences accounted in the PERMANOVA are shown in PCoA (Fig. 2).

Tab. II.
Values of significant correlation of food items with the Principal Coordinate Analysis (PCoA) axes. *** p-value significant.

Fig. 2.
Ordination by principal coordinate analysis (PCoA) of the food items for the size classes of Astronotus crassipinnis (Heckel, 1840) along the upper Paraná River floodplain. Axis 1 separated the diet of Class I (spheres on the right) from the other two classes (square and diamond in the left, with little variability) (Chiro, Chironomidae larvae; Ostra, Ostracoda; Ephe, Ephemeroptera).

Laboratory experiment. The amount of consumed prey differed for the interaction of predator species and prey type (χ² = 6.67, p = 0.01). Astronotus crassipinnis predated less fish than Hoplias sp. 2 (Z = 2.67, p = 0.037), and the predation of shrimp among predators did not differ (Z = -0.59, p = 0.93). Astronotus crassipinnis predated, on average, four individual shrimps more than individual fish, and Hoplias sp. 2 predated, on average, three individual fish more than individual shrimps (Fig. 3). All individuals of Hoplias sp. 2 consumed fish, while the same did not occur for A. crassipinnis.

Fig. 3.
Boxplot of the predation rate of Astronotus crassipinnis (Heckel, 1840) (introduced species) and Hoplias sp. 2 (native species) in relation to prey type Moenkhausia sanctafilomenae (Steindachner, 1907) (Fish) and Macrobrachium amazonicum (Heller, 1862) (Shrimp).

DISCUSSION

The introduced species A. crassipinnis shows ontogenetic diet shift, with generalist feeding habit in juvenile stage and specialist habit in the adult stage in the upper Paraná River floodplain. Under experimental conditions, A. crassipinnis predated more shrimp than fish compared with the piscivorous native species (Hoplias sp. 2). The feeding preference of A. crassipinnis in experimental conditions corroborates with its diet in the native basin (Rebelo et al., 2010Rebelo, S. R. M.; Freitas, C. E. C. F. & Soares, M. G. M. 2010. Fish diet from Manacapuru Big Lake complex (Amazon): an approach starting from the traditional knowledge. Biota Neotropica 10(3).; Trindade & Queiroz, 2012Trindade, M. E. J. & Queiroz, H. L. 2012. Feeding ecology and morphometry of the digestive tract of Astronotus ocellatus. Uakari 8(1):45-57.). The piscivorous habit in the invaded environment can be considered a trophic strategy that facilitates the invasion of A. crassipinnis, which feeds on an abundant resource in the upper Paraná River floodplain.

In the juvenile stage (Class I), individuals consumed a wider variety of invertebrates. Ontogenetic diet shifts are well known in fishes (Wootton, 1999Wootton, R. J. 1999. Ecology of teleost fishes. Dordrecht, Kluwer Academic Publishers. 404p.; Amundsen et al., 2003Amundsen, P.; Bohn, T.; Popova, A. O.; Staldvik, F. J.; Reshetnikov, Y. S.; Kashulin, N. A. & Lukin, A. A. 2003. Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild. Hydrobiologia 497:109-119.;) and may reduce intraspecific competition through diet segregation (Canavero et al., 2013Canavero, A.; Hernández, D.; Zarucki, M. & Arim, M. 2013. Patterns of co-ocurrences in a killifish metacommunity are more related with body size than with species identity. Austral Ecology 39(4):455-461.; Alves et al., 2021Alves, G. H. Z.; Figueiredo, B. R. S.; Manetta, G. I. & Benedito, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências 93(4):e20190868.). The relative proportions of the body and other anatomical characteristics developed during growth are the key factors determining the type and food size that fish predators will prey on (Werner, 1974Werner, E. E. 1974. Fish size, prey size, handling time relation in several sunfishes and some implications. Journal of the Fisheries Research Board of Canada 31:1531-1536.; Keast, 1985Keast, A. 1985. Development of dietary specializations in a summer community of juvenile fishes. Environmental Biology of Fishes 13:211-224.; Scharf et al., 2000Scharf, F. S.; Juanes, F. & Rountree, R. A. 2000. Predator size-prey size relationships of marine fish predators: interspecific variation and effect of ontogeny and body size on trophic-niche breadth. Marine Ecology Progress Serie 208:229-248.; Huskey & Turingan, 2001Huskey, S. H. & Turingan, R. G. 2001. Variation in prey-resource utilization and oral jaw gape between two populations of largemouth bass, Micropterus salmoides. Environmental Biology of Fishes 61:185-194.). Juveniles have limited body size and mouth gape, determining the consumption of only small food (Schmitt & Holbrook, 1984Schmitt, R. J. & Holbrook, S. J. 1984. Gape-limitation, foraging tactis and prey size selectivity of two microcarnivorous species of fish. Oecologia 63:6-12.; King, 2005King, A. J. 2005. Ontogenetic dietary shifts of fishes in an Australian floodplain river. Marine Freshwater Research 56(2):215-225.). Also, the small size of the fish at this stage makes them highly vulnerable to predators, which may lead them to forage in smaller or protected areas and consume only the locally available resources as a defense against predators (Sánchez-Hernández et al., 2019Sánchez-Hernández, J.; Nunn, A. D.; Adams, C. E. & Amundsen, P. A. 2019. Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models. Biological Reviews 94:539-554.). The generalist feeding behavior in the juvenile stage and the tendency to consume low-trophic level prey, is considered a feature that contributes to the successful establishment of some invasive fish species (Koehn, 2004Koehn, J. D. 2004. Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshwater Biology 49(7):882-894.; Gido & Franssen, 2007Gido, K. B. & Franssen, N. R. 2007. Invasion of stream fishes into low trophic positions. Ecology of Freshwater Fish 16(3):457-464.; Alves et al., 2021Alves, G. H. Z.; Figueiredo, B. R. S.; Manetta, G. I. & Benedito, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências 93(4):e20190868.) because food resources do not become a limiting factor. Therefore, this characteristic of A. crassipinnis may be one that may have favored its establishment in the upper Paraná River floodplain. The same pattern was observed for Cichla kelberi Kullander, Ferreira, 2006 (Gomiero et al., 2010Gomiero, L. M.; Villares Junior, G. A. & Naous, F. 2010. Seasonal and ontogenetic variations in the diet of Cichla kelberi Kullander and Ferreira, 2006 introduced in an artificial lake in southeastern Brazil. Brazilian Journal Biology 70(4):1033-1037.) and Serrasalmus marginatus (Alves et al., 2021Alves, G. H. Z.; Figueiredo, B. R. S.; Manetta, G. I. & Benedito, E. 2021. Ontogenetic diet shifts: an additional mechanism for successful invasion of a piranha species in a Neotropical floodplain. Anais da Academia Brasileira de Ciências 93(4):e20190868.), two other piscivorous fish species introduced in the study area.

In the adult stage, A. crassipinnis shifts the intake to other items, such as fish and mollusks. Due to the high percentage of fish in their diet, in this study the species was classified as piscivorous in the upper Paraná River floodplain, just as it was proposed by Hahn et al. (2004Hahn, N. S.; Fugi, R. & Andrian, I. F. 2004. Trophic ecology of the fish assemblages. In: Thomaz, S. M.; Agostinho, A. A. & Hahn, N. S. eds. The Upper Paraná River and its Floodplain: physical aspects, ecology and conservation. Leiden, Backhuys Publishers, p. 247-269.) and Abujanra et al. (2009Abujanra, F.; Agostinho, A. A. & Hahn, N. S. 2009. Effects of the flood regime on the body condition of fish of different trophic guilds in the Upper Paraná River floodplain. Brazilian Journal Biology 69(2, Suppl.):469-479.). Thus, the omnivorous feeding habit of A. crassipinnis in the Amazon river basin (native; Rebelo et al., 2010Rebelo, S. R. M.; Freitas, C. E. C. F. & Soares, M. G. M. 2010. Fish diet from Manacapuru Big Lake complex (Amazon): an approach starting from the traditional knowledge. Biota Neotropica 10(3).; Trindade & Queiroz, 2012Trindade, M. E. J. & Queiroz, H. L. 2012. Feeding ecology and morphometry of the digestive tract of Astronotus ocellatus. Uakari 8(1):45-57.) and São Francisco river basin (invaded; Costa et al., 2018Costa, L. X.; Maciel Junior, L.; Silva, J. C.; Nascimento, L. S. & Maciel, C. M. R. R. 2018. Anatomia funcional do aparelho digestório e conteúdo estomacal de Astronotus crassipinnis (Perciformes, Cichlidae). Enciclopédia Biosfera 15(28):965-976.) displayed a shift in the upper Paraná River floodplain. Although we have evaluated large individuals of A. crassipinnis (20 to 27 cm in class III), class II individuals correspond to those evaluated in Costa et al. (2018Costa, L. X.; Maciel Junior, L.; Silva, J. C.; Nascimento, L. S. & Maciel, C. M. R. R. 2018. Anatomia funcional do aparelho digestório e conteúdo estomacal de Astronotus crassipinnis (Perciformes, Cichlidae). Enciclopédia Biosfera 15(28):965-976.), which also have high fish consumption. Many species have trophic plasticity and diet variation between different locations, depending on the abundance of the available resources (Abelha & Goulart, 2004Abelha, M. C. F. & Goulart, E. 2004. Oportunismo trófico de Geophagus brasiliensis (Quoy & Gaimard, 1824) (Osteichthyes, Cichlidae) no reservatório de Capivari, Estado do Paraná, Brasil. Acta Scientiarum, Biological Sciences 26(1):37-45.; Loureiro-Crippa & Hahn, 2006Loureiro-Crippa, V. E. & Hahn, N. S. 2006. Use of food resources by the fish fauna of a small reservoir (Rio Jordão, Brazil) before and shortly after its filling. Neotropical Ichthyology 4(3):357-362.; Gomiero & Braga, 2008Gomiero, L. M. & Braga, F. M. S. 2008. Feeding habits of the ichthyofauna in a protected area in the state of São Paulo, southeastern Brazil. Biota Neotropica 8(1):41-47.; Tonella et al., 2017Tonella, L. H.; Fugi, R.; Vitorino Jr, O. B.; Suzuki, H. I.; Gomes, L. C. & Agostinho, A. A. 2017. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817:239-252., Malpica-Cruz et al., 2019Malpica-Cruz, L.; Green, S. J. & Côté, I. M. 2019. Temporal and ontogenetic changes in the trophic signature of an invasive marine predator. Hydrobiologia 839:71-86.).

The preference for shrimps displayed by A. crassipinnis under experimental conditions was similar to its diet in the native environment, favored by morphological features, such as mouth size and intestine shape (Costa et al., 2018Costa, L. X.; Maciel Junior, L.; Silva, J. C.; Nascimento, L. S. & Maciel, C. M. R. R. 2018. Anatomia funcional do aparelho digestório e conteúdo estomacal de Astronotus crassipinnis (Perciformes, Cichlidae). Enciclopédia Biosfera 15(28):965-976.). The behavior of predators and prey may have favored this consumption. The predator A. crassipinnis has a benthopelagic habit (Froese & Pauly, 2019Froese, R. & Pauly, D. 2019. FishBase. World Wide Web electronic publication [Internet]. Available from: http://www.fishbase.org
http://www.fishbase.org...
), similar to that of prey. Also, its foraging behavior is pursuing, and the shrimp swimming slower compared to the fish M. sanctaefilomenae (Felipe et al., 2009Felipe, T. R. A.; Súarez, Y. R. & Antonialli Junior, W. F. 2009. The social organization of fish schools: antipredator responses of Moenkhausia sanctaefilomenae (Characidae, Tetragonopterinae) under simulated predation in the laboratory. Sociobiology 54(1):275-281.). Then, predators prefer to consume the prey requiring less energy to be captured (MacArthur & Pianka, 1966MacArthur, R. H. & Pianka, E. R. 1966. On optimal use of a patchy environment. The American Naturalist 100(916):603-609.). In contrast, Hoplias sp. 2 has characteristics that may have disadvantages in shrimp predation, as a benthic habit, foraging behavior sit-and-wait (Winemiller, 1989Winemiller, K. O. 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environmental Biology of Fishes 26:177-199.; Pereira et al., 2017bPereira, L. S.; Mise, F. T.; Tencatt, L. F. C.; Baumgartner, M. T. & Agostinho, A. A. 2017b. Is coexistence between non-native and native Erythrinidae species mediated by niche differentiation or environmental filtering? A case study in the upper Paraná River floodplain. Neotropical Ichthyology 15(2):e160142.), and the reduced trophic plasticity. Some piscivorous fishes, commonly considered specialists, can exhibit some feeding plasticity by including invertebrates in their diets (Pereira et al., 2017aPereira, L. S; Tencatt, L. F. C.; Dias, R. M.; Oliveira, A. G. & Agostinho, A. A. 2017a. Effects of long and short flooding years on the feeding ecology of piscivorous fish in floodplain river systems. Hydrobiologia 795(1):65-80.). The optimal foraging theory postulates that fishes should feed on prey that maximizes their energy gain (Gerking, 1994Gerking, S. D. 1994. Feeding Ecology of Fish. San Diego, Academic Press. 416p.). Thus, the consumption of invertebrates would be higher when prey fishes are not available or demand a high energetic cost for foraging (Pereira et al., 2017aPereira, L. S; Tencatt, L. F. C.; Dias, R. M.; Oliveira, A. G. & Agostinho, A. A. 2017a. Effects of long and short flooding years on the feeding ecology of piscivorous fish in floodplain river systems. Hydrobiologia 795(1):65-80.).

Therefore, the preference for shrimp in the experiment and the omnivory in the native environment (Rebelo et al., 2010Rebelo, S. R. M.; Freitas, C. E. C. F. & Soares, M. G. M. 2010. Fish diet from Manacapuru Big Lake complex (Amazon): an approach starting from the traditional knowledge. Biota Neotropica 10(3).; Trindade & Queiroz, 2012Trindade, M. E. J. & Queiroz, H. L. 2012. Feeding ecology and morphometry of the digestive tract of Astronotus ocellatus. Uakari 8(1):45-57.) suggests that the piscivory of A. crassipinnis adults in the upper Paraná River floodplain is context dependent. In this invaded environment, the species might be adopting a feeding strategy of consuming an abundant resource. In addition, the species lives amid aquatic macrophytes, a place of refuge for small fishes (Lopes et al., 2015Lopes, T. M.; Cunha, E. R.; Silva, J. C. B.; Behrend, R. D. L. & Gomes, L. C. 2015. Dense macrophytes influence the horizontal distribution of fish in floodplain lakes. Environmental Biology of Fishes 98: 1741-1755.) and where it does not have piscivore competitors (Gomes et al., 2012Gomes, L. C.; Bulla, C. K. C.; Agostinho, A. A.; Vasconcelos, L. P. & Miranda, L. E. 2012. Fish assemblage dynamics in a Neotropical floodplain relative to aquatic macrophytes and the homogenizing effects of a flood pulse. Hydrobiologia 685:97-107.). In this floodplain, the piscivorous habit favored some invasive species even in the presence of native piscivores due to the high abundance of this food resource (Pereira et al., 2015Pereira, L. S.; Agostinho, A. A. & Gomes, L. C. 2015. Eating the competitor: a mechanism of invasion. Hydrobiologia 746:223-231.).

In summary, our study combining data obtained from fish in the natural environment and experimental data demonstrated that the introduced species A. crassipinnis can use two mechanisms to invade and establish in the upper Paraná River floodplain. The generalist (omnivorous) feeding habit in the juvenile stage associated with the parental care characteristic of this species (Suzuki et al., 2004Suzuki, H. I.; Vazzoler, A. E. M. A.; Marques, E. E.; Lizama, M. A. P. & Inada, P. 2004. Reproductive Ecology of the fish assemblages. In: Thomaz, S. M.; Agostinho, A. A. & Hahn, N. S. eds. The Upper Paraná River and its floodplain: Physical aspects, ecology and conservation. Leiden, Backhuys Publishers, p. 271-292. ) can maximize their survival in the initial development stages. In the adult stage, the species has a specialist (piscivorous) but opportunistic behavior, as it may alter their feeding habits to take advantage of an abundant resource (fishes and mollusks) in the invaded area. We encourage further studies of the biology of A. crassipinnis and experimental studies to assess its invasiveness, potential impacts on the native community of this region, and the associations with other invasive species.

Acknowledgments

We are grateful to Valmir A. Capatti, Ragna W. Tavares, Herick Santana, Valmir A. Teixeira and Sebastião Rodrigues for field assistance; Angelo A. Agostinho, Pitágoras Piana, Norma Hahn, and Lisiane Hahn for insightful comments on the initial manuscript version. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES/ PROEX) - Finance Code 001 (scholarships awarded to TML and funding to research), and Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (logistical support).

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Publication Dates

  • Publication in this collection
    25 Feb 2022
  • Date of issue
    2022

History

  • Received
    05 Mar 2021
  • Accepted
    12 Nov 2021
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