Advertisement

Trophic shifts in a native predator following the introduction of a top predator in a tropical lake

  • Marisol P. ValverdeEmail author
  • Diana M. T. Sharpe
  • Mark E. Torchin
  • David G. Buck
  • Lauren J. Chapman
Original Paper
  • 52 Downloads

Abstract

Some of the most dramatic and well-studied impacts of introduced predators involve their ecological effects on native prey communities. However, how native predators respond to introduced predators has received less attention. Here, we examined the potential impacts of an introduced predatory fish (Cichla monoculus, the peacock bass) on the diet and trophic ecology of a native predator (Hoplias microlepis) in Lake Gatun, Panama. We used stomach content analysis and stable isotope analysis to quantify the dietary niche of both species in sympatry, and of the native predator in the presence vs. absence of the peacock bass. We found that in the presence of the peacock bass, H. microlepis had a more diverse diet and a wider (five-fold) isotopic niche, relative to where it occurred alone. Specifically, H. microlepis, which were predominantly piscivorous in the absence of peacock bass, broadened their diet in the invaded Lake Gatun to include invertebrates and scavenged fish, the latter comprising 26% of its diet. Scavenged fish consisted of C. monoculus and Oreochromis niloticus (Nile tilapia) remains, both heavily harvested, non-native species in Lake Gatun, whose scraps are often thrown back into the lake by fishers. We suspect that these human-mediated food subsidies may lead to indirect facilitative interactions between introduced and native species in this system.

Keywords

Invasive species Lake Gatun Cichla monoculus Competition Facilitation Human food subsidies 

Notes

Acknowledgements

We would like to thank V. Bravo, R. González, C. Schloeder and J. Pereira for their invaluable field and laboratory assistance. We are grateful to the fishing communities of Cuipo, Gamboa, La Laguna, Emberá-Wounan, and Bayano for their extraordinary help in the field. We would also like to thank the staff in STRI’s Naos Laboratories, particularly C. Bonilla, for their logistical support. We thank the Associate Editor and two anonymous reviewers whose constructive feedback greatly improved this manuscript. This work was supported by CONACyT (Consejo Nacional de Ciencia y Tecnología, M.Sc. Fellowship to MPV), McGill University Department of Biology (NEO/BESS programs), Quebec Center for Biodiversity Science (QCBS, Excellence Award to MPV), STRI (Smithsonian Tropical Research Institute), and Canada Research Chair funds to LJC.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals

Our field sampling and handling of live organisms complied with Panama’s Ministerio del Ambiente (Permit # SE/AP-40-15) and STRI’s Institutional Animal Care Committee (Protocol # 2016-0224-2019).

Supplementary material

10530_2019_2119_MOESM1_ESM.docx (1.6 mb)
Supplementary material 1 (DOCX 1629 kb)

References

  1. Angermeier PL, Karr JR (1983) Fish communities along environmental gradients in a system of tropical streams. Environ Biol Fishes 9:117–135CrossRefGoogle Scholar
  2. Anson JR, Dickman CR, Boonstra R, Jessop TS (2013) Stress triangle: do introduced predators exert indirect costs on native predators and prey? PLoS ONE 8:e60916PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bacheler N, Neal J, Noble R (2004) Diet overlap between native bigmouth sleepers (Gobiomorus dormitor) and introduced predatory fishes in a Puerto Rico reservoir. Ecol Freshw Fish 13:111–118CrossRefGoogle Scholar
  4. Bøhn T, Amundsen PA (2001) The competitive edge of an invading specialist. Ecology 82:2150–2163CrossRefGoogle Scholar
  5. Bøhn T, Amundsen PA, Sparrow A (2008) Competitive exclusion after invasion? Biol Invasions 10:359–368CrossRefGoogle Scholar
  6. Busacker GP, Adelman IR, Goolish EM (1990) Growth. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 363–387Google Scholar
  7. Bussing WA (1998) Freshwater fishes of Costa Rica. Editorial Universidad de Costa Rica, San JoséGoogle Scholar
  8. Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci 93:10844–10847PubMedCrossRefGoogle Scholar
  9. Capra L, Bennemann S (2009) Low feeding overlap between Plagioscion squamosissimus (Heckel, 1840) and Cichla monoculus (Spix & Agassiz, 1831), fishes introduced in tropical reservoir of South Brazil. Acta Limnol Bras 21:343–348Google Scholar
  10. Carvalho LN, Fernandes CHV, Moreira VSS (2009) Alimentação de Hoplias malabaricus (Bloch, 1794)(Osteichthyes, Erythrinidae) no rio Vermelho, Pantanal Sul Mato-Grossense. Revista Brasileira de Zoociências 4:227–236Google Scholar
  11. Clavel J, Julliard R, Devictor V (2011) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9:222–228CrossRefGoogle Scholar
  12. Cohen AN (2006) Chapter III species introductions and the Panama Canal. In: Gollasch S, Galil BS, Cohen AN (eds) Bridging divides. Springer, Dordrecht, pp 127–206CrossRefGoogle Scholar
  13. Córdova-Tapia F, Contreras M, Zambrano L (2015) Trophic niche overlap between native and non-native fishes. Hydrobiologia 746:291–301CrossRefGoogle Scholar
  14. Correa C, Bravo AP, Hendry AP (2012) Reciprocal trophic niche shifts in native and invasive fish: salmonids and galaxiids in Patagonian lakes. Freshw Biol 57:1769–1781CrossRefGoogle Scholar
  15. Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can J Fish Aquat Sci 54:726–738CrossRefGoogle Scholar
  16. Côté IM, Green SJ, Morris JA Jr, Akins JL, Steinke D (2013) Diet richness of invasive Indo-Pacific lionfish revealed by DNA barcoding. Mar Ecol Prog Ser 472:249–256CrossRefGoogle Scholar
  17. Cox JG, Lima SL (2006) Naiveté and an aquatic–terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680PubMedCrossRefGoogle Scholar
  18. Dinno A (2017) R Package ‘dunn.test’. https://cran.r-project.org/web/packages/dunn.test/dunn.test.pdf
  19. Dudgeon D et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182PubMedCrossRefGoogle Scholar
  20. Eigenmann CH, Eigenmann RS (1889) A review of the Erythrininae. Proc Calif Acad Sci 2:100–117Google Scholar
  21. Fugi R, Luz-Agostinho KG, Agostinho A (2008) Trophic interaction between an introduced (peacock bass) and a native (dogfish) piscivorous fish in a neotropical impounded river. Hydrobiologia 607:143–150CrossRefGoogle Scholar
  22. Glen AS, Dickman CR (2005) Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biol Rev 80:387–401PubMedCrossRefGoogle Scholar
  23. Gomiero L, Braga FMdS (2004) Feeding of introduced species of Cichla (Perciformes, Cichlidae) in Volta Grande reservoir, river Grande (MG/SP). Braz J Biol 64:787–795PubMedCrossRefGoogle Scholar
  24. González R (1993) Actualidad de las pesquerías del pez sargento (Cichla ocellaris) en el lago Gatún. Revista Universidad 48:87–95Google Scholar
  25. Guzzo MM, Haffner GD, Legler ND, Rush SA, Fisk AT (2013) Fifty years later: trophic ecology and niche overlap of a native and non-indigenous fish species in the western basin of Lake Erie. Biol Invasions 15:1695–1711CrossRefGoogle Scholar
  26. Hanna DEL, Buck DG, Chapman LJ (2015) Effects of habitat on mercury concentrations in fish: a case study of Nile perch (Lates niloticus) in Lake Nabugabo, Uganda. Ecotoxicology 25:1–14Google Scholar
  27. Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297Google Scholar
  28. Hernandez-Santin L, Goldizen AW, Fisher DO (2016) Introduced predators and habitat structure influence range contraction of an endangered native predator, the northern quoll. Biol Conserv 203:160–167CrossRefGoogle Scholar
  29. Hildebrand SF (1938) A new catalogue of the freshwater fishes of Panama. Field Museum of Natural History, Zoological SeriesCrossRefGoogle Scholar
  30. Hyslop E (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  31. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER–Stable isotope bayesian ellipses in R. J Animal Ecol 80:595–602CrossRefGoogle Scholar
  32. Jepsen DB, Winemiller KO, Taphorn DC (1997) Temporal patterns of resource partitioning among Cichla species in a Venezuelan blackwater river. J Fish Biol 51:1085–1108PubMedGoogle Scholar
  33. King R, Ray J, Stanford K (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115CrossRefGoogle Scholar
  34. Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299:1388–1391PubMedCrossRefGoogle Scholar
  35. Latini A, Petrere M (2004) Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fish Manag Ecol 11:71–79CrossRefGoogle Scholar
  36. Layman CA, Winemiller KO, Arrington DA (2005a) Describing a species-rich river food web using stable isotopes, stomach contents, and functional experiments. In: de Ruiter PC, Wolters V, Moore JC (eds) Dynamic food webs: multispecies assemblages, ecosystem development and environmental change. Elsevier, Amsterdam, pp 395–496CrossRefGoogle Scholar
  37. Layman CA, Winemiller KO, Arrington DA, Jepsen DB (2005b) Body size and trophic position in a diverse tropical food web. Ecology 86:2530–2535CrossRefGoogle Scholar
  38. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48PubMedCrossRefPubMedCentralGoogle Scholar
  39. Locke SA, Bulté G, Forbes MR, Marcogliese DJ (2013) Estimating diet in individual pumpkinseed sunfish Lepomis gibbosus using stomach contents, stable isotopes and parasites. J Fish Biol 82:522–537PubMedCrossRefPubMedCentralGoogle Scholar
  40. Mattox GM, Bifi AG, Oyakawa OT (2014) Taxonomic study of Hoplias microlepis (Günther, 1864), a trans-Andean species of trahiras (Ostariophysi: Characiformes: Erythrinidae). Neotrop Ichthyol 12:343–352CrossRefGoogle Scholar
  41. Meek SE, Hildebrand SF (1916) The fishes of the freshwaters of Panama. Field Museum of Natural History, Zoological SeriesGoogle Scholar
  42. Newsome TM, Dellinger JA, Pavey CR, Ripple WJ, Shores CR, Wirsing AJ, Dickman CR (2015) The ecological effects of providing resource subsidies to predators. Glob Ecol Biogeogr 24:1–11CrossRefGoogle Scholar
  43. Olden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24PubMedCrossRefGoogle Scholar
  44. Oliveros O, Rossi L (1991) Ecología trófica de Hoplias malabaricus malabaricus (Pisces, Erythrinidae). Rev Asoc Cienc Nat Litoral 22:55–68Google Scholar
  45. Olowo J, Chapman LJ (1999) Trophic shifts in predatory catfishes following the introduction of Nile perch into Lake Victoria. Afr J Ecol 37:457–470CrossRefGoogle Scholar
  46. Oro D, Genovart M, Tavecchia G, Fowler MS, Martínez-Abraín A (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514PubMedCrossRefGoogle Scholar
  47. Ortiz-Sandoval J, Górski K, Sobenes C, González J, Manosalva A, Elgueta A, Habit E (2017) Invasive trout affect trophic ecology of Galaxias platei in Patagonian lakes. Hydrobiologia 790:201–212CrossRefGoogle Scholar
  48. Paiva MP (1974) Crescimento, alimentação e reprodução da traíra, Hoplias malabaricus (Bloch), no nordeste brasileiro. Imprensa Universitária da Universidade Federal do CearáGoogle Scholar
  49. Parnell AC, Jackson AL (2015) R Package ‘siar’. https://cran.r-project.org/web/packages/siar/siar.pdf
  50. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  51. Petry AC, Gomes LC, Piana PA et al (2010) The role of the predatory trahira (Pisces: Erythrinidae) in structuring fish assemblages in lakes of a Neotropical floodplain. Hydrobiologia 651:115–126CrossRefGoogle Scholar
  52. Pilger TJ, Gido KB, Propst DL (2010) Diet and trophic niche overlap of native and nonnative fishes in the Gila River, USA: implications for native fish conservation. Ecol Freshw Fish 19:300–321CrossRefGoogle Scholar
  53. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  54. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189PubMedCrossRefGoogle Scholar
  55. PREPAC (2005) Inventario de cuerpos de agua continentales de la República de Panamá con énfasis en la pesca y la acuicultura. MIDA-OSPESCAGoogle Scholar
  56. Rabelo H, Araújo-Lima CARM (2002) A dieta e o consumo diário de alimento de Cichla monoculus na Amazônia Central. Acta Amazon 32:707–724CrossRefGoogle Scholar
  57. Reis RE, Kullander SO, Ferraris CJ (2003) Check list of the freshwater fishes of South and Central America. Edipucrs, Porto AlegreGoogle Scholar
  58. Ricciardi A, MacIsaac HJ (2011) Impacts of biological invasions on freshwater ecosystems. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, Hoboken, pp 211–224Google Scholar
  59. Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939CrossRefGoogle Scholar
  60. Roy HE et al (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725CrossRefGoogle Scholar
  61. Salo P, Korpimäki E, Banks PB, Nordström M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond B Biol Sci 274:1237–1243CrossRefGoogle Scholar
  62. Schlaepfer MA, Sax DF, Olden JD (2011) The potential conservation value of non-native species. Conserv Biol 25:428–437PubMedCrossRefGoogle Scholar
  63. Schoener TW (1968) The anolis lizards of bimini: resource partitioning in a complex fauna. Ecology 49:704–726CrossRefGoogle Scholar
  64. Shafland PL (1999) The introduced butterfly peacock (Cichla ocellaris) in Florida. II. Food and reproductive biology. Rev Fish Sci 7:95–113CrossRefGoogle Scholar
  65. Sharpe DMT, De León LF, González R, Torchin ME (2017) Tropical fish community does not recover 45 years after predator introduction. Ecology 98:412–424PubMedCrossRefGoogle Scholar
  66. Sih A et al (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621CrossRefGoogle Scholar
  67. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122CrossRefGoogle Scholar
  68. Snyder WE, Clevenger GM, Eigenbrode SD (2004) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140:559–565PubMedCrossRefGoogle Scholar
  69. Syväranta J, Lensu A, Marjomäki TJ et al (2013) An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS ONE 8:e56094PubMedPubMedCentralCrossRefGoogle Scholar
  70. Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404CrossRefGoogle Scholar
  71. Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467CrossRefGoogle Scholar
  72. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182PubMedCrossRefGoogle Scholar
  73. Vitousek PM, D’antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16Google Scholar
  74. Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, Newton J (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497CrossRefGoogle Scholar
  75. White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455CrossRefGoogle Scholar
  76. Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol 26:129–135PubMedCrossRefGoogle Scholar
  77. Winemiller KO (1989) Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environ Biol Fishes 26:177–199CrossRefGoogle Scholar
  78. Winemiller KO, Taphorn DC, Barbarino-Duque A (1997) Ecology of Cichla (Cichlidae) in two blackwater rivers of southern Venezuela. Copeia 4:690–696CrossRefGoogle Scholar
  79. Yuille MJ, Fisk AT, Stewart T, Johnson TB (2015) Evaluation of Lake Ontario salmonid niche space overlap using stable isotopes. J Great Lakes Res 41:934–940CrossRefGoogle Scholar
  80. Zaret TM, Paine R (1973) Species introduction in a tropical lake. Science 182:449–455PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyMcGill UniversityMontrealCanada
  2. 2.Naos LaboratoriesSmithsonian Tropical Research InstitutePanama CityPanama
  3. 3.Shoals Marine LaboratoryUniversity of New HampshireDurhamUSA

Personalised recommendations