Interspecific competitive interactions affect body size and oxidative status of two nonnative salmonid species.

Allopatry Antioxidant defenses Brown trout Rainbow trout Sympatry

Journal

Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049

Informations de publication

Date de publication:
19 Jan 2024
Historique:
received: 12 09 2023
accepted: 10 01 2024
medline: 19 1 2024
pubmed: 19 1 2024
entrez: 19 1 2024
Statut: aheadofprint

Résumé

In fish, interspecific interactions between nonnative and other sympatric species are considered determinants in shaping species assemblages. Such interactions can also arise between nonnative fish species only, including salmonids such as the brown trout (Salmo trutta, Linnaeus, 1758) and the rainbow trout (Oncorhynchus mykiss, Walbaum, 1792), returning contrasting outcomes. The present manipulative experiment was aimed at exploring the effect of interspecific competition on the body growth and the oxidative status of parr (2 + -year-old individuals) of the brown trout and the rainbow trout. Allopatric (intraspecific competition) and sympatric (interspecific competition) populations of these species were experimentally recreated in two wild streams. At the end of a 2-month-long experiment, changes in specific growth rate (SGR), oxidative status (i.e., levels of reactive oxygen species and activity of antioxidant enzymes such as superoxide dismutase - SOD, catalase - CAT and glutathione peroxidase - GPx) and oxidative damage (i.e., lipid peroxidation) were investigated in brown and rainbow trout individuals maintained in allopatric or sympatric populations. Sympatric interactions between rainbow and brown trout parr resulted in a significant decrease in SGR of brown trout individuals only. Moreover, an overall modulation of the oxidative status, in terms of an increase in ROS levels coupled with the activation of SOD and CAT activity, occurred in brown trout individuals under sympatric conditions. These findings might suggest that, under sympatric conditions, parr of the rainbow trout are more competitive than brown trout for food acquisition. However, this competition affected the antioxidant defenses of the brown trout only, probably because of reduced ingestion of dietary antioxidants or increased physical activity and aggressive behavior. Thus, interspecific interactions can induce physiological and phenotypic effects on parr of nonnative salmonids, with potential consequences on the establishment of populations of these species in freshwater ecosystems.

Identifiants

pubmed: 38240889
doi: 10.1007/s10695-024-01301-0
pii: 10.1007/s10695-024-01301-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Alessio HM, Goldfarb AH (1988) Lipid peroxidation and scavenger enzymes during exercise: adaptive response to training. J Appl Physiol 64(4):1333–1336
pubmed: 3378967 doi: 10.1152/jappl.1988.64.4.1333
Aras NM, Bayir A, Sirkecioglu AN, Bayir M, Aksakal E, Haliloglu HI (2009) Seasonal changes in antioxidant defence system of liver and gills of Salmo trutta caspius, Salmo trutta labrax and Salmo trutta macrostigma. J Fish Biol 74(4):842–856
pubmed: 20735603 doi: 10.1111/j.1095-8649.2008.02164.x
Avila BW, Winkelman DL, Fetherman ER (2018) Survival of whirling-disease-resistant rainbow trout fry in the wild: a comparison of two strains. J Aquat Anim Health 30(4):280–290
pubmed: 30157300 doi: 10.1002/aah.10040
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42(3):517–525
pubmed: 21708747 doi: 10.1093/icb/42.3.517
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26
doi: 10.1016/0959-8030(91)90019-G
Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Biol Indic Aquat Ecosyst, pp 111–148. American Fisheries Society, USA
Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM (2011) Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defenses. Comp Biochem Physiol Part B: Biochem Mol Biol 159(4):191–196
Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34:171–182
doi: 10.1111/j.1095-8649.1989.tb03300.x
Chowdhury S, Saikia SK (2020) Oxidative stress in fish: a review. J Sci Res 12(1):145–160
doi: 10.3329/jsr.v12i1.41716
Cook KV, O’Connor CM, McConnachie SH, Gilmour KM, Cooke SJ (2012) Condition dependent intra-individual repeatability of stress-induced cortisol in a freshwater fish. Comp Biochem Physiol a: Mol Integr Physiol 161(3):337–343
pubmed: 22179071 doi: 10.1016/j.cbpa.2011.12.002
Deng J, Yu L, Liu C, Yu K, Shi X, Yeung LW, Zhou B (2009) Hexabromocyclododecane-induceddevelopmental toxicity and apoptosis in zebrafish embryos. Aquat Toxicol 93(1):29–36
Deslauriers D, Chipps SR, Breck JE, Rice JA, Madenjian CP (2017) Fish bioenergetics 4.0: an R-based modeling modeling application. Fisheries 42(11):586–596
doi: 10.1080/03632415.2017.1377558
DiBattista JD, Levesque HM, Moon TW, Gilmour KM (2006) Growth depression in socially subordinate rainbow trout Oncorhynchus mykiss: more than a fasting effect. Physiol Biochem Zool 79(4):675–687
pubmed: 16826494 doi: 10.1086/504612
Fausch KD (2007) Introduction, establishment and effects of non-native salmonids: considering the risk of rainbow trout invasion in the United Kingdom. J Fish Biol 71:1–32
doi: 10.1111/j.1095-8649.2007.01682.x
Gatz AJ, Sale MJ, Loar JM (1987) Habitat shifts in rainbow trout: competitive influences of brown trout. Oecologia 74(1):7–19
pubmed: 28310408 doi: 10.1007/BF00377339
Gomez CF, Constantine L, Huggett DB (2010) The influence of gill and liver metabolism on the predicted bioconcentration of three pharmaceuticals in fish. Chemosphere 81(10):1189–1195
pubmed: 20980039 doi: 10.1016/j.chemosphere.2010.09.043
Grant JWA, Imre I (2005) Patterns of density-dependent growth in juvenile stream-dwelling salmonids. J Fish Biol 67:100–110
doi: 10.1111/j.0022-1112.2005.00916.x
Grossman GD, Simon TN (2020) Density-dependent effects on salmonid populations: a review. Ecol Freshw Fish 29(3):400–418
doi: 10.1111/eff.12523
Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19(9):470–474
pubmed: 16701309 doi: 10.1016/j.tree.2004.07.005
Hagelin A, Bergman E (2021) Competition among juvenile brown trout, grayling, and landlocked Atlantic salmon in flumes—predicting effects of interspecific interactions on salmon reintroduction success. Can J Fish Aquat Sci 78(3):332–338
doi: 10.1139/cjfas-2020-0155
Hasegawa K (2016) The density dependent interspecific competition between nonnative salmonids, rainbow trout and brown trout. Environ Biol Fish 99(4):433–438
doi: 10.1007/s10641-016-0484-y
Hasegawa K (2020) Invasions of rainbow trout and brown trout in Japan: a comparison of invasiveness and impact on native species. Ecol Freshw Fish 29(3):419–428
doi: 10.1111/eff.12534
Hasegawa K, Maekawa K (2008) Different longitudinal distribution patterns of native white-spotted charr and non-native brown trout in Monbetsu stream, Hokkaido, northern Japan. Ecol Freshw Fish 17(1):189–192
doi: 10.1111/j.1600-0633.2007.00254.x
Iacobuzio R (2017) Survey of the fish fauna of the Gran Paradiso National Park: towards a conservation action for the marble trout (Salmo marmoratus). PhD thesis; PhD Course in Environmental Sciences, XXX Cycle, University of Milan
Imre I, Grant JWA, Cunjak RA (2005) Density-dependent growth of young-of-the-year Atlantic salmon Salmo salar in Catamaran Brook, New Brunswick. J Anim Ecol 74(3):508–516
doi: 10.1111/j.1365-2656.2005.00949.x
Inoue M, Miyata H, Tange Y, Taniguchi Y (2009) Rainbow trout (Oncorhynchus mykiss) invasion in Hokkaido streams, northern Japan, in relation to flow variability and biotic interactions. Can J Fish Aquat Sci 66(9):1423–1434
doi: 10.1139/F09-088
Inoue M, Ichimori D, Abe H, Mizuno N (2022). Complementary distribution of non-native white-spotted charr and native red-spotted masu salmon in Shikoku Island, southwestern Japan: a consequence of interspecific interactions?. Ichthyol Res 1–9
Kassahn KS, Crozier RH, Pörtner HO, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol Rev 84(2):277–292
pubmed: 19344429 doi: 10.1111/j.1469-185X.2008.00073.x
Korsu K, Huusko A, Muotka T (2008) Ecology of alien species with special reference to stream salmonids. Boreal Environ Res 13:43–52
Laursen DC, Silva PI, Larsen BK, Höglund E (2013) High oxygen consumption rates and scale loss indicate elevated aggressive behaviour at low rearing density, while elevated brain serotonergic activity suggests chronic stress at high rearing densities in farmed rainbow trout. Physiol Behav 122:147–154
pubmed: 24018332 doi: 10.1016/j.physbeh.2013.08.026
Li HW, Brocksen RW (1977) Approaches to the analysis of energetic costs of intraspecific competition for space by rainbow trout (Salmo gairdneri). J Fish Biol 11(4):329–341
doi: 10.1111/j.1095-8649.1977.tb04126.x
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. Invasive Species Specialist Group of the World Conservation Union, Auckland
Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fisheries 15(1):75–88
doi: 10.1007/s11160-005-7846-4
McDowall RM (2003) Impacts of introduced salmonids on native galaxiids in New Zealand upland streams: a new look at an old problem. Trans Am Fish Soc 132(2):229–238
doi: 10.1577/1548-8659(2003)132<0229:IOISON>2.0.CO;2
McGhee KE, Travis J (2011) Early food and social environment affect certain behaviours but not female choice or male dominance in bluefin killifish. Anim Behav 82(1):139–147
doi: 10.1016/j.anbehav.2011.04.009
McHugh P, Budy P (2006) Experimental effects of nonnative brown trout on the individual-and population level performance of native Bonneville cutthroat trout. Trans Am Fish Soc 135(6):1441–1455
Miyasaka H, Nakano S, Furukawa-Tanaka T (2003) Food habit divergence between white-spotted charr and masu salmon in Japanese mountain streams: circumstantial evidence for competition. Limnology 4(1):0001–0010
doi: 10.1007/s10201-002-0088-4
Morita K, Sahashi G, Tsuboi JI (2016) Altitudinal niche partitioning between white-spotted charr (Salvelinus leucomaenis) and masu salmon (Oncorhynchus masou) in a Japanese river. Hydrobiologia 783(1):93–103
doi: 10.1007/s10750-015-2571-z
Otto DM, Moon TW (1996) Endogenous antioxidant systems of two teleost fish, the rainbow trout and the black bullhead, and the effect of age. Fish Physiol Biochem 15(4):349–358
pubmed: 24194254 doi: 10.1007/BF02112362
Parolini M, Iacobuzio R, Possenti CD, Bassano B, Pennati R, Saino N (2018a) Carotenoid-based skin coloration signals antioxidant defenses in the brown trout (Salmo trutta). Hydrobiologia 815(1):267–280
doi: 10.1007/s10750-018-3571-6
Parolini M, Iacobuzio R, Bassano B, Pennati R, Saino N (2018b) Melanin-based skin coloration predicts antioxidant capacity in the brown trout (Salmo trutta). Physiol Biochem Zool 91(5):1026–1035
pubmed: 30084732 doi: 10.1086/699522
Parolini M, Iacobuzio R, De Felice B, Bassano B, Pennati R, Saino N (2019) Age-and sex-dependent variation in the activity of antioxidant enzymes in the brown trout (Salmo trutta). Fish Physiol Biochem 45(1):145–154
pubmed: 30109448 doi: 10.1007/s10695-018-0545-6
Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 145(2):191–199
pubmed: 12686495 doi: 10.1016/S0009-2797(03)00002-4
Pennock CA, Carl Saunders W, Budy P (2022) High densities of conspecifics buffer native fish from negative interactions with an ecologically similar invasive. Biol Invasions 24(5):1283–1297
doi: 10.1007/s10530-021-02725-y
Perez-Campo R, Lopez-Torres M, Rojas C, Cadenas S, Barja G (1993) A comparative study of free radicals in vertebrates--I. Antioxidant enzymes. Comp Biochem Physiol B Comp Biochem 105(3–4):749–755
Prati S, Henriksen EH, Smalås A, Knudsen R, Klemetsen A, Sánchez-Hernández J, Amundsen PA (2021) The effect of inter-and intraspecific competition on individual and population niche widths: a four-decade study on two interacting salmonids. Oikos 130(10):1679–1691
doi: 10.1111/oik.08375
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Robinson MK, Rustum RR, Chambers EA, Rounds JD, Wilmore DW, Jacobs DO (1997) Starvation enhances hepatic free radical release following endotoxemia. J Surg Res 69(2):325–330
pubmed: 9224401 doi: 10.1006/jsre.1997.5062
Scott D, Irvine JR (2000) Competitive exclusion of brown trout Salmo trutta L., by rainbow trout Oncorhynchus mykiss Walbaum, in lake tributaries, New Zealand. Fish Manag Ecol 7(3):225–237
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17(4):170–176
doi: 10.1016/S0169-5347(02)02495-3
Sies H, Stahl W, Sevanian A (2005) Nutritional, dietary and postprandial oxidative stress. J Nutr 135(5):969–972
pubmed: 15867266 doi: 10.1093/jn/135.5.969
Solé M, Rodríguez S, Papiol V, Maynou F, Cartes JE (2009) Xenobiotic metabolism markers in marine fish with different trophic strategies and their relationship to ecological variables. Comp Biochem Physiol c: Toxicol Pharmacol 149(1):83–89
pubmed: 18708160
Underwood AJ (2012) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, New York
Wilhelm-Filho D, Giulivi C, Boveris A (1993) Antioxidant defences in marine fish—I. Teleosts. Comp Biochem Physiol Part C: Pharmacol Toxicol Endocrinol 106(2):409–413
Yamamoto T, Reinhardt U (2003) Dominance and predator avoidance in domesticated and wild masu salmon Oncorhynchus masou. Fish Sci 69(1):88–94
doi: 10.1046/j.1444-2906.2003.00591.x

Auteurs

Marco Parolini (M)

Department of Environmental Science and Policy, University of Milan, Via Celoria 2, 20133, Milan, Italy. marco.parolini@unimi.it.

Rocco Iacobuzio (R)

Department of Environmental Science and Policy, University of Milan, Via Celoria 2, 20133, Milan, Italy.
Parco Nazionale Gran Paradiso, Via Pio VII 9, 10135, Turin, Italy.

Bruno Bassano (B)

Parco Nazionale Gran Paradiso, Via Pio VII 9, 10135, Turin, Italy.

Roberta Pennati (R)

Department of Environmental Science and Policy, University of Milan, Via Celoria 2, 20133, Milan, Italy.

Classifications MeSH