Abstract
Reproductive interference occurs when fitness of females of one species decreases because of misdirected courtship behaviors by males of another species. Reproductive interference strongly excludes either species in the interaction but it does not persist for long on an evolutionary time scale. Therefore, reproductive interference between a pair of co-evolved native species is difficult to observe because exclusion ends the interaction even if even the potential for reproductive interference still exists. However, anthropogenic environmental changes can bring about secondary contact between two species and trigger reproductive interference, leading to local species extinction. We demonstrated this phenomenon with two native spined loaches: Cobitis magnostriata (Cmag) and C. minamorii oumiensis (Cmio). In 2015 and 2016, we investigated the spatiotemporal dynamics of adults and juveniles of both species to estimate the effects of the relative abundance of adults on reproductive success. Additionally, we surveyed the distribution of juveniles and investigated the proportion of gravid females which failed to reproduce at the end of the spawning season. In 2016, Cmio juveniles were fewer than in 2015, although the abundances of Cmio adults were similarly low in both years and the Cmag adults were more abundant in 2016 than in 2015. The juveniles of the two species exhibited similar spatiotemporal dynamics. At the end of the spawning season, Cmag males were abundant and most Cmio females failed to reproduce. These results suggest that the two species share spawning habitats and seasons and that Cmag males exert reproductive interference on Cmio females. This report is the first of a study suggesting that anthropogenic environmental changes triggered reproductive interference between native species in the field.
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References
Bohlen J (2008) Spawning marks in spined loaches (Cobitis taenia, Cobitidae, Teleostei). Folia Zool 57:168–171
Dame EA, Petren K (2006) Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Anim Behav 71:1165–1173. https://doi.org/10.1016/j.anbehav.2005.10.009
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282
Hettyey A, Vági B, Kovács T, Ujszegi J, Katona P, Szederkényi M, Pearman BP, Griggio M, Hoi H (2014) Reproductive interference between Rana dalmatina and Rana temporaria affects reproductive success in natural populations. Oecologia 176:457–464. https://doi.org/10.1007/s00442-014-3046-z
Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20
Janko K, Flajšhans M, Choleva L, Bohlen J, Šlechtová V, Rábová M, Lajbner Z, ŠLechta V, Ivanova P, Dobrovolov I, Culling M, Persat H, Kotusz J, Ráb P (2007) Diversity of European spined loaches (genus Cobitis L.): an update of the geographic distribution of the Cobitis taenia hybrid complex with a description of new molecular tools for species and hybrid determination. J Fish Biol 71:387–408. https://doi.org/10.1111/j.1095-8649.2007.01663.x
Kishi S, Nishida T, Tsubaki Y (2009) Reproductive interference determines persistence and exclusion in species interactions. J Anim Ecol 78:1043–1049. https://doi.org/10.1111/j.1365-2656.2009.01560.x
Konishi M, Takata K (2004) Impact of asymmetrical hybridization followed by sterile F1 hybrids on species replacement in Pseudorasbora. Conserv Genet 5:463–474. https://doi.org/10.1023/B:COGE.0000041027.64785.77
Kottelat M (2012) Conspectus cobitidum: an inventory of the loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull Zool 26:23–30
Kuno E (1992) Competitive exclusion through reproductive interference. Res Popul Ecol 34:275–284. https://doi.org/10.1007/BF02514797
Minamori S (1956) Physiological isolation in Cobitidae. IV. Speciation of two sympatric races of Lake Biwa of the striated spinous loach. Jpn. J Zool 12:89–104
Ministry of the Environment (2015) Red Data Book 2014 – Threatened Wildlife of Japan – Volume 4, Pisces-Brackish and Fresh Water Fishes. Tokyo, Japan
Morisita M (1959) Measuring of interspecific association and similarity between communities. Reprinted from the Memoirs of the Faculty of Science, Kyushu University, Series E (Biology) 3:65–80. 10.18960/seitai.11.6_252_4
Nakajima J (2012) Taxonomic study of the Cobitis striata complex (Cypriniformes, Cobitidae) in Japan. Zootaxa 3586:103–130
Nakano M, Uehara K, Urabe M (2015) Habitat and breeding season of striated spined loaches on the northwest coast of Lake Biwa. Jpn J Conserv Ecol 20:49–58. https://doi.org/10.18960/hozen.20.1_49
Noriyuki S, Osawa N, Nishida T (2012) Asymmetric reproductive interference between specialist and generalist predatory ladybirds. J Anim Ecol 81:1077–1085. https://doi.org/10.1111/j.1365-2656.2012.01984.x
Pereira RJ, Wake DB (2009) Genetic leakage after adaptive and nonadaptive divergence in the Ensatina eschscholtzii ring species. Evolution 63:2288–2301. https://doi.org/10.1111/j.1558-5646.2009.00722.x
Ribeiro JMC, Spielman A (1989) The satyr effect: a model predicting parapatry and species extinction. Am Nat 128:513–528. https://doi.org/10.1086/284584
Saitoh K (1990) Reproductive and habitat isolation between two populations of the striated spined loach. Environ Biol Fish 28:237–248. https://doi.org/10.1007/BF00751037
Saitoh K (1993) Smaller race and the large race of the striated spined loach are threatened. Jpn J Ichthyol 40:394–397
Saitoh K (2005) Cobitis striata species complex. In: Katano K, Mori S (eds) The present and future of endangered freshwater fishes: scenario of fruitful conservation. Shinzansha, Tokyo, pp 186–192
Saitoh K, Matsuda S (1990) Spined loaches distributed in the Lake Biwa water system. The Annual Reports of the Biwako Bunkakan 8:19–23
Saitoh K, Takai A, Ojima Y (1984) Chromosomal study of the three local races of the striated spined loach (Cobitis taenia striata). P Jpn Acad B-Phys 60:187–190. https://doi.org/10.2183/pjab.60.187
Saitoh K, Chen WJ, Mayden RL (2010) Extensive hybridization and tetrapolyploidy in spined loach fish. Mol Phylogenet Evol 56:1001–1010. https://doi.org/10.1016/j.ympev.2010.04.021
Sun DB, Li J, Liu YQ, Crowder DW, Liu SS (2014) Effects of reproductive interference on the competitive displacement between two invasive whiteflies. Bull Entomol Res 104:334–346. https://doi.org/10.1017/S0007485314000108
Takakura KI, Fujii S (2010) Reproductive interference and salinity tolerance differentiate habitat use between two alien cockleburs: Xanthium occidentale and X. italicum (Compositae). Plant Ecol 206:309–319. https://doi.org/10.1007/s11258-009-9644-x
Takakura KI, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects. Biol Invasions 11:973–981. https://doi.org/10.1007/s10530-008-9309-z
Acknowledgements
We deeply thank A. Honma, D. Kitano, T. Hisaoka, R. Kanai, Y. Nishihira, A. Okada, K. Anan, and T. Anan for their support with field surveys. We also thank K. Uehara for his management of the study site and for his help for the consensus formation among neighboring farmers. This study was partly supported by Takara Harmonist Fund (in 2016) and JSPS KAKENHI Grant Number KB1 7 K07273.
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Morii, K., Nakano, M. & Takakura, KI. Does simultaneous and sympatric reproduction between two native spined loaches lead to reproductive interference and local extinction?. Environ Biol Fish 101, 1407–1416 (2018). https://doi.org/10.1007/s10641-018-0787-2
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DOI: https://doi.org/10.1007/s10641-018-0787-2