eDNA-based detection of invasive South American loricariid catfishes (Pterygoplichthys spp.) in upper tributaries of Krishna River system, India

Abstract

The invasiveness of the fishes in the genus Pterygoplichthys poses a considerable environmental threat to native aquatic ecosystems worldwide. This disruption of natural biodiversity and fish ecosystems corresponds to changes in nutrient dynamics resulting from the impact of Pterygoplichthys, exploitation of benthic resources, and increased interspecific competition. Fish species from this genus have been reported from various places, including the Indian subcontinent. The present study aims to develop a rapid eDNA-based assay to detect the presence of Pterygoplichthys in the Bhima River, one of the major tributaries of the Krishna River system, located in the biodiverse northern Western Ghats of India. The qPCR method was optimised with newly designed Pterygoplichthys-specific primers. Subsequently, eDNA samples collected from the seven locations were analysed under these conditions. This advanced and suitable method can be applied in other regions of India as well as in neighbouring countries where an invasion is suspected or has already occurred. Our results confirmed the presence of Pterygoplichthys eDNA in four of the seven sites. This indicates the ongoing invasion throughout the region, which is one of the global freshwater eco-regions characterized by a high degree of endemism.

Keywords

• Environmental DNA
• Invasion
• Bhima River
• Quantitative PCR
• Western Ghats

References

1. Balasingham, K. D., Walter, R. P., Mandrak, N. E., & Heath, D. D. (2018). Environmental DNA detection of rare and invasive fish species in two Great Lakes tributaries. Molecular ecology, 27(1), 112-127. google scholar
2. Balasingham, K. D., Walter, R. P., Mandrak, N. E., & Heath, D. D. (2018). Environmental DNA detection of rare and invasive fish species in two Great Lakes tributaries. Molecular Ecology, 27(1), 112–127. google scholar
3. Bijukumar, A., Smrithy, R., Sureshkumar, U., & George, S. (2015). Invasion of South American suckermouth armoured catfishes Pterygoplichthys spp. (Loricariidae) in Kerala, India – a case study. Journal of Threatened Taxa, 7, 6987–6995. google scholar
4. Chaichana, R., & Jongphadungkiet, S. (2012). Assessment of the invasive catfish Pterygoplichthys pardalis (Castelnau, 1855) in Thailand: ecological impacts and biological control alternatives. Tropical Zoology, 25, 173–182. google scholar
5. Chakraborty, P., Chakrabarti, S., Mukherjee, P., Yardi, K., & Das, S. (2020). Notes on the discovery and ecology of the invasive armoured catfish Pterygoplichthys disjunctivus (Weber, 1991) and the exotic cichlid Amphilophus trimaculatus (Günther, 1867) from southern West Bengal, India. Ecological Questions, 31, 7–13. google scholar
6. Dahanukar, N., Raghavan, R., Ali, A., Abraham, R., & Shaji, C. P. (2011). The status and distribution of freshwater fishes of the Western Ghats. In S. Molur, K. G. Smith, B. A. Daniel, & W. R. T. Darwall (Eds.), The status and distribution of freshwater biodiversity in the Western Ghats, India (pp. 21–48). IUCN, Cambridge, UK and Gland, Switzerland, and Zoo Outreach Organisation, Coimbatore, India. google scholar
7. Das, B. K., Ray, A., Manna, R. K., Roshith, C. M., Baitha, R., Karna, S. K., Gupta, S. D., & Bhor, M. (2020). Occurrence of exotic vermiculated sailfin catfish Pterygoplichthys disjunctivus from the lower stretch of River Ganga, West Bengal, India. Current Science, 119(12), 2006–2009. google scholar
8. Ferraris, C. J. (2007). Checklist of catfishes, recent and fossil (Osteichthyes: Siluriformes), and catalogue of siluriform primary types. Zootaxa, 1418, 1–628. google scholar

9. Fricke, R., Eschmeyer, W. N., & Van der Laan, R. (Eds.). (2024). Eschmeyer’s catalog of fishes: Genera, species, references. Electronic version, accessed 03 July 2024. google scholar
10. Ganguly, N., & Umapathy, G. (2024). Is it there? Estimating the invasion of armored sailfin catfish (Pterygoplichthys sp.) in the water bodies of the Eastern Ghats, India using the eDNA approach. Environmental DNA, 6(3), e538. google scholar
11. Goldberg, C. S., Turner, C. R., Deiner, K., Klymus, K. E., Thomsen, P. F., Murphy, M. A., Spear, S. F., McKee, A., Oyler-McCance, S. J., Cornman, R. S., & Laramie, M. B. (2016). Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods in Ecology and Evolution, 7, 1299–1307. google scholar
12. Hill, J. E., & Sowards, J. (2015). Successful eradication of the non-native loricariid catfish Pterygoplichthys disjunctivus from the Rainbow River, Florida. Management of Biological Invasions, 6(3), 311–317. google scholar
13. Hossain, M. S., Akmal, S. G., Buřič, M., & Patoka, J. (2024). Invasive Amazon sailfin catfish in Bangladesh: wild distribution, environmental and perceived socio- economic consequences. Aquatic Invasions, 19(1), 121–136. google scholar
14. Hussan, A., Sundaray, J. K., Mandal, R. N., Hoque, F., Das, A., Chakrabarti, P. P., & Adhikari, S. (2019). Invasion of non-indigenous suckermouth armoured catfish of the genus Pterygoplichthys (Loricariidae) in the East Kolkata Wetlands: stakeholders’ perception. Indian Journal of Fisheries, 66(2), 29–42. google scholar
15. Joseph, C., Faiq, M. E., Li, Z., et al. (2022). Persistence and degradation dynamics of eDNA affected by environmental factors in aquatic ecosystems. Hydrobiologia, 849, 4119–4133. google scholar
16. Krishnakumar, K., Raghavan, R., Prasad, G., Bijukumar, A., Sekharan, M., Pereira, B., & Ali, A. (2009). When pets become pests – exotic aquarium fishes and biological invasions in Kerala, India. Current Science, 97(4), 474–476. google scholar
17. Larson, E. R., Graham, B. M., Achury, R., Coon, J. J., Daniels, M. K., Gambrell, D. K., Jonasen, K. L., King, G. D., LaRacuente, N., Perrin-Stowe, T. I. N., Reed, E. M., Rice, C. J., Ruzi, S. A., Thairu, M. W., Wilson, J. C., & Suarez, A. V. (2020). From eDNA to citizen science: emerging tools for the early detection of invasive species. Frontiers in Ecology and the Environment, 18(4), 194–202. google scholar
18. Marr, S. M., Patoka, J., & Zworykin, D. D. (2024). Estimating the potential distribution range of the invasive South American suckermouth armoured catfishes Pterygoplichthys spp. in the Indo‐Burma biodiversity hotspot using MaxEnt. Aquatic Conservation: Marine and Freshwater Ecosystems, 34(5), e4173. google scholar
19. Novák, J., Hofmann, J., Hohl, D., Magalhães, A. L. B., & Patoka, J. (2022). Enigmatic armoured catfishes (Siluriformes: Callichthyidae and Loricariidae) in ornamental aquaculture: A new insight into Neotropical fish diversity. Aquaculture, 547, 737460. google scholar
20. Orfinger, A. B., & Goodding, D. D. (2018). The global invasion of the suckermouth armoured catfish genus Pterygoplichthys (Siluriformes: Loricariidae): annotated list of species, distributional summary, and assessment of impacts. Zoological Studies, 57, 57-07. google scholar
21. Patoka, J., Takdir, M., Yonvitner, Aryadi, H., Jerikho, R., Nilawati, J., Tantu, F. Y., Bohatá, L., Aulia, A., Kamal, M. M., Wardiatno, Y., & Petrtýl, M. (2020). Two species of illegal South American sailfin catfish of the genus Pterygoplichthys well established in Indonesia. Knowledge & Management of Aquatic Ecosystems, 421, 28. google scholar
22. Prabhakaran, G. K., Sunkara, M., Raghavan, R., & Umapathy, G. (2023). Development of a species-specific qPCR assay for the detection of invasive African sharptooth catfish (Clarias gariepinus) using environmental DNA. Biological Invasions, 25(4), 975–982. google scholar
23. Quintana, Y., Keppeler, F. W., & Winemiller, K. O. (2023). Does invasion by armoured catfish shift trophic ecology of native fishes? Evidence from stable isotope analysis. Ecology, 104(5), e4024. google scholar
24. Raj, S., Prakash, P., Reghunath, R., Tharian, J. C., Raghavan, R., & Kumar, A. B. (2021). Distribution of alien invasive species in aquatic ecosystems of the southern Western Ghats, India. Aquatic Ecosystem Health & Management, 24(2), 64–75. google scholar
25. Rees, H. C., Maddison, B. C., Middleditch, D. J., Patmore, J. R., & Gough, K. C. (2014). The detection of aquatic animal species using environmental DNA: a review of eDNA as a survey tool in ecology. Journal of Applied Ecology, 51(5), 1450–1459. google scholar
26. Ricciardi, A., & MacIsaac, H. J. (2011). Impacts of biological invasions on freshwater ecosystems. In D. M. Richardson (Ed.), Fifty years of invasion ecology: The legacy of Charles Elton (pp. 211–224). google scholar
27. Rishan, S. T., Kline, R. J., & Rahman, M. S. (2023). Applications of environmental DNA (eDNA) to detect subterranean and aquatic invasive species: a critical review on the challenges and limitations of eDNA metabarcoding. Environmental Advances, 12, 100370. google scholar
28. Sahoo, L., Swain, P. P., Hussan, A., Mohapatra, A., & Sundaray, J. K. (2022). DNA barcoding delineates the identity of invasive South American sucker mouth armoured catfishes of genus Pterygoplichthys of the East Kolkata Wetlands, West Bengal, India as a single species. Indian Journal of Fisheries, 69(4), 115–118. google scholar
29. Seshagiri, B., Swain, S. K., Pillai, B. R., Satyavati, C., Sravanti, Y., Rangacharyulu, P. V., Rathod, R., & Ratnaprakash, V. (2021). Suckermouth armoured catfish (Pterygoplichthys spp.) menace in freshwater aquaculture and natural aquatic systems in Andhra Pradesh, India. International Journal of Fisheries and Aquatic Studies, 9(1), 375–384. google scholar
30. Sinha, R. K., Sinha, R. K., Sarkar, U. K., & Lakra, W. S. (2010). First record of the southern sailfin catfish, Pterygoplichthys anisitsi Eigenmann & Kennedy, 1903 (Teleostei: Loricariidae), in India. Journal of Applied Ichthyology, 26(4), 606–608. google scholar
31. Simberloff, D. (2002). Today Tiritiri Matangi, tomorrow the world! Are we aiming too low in invasive control? In C. R. Veitch & M. N. Clout (Eds.), Turning the tide: the eradication of invasive species (pp. 4–12). google scholar
32. Simberloff, D. (2003). How much information on population biology is needed to manage introduced species? Conservation Biology, 17(1), 83–92. google scholar
33. Stothard, P. (2000). The Sequence Manipulation Suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques, 28, 1102–1104. google scholar
34. Suresh, V. R., Ekka, A., Biswas, D. K., Sahu, S. K., Yousuf, A., & Das, S. (2019). Vermiculated sailfin catfish, Pterygoplichthys disjunctivus (Actinopterygii: Siluriformes: Loricariidae): invasion, biology, and initial impacts in the East Kolkata Wetlands, India. Acta Ichthyologica et Piscatoria, 49(3), 221–233. google scholar
35. Verma, C. R., Pise, M., Khare, T., Kumkar, P., & Kalous, L. (2024). Social media and genetic evidence demonstrate the expansion of an invasive fish in India. Journal of Vertebrate Biology, 73(23087), 23087.1-6. google scholar
36. Wei, H., Copp, G. H., Vilizzi, L., Liu, F., Gu, D., Luo, D., … & Hu, Y. (2017). The distribution, establishment and life-history traits of non-native sailfin catfishes Pterygoplichthys spp. in Guangdong Province, China. Aquatic Invasions, 12(2), 241–249. google scholar
37. Wu, Y., Colborne, S. F., Charron, M. R., & Heath, D. D. (2023). Development and validation of targeted environmental DNA (eDNA) metabarcoding for early detection of 69 invasive fishes and aquatic invertebrates. Environmental DNA, 5(1), 73–84. google scholar