Reproductive environment of the decreasing Indian river shad in Asian inland waters: disentangling the climate change and indiscriminative fishing threats

Abstract

The regional climate has significantly warmed with erratically declining annual rainfall and intensified downpour within a narrower span of monsoon months, which led to an increased trophic state (≈algae) in most inland waters. Freshwater clupeids vitally control the aquatic food chain by grazing on algae. Despite increasing food availability, IUCN Red List® revealed 16 freshwater clupeids with a decreasing population trend. We investigated one such species’ reproductive dependencies, Gudusia chapra (Indian river shad), in the lower Gangetic drainage (India) under a mixed context of climate change and overfishing. Monthly rainfall (≥ 60–100 mm) and water temperature (≥ 31–32 °C) are key breeding cues for females. The regional climate seems inclined to fulfill these through the significant part of the breeding season, and indeed the species has maintained consistent breeding phenology over 20 years. Other breeding thresholds relevant to fishing include size at first maturity (≥ 6.8 cm; reduced by ~ 25–36%) and pre-spawning girth (Girthspawn50 ≥ 7 cm; first record). Girthspawn50 is a proxy of the minimum mesh size requirement of fishing nets to allow safe passage of “gravid” females (+ 22% bulged abdomen) and breed. The operational fishing nets (3–10 cm mesh) probably have been indulged in indiscriminative fishing of gravid females for generations. Under a favorably changing climate and food availability, existing evidence suggests a fishery-induced evolution in regional females (to circumvent such mesh sizes) through earlier maturation/puberty at smaller sizes. It could be an early warning sign of population collapse (smaller females → lessening fecundity → fewer offspring). Overfishing seemed to be a bigger threat than climate change.

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Data availability

The data has been submitted along with the manuscript and can be found as supplementary material.

References

  1. Ahamed F, Ahamed ZF, Hossain MY, Ohtomi J (2014) Population biology of the Indian river shad, Gudusia chapra (Clupeidae) in the Old Brahmaputra River, north-eastern Bangladesh. Sains Malaysiana 43:1645–1655

    Google Scholar 

  2. Alix M, Kjesbu OS, Anderson KC (2020) From gametogenesis to spawning: how climate-driven warming affects teleost reproductive biology. J Fish Biol:jfb.14439. https://doi.org/10.1111/jfb.14439

  3. APHA (2012) Standard methods for examination of water and waste water, 22nd edn. American Public Health Association, Washington, DC

    Google Scholar 

  4. Ara MG, Ahmed ZF, Ahmed F, Fatema MK (2018) Resolution of confusion in systematics of two major clupeid fish species in Bangladesh. FishTaxa 3:81–86

    Google Scholar 

  5. Arunachalam M, Flora A, Chinnaraja S, Rayamajhi A (2015) Identity of Gudusia chapra and re-establishment of Gudusia suhia (Family Clupeidae: Clupeiformes). Int J Pure Appl Zool 3:322–327

    Google Scholar 

  6. Baudron AR, Needle CL, Marshall CT (2011) Implications of a warming North Sea for the growth of haddock Melanogrammus aeglefinus. J Fish Biol 78:1874–1889. https://doi.org/10.1111/j.1095-8649.2011.02940.x

    CAS  Article  Google Scholar 

  7. Bogard JR, Hother A-L, Saha M, Bose S, Kabir H, Marks GC, Thilsted SH (2015) Inclusion of small indigenous fish improves nutritional quality during the first 1000 days. Food Nutr Bull 36:276–289. https://doi.org/10.1177/0379572115598885

    Article  Google Scholar 

  8. Castine SA, Bogard JR, Barman BK, Karim M, Mokarrom Hossain M, Kunda M, Mahfuzul Haque ABM, Phillips MJ, Thilsted SH (2017) Homestead pond polyculture can improve access to nutritious small fish. Food Secur 9:785–801. https://doi.org/10.1007/s12571-017-0699-6

    Article  Google Scholar 

  9. Chaudhry S (2010) Gudusia chapra. The IUCN Red List of Threatened Species 2010: e.T166523A6227899. https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T166523A6227899.en. Downloaded on 28 April 2020

  10. Chondar SL (1977) Fecundity and its role in racial studies of Gudusia chapra (Pisces: Clupeidae). Proc Indian Acad Sci - Sect B 86:245–254. https://doi.org/10.1007/BF03050969

    Article  Google Scholar 

  11. Das RK, Barat S (2014) Fishing gears operated in lentic and lotic water bodies of Cooch Behar District, West Bengal, India. Indian J Tradit Knowl 13:619–625

    Google Scholar 

  12. Engelhard GH, Heino M (2006) Climate change and condition of herring (Clupea harengus) explain long-term trends in extent of skipped reproduction. Oecologia 149:593–603. https://doi.org/10.1007/s00442-006-0483-3

    Article  Google Scholar 

  13. Froese R (2006) Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253. https://doi.org/10.1111/j.1439-0426.2006.00805.x

    Article  Google Scholar 

  14. Froese R, Pauly D (Eds) (2019) Gudusia chapra. In: FishBase. World Wide Web electronic publication. www.fishbase.org. (12/2019). Accessed on 28 April 2020

  15. Ghosh AS, Ghosh SK, Ghosh M, Ali A (2018) Studies on biodiversity of selected indigenous fish species, in Beels and Baors of South Bengal and their breeding potential through habitat modification. Int J Fish Aquat 6(4):479–483

    Google Scholar 

  16. Heino M, Díaz Pauli B, Dieckmann U (2015) Fisheries-induced evolution. Annu Rev Ecol Evol Syst 46:461–480. https://doi.org/10.1146/annurev-ecolsys-112414-054339

    Article  Google Scholar 

  17. Hossain MY, Ahmed ZF, Islam ABMS, Jasmine S, Ohtomi J (2010) Gonadosomatic index-based size at first sexual maturity and fecundity indices of the Indian River shad Gudusia chapra (Clupeidae) in the Ganges River (NW Bangladesh). J Appl Ichthyol 26:550–553. https://doi.org/10.1111/j.1439-0426.2010.01454.x

    Article  Google Scholar 

  18. Hossain MAR, Das I, Genevier L, Hazra S, Rahman M, Barange M, Fernandes JA (2019) Biology and fisheries of Hilsa shad in Bay of Bengal. Sci Total Environ 651:1720–1734. https://doi.org/10.1016/j.scitotenv.2018.10.034

    CAS  Article  Google Scholar 

  19. Hunter A, Speirs DC, Heath MR (2015) Fishery-induced changes to age and length dependent maturation schedules of three demersal fish species in the Firth of Clyde. Fish Res 170:14–23. https://doi.org/10.1016/j.fishres.2015.05.004

    Article  Google Scholar 

  20. Hunter A, Speirs DC, Heath MR (2019) Population density and temperature correlate with long-term trends in somatic growth rates and maturation schedules of herring and sprat. PLoS One 14:e0212176. https://doi.org/10.1371/journal.pone.0212176

    CAS  Article  Google Scholar 

  21. Hutchings JA (2000) Collapse and recovery of marine fishes. Nature 406(6798):882–885. https://doi.org/10.1038/35022565

    CAS  Article  Google Scholar 

  22. Hutchings JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54:297–309

    Article  Google Scholar 

  23. Hutchings JA, Côté IM, Dodson JJ, Fleming IA, Jennings S, Mantua NJ, Peterman RM, Riddell BE, Weaver AJ (2012) Climate change, fisheries, and aquaculture: trends and consequences for Canadian marine biodiversity. Environ Rev 20:220–311. https://doi.org/10.1139/a2012-011

    Article  Google Scholar 

  24. IUCN (International Union for Conservation of Nature) (2020) The IUCN Red List of Threatened Species. Version 2020-2. https://www.iucnredlist.org. Accessed 09 July 2020

  25. James AG (1988) Are clupeid microphagists herbivorous or omnivorous? A review of the diets of some commercially important clupeids. South Afr J Mar Sci 7:161–177. https://doi.org/10.2989/025776188784379017

    Article  Google Scholar 

  26. Jarić I, Bellard C, Courchamp F, Kalinkat G, Meinard Y, Roberts DL, Correia RA (2020) Societal attention toward extinction threats: a comparison between climate change and biological invasions. Sci Rep 10:11085. https://doi.org/10.1038/s41598-020-67931-5

    CAS  Article  Google Scholar 

  27. Jayaprakash AA (2002) Long term trends in rainfall, sea level and solar periodicity: a case study for forecast of Malabar sole and oil sardine fishery. J Mar Biol Assoc India 44:163–175

    Google Scholar 

  28. Jonsson B, Jonsson N, Finstad AG (2013) Effects of temperature and food quality on age and size at maturity in ectotherms: an experimental test with Atlantic salmon. J Anim Ecol 82:201–210. https://doi.org/10.1111/j.1365-2656.2012.02022.x

    Article  Google Scholar 

  29. Jorgensen T (1990) Long-term changes in age at sexual maturity of Northeast Arctic cod (Gadus morhua L.). ICES J Mar Sci 46:235–248. https://doi.org/10.1093/icesjms/46.3.235

    Article  Google Scholar 

  30. Jørgensen C, Ernande B, Fiksen Ø, Dieckmann U (2006) The logic of skipped spawning in fish. Can J Fish Aquat Sci 63:200–211. https://doi.org/10.1139/f05-210

    Article  Google Scholar 

  31. Kabir AKMA, Hossain MA, Rahmatullah SM, Dewan S, Islam MS (1998) Studies on the gonadosomatic index and fecundity of Chapila (Gudusia chapra Ham.). Bangladesh J Fish Res 2:195–200

    Google Scholar 

  32. Karnatak G, Sarkar UK, Naskar M, Roy K, Gupta S, Nandy SK, Srivastava PK, Sarkar SD, Sudheesan D, Bose AK, Verma VK (2018) Understanding the role of climatic and environmental variables in gonadal maturation and spawning periodicity of spotted snakehead, Channa punctata (Bloch, 1793) in a tropical floodplain wetland, India. Environ Biol Fish 101:595–607. https://doi.org/10.1007/s10641-018-0722-6

    Article  Google Scholar 

  33. Krabbenhoft TJ, Myers BJE, Wong JP, Chu C, Tingley RW, Falke JA, Kwak TJ, Paukert CP, Lynch AJ (2020) FiCli, the Fish and Climate Change Database, informs climate adaptation and management for freshwater fishes. Sci Data 7:124. https://doi.org/10.1038/s41597-020-0465-z

    Article  Google Scholar 

  34. Kripa V, Mohamed KS, Koya KPS, Jeyabaskaran R, Prema D, Padua S, Kuriakose S, Anilkumar PS, Nair PG, Ambrose TV, Dhanya AM, Abhilash KS, Bose J, Divya ND, Shara AS, Vishnu PG (2018) Overfishing and climate drives changes in biology and recruitment of the Indian oil sardine Sardinella longiceps in southeastern Arabian Sea. Front Mar Sci 5. https://doi.org/10.3389/fmars.2018.00443

  35. Kumari S, Sarkar UK, Mandhir SK, Lianthuamluaia L, Panda D, Chakraborty SK, Karnatak G, Kumar V, Puthiyottil M (2018) Studies on the growth and mortality of Indian River shad, Gudusia chapra (Hamilton, 1822) from Panchet reservoir, India. Environ Sci Pollut Res 25:33768–33772. https://doi.org/10.1007/s11356-018-3232-3

    Article  Google Scholar 

  36. Kumari S, Sandhya KM, Karnatak G, Lianthuamluaia L, Sarkar UK, Panda D, Mishal P (2019) Length-weight relationship and condition factor of Gudusia chapra (Hamilton, 1822) from Panchet Reservoir, Jharkhand, India. Indian J Fish 66:138–141. https://doi.org/10.21077/ijf.2019.66.3.81017-18

    Article  Google Scholar 

  37. Kumari S, Sarkar UK, Karnatak G, Mandhir SK, Lianthuamluaia L, Kumar V, Panda D, Puthiyottil M, Das BK (2020) Food selectivity and reproductive biology of small indigenous fish Indian river shad, Gudusia chapra (Hamilton, 1822) in a large tropical reservoir. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-11217-w

  38. Lappalainen A, Saks L, Šuštar M, Heikinheimo O, Jürgens K, Kokkonen E, Kurkilahti M, Verliin A, Vetemaa M (2016) Length at maturity as a potential indicator of fishing pressure effects on coastal pikeperch (Sander lucioperca) stocks in the northern Baltic Sea. Fish Res 174:47–57. https://doi.org/10.1016/j.fishres.2015.08.013

    Article  Google Scholar 

  39. Mary AA, Balasubramanian T, Selvaraju S, Shiny A (2017) Description of a new species of clupeid fish, Amblygaster indiana (Clupeiformes: Clupeidae), off Eraviputhenthurai, west coast of India. Zootaxa 4247:461. https://doi.org/10.11646/zootaxa.4247.4.7

    Article  Google Scholar 

  40. Miah MS (2015) Climatic and anthropogenic factors changing spawning pattern and production zone of Hilsa fishery in the Bay of Bengal. Weather Clim Extrem 7:109–115. https://doi.org/10.1016/j.wace.2015.01.001

    Article  Google Scholar 

  41. Mishra SS, Pradhan P, Kar S, Chakraborty SK (2003) Ichthyofaunal diversity of Midnapore, Bankura and Hooghly Districts, South West Bengal. Records of the Zoological Survey of India, Occasional Paper No. 220, 1-65. Available online at https://faunaofindia.nic.in/PDFVolumes/occpapers/220/index.pdf

  42. Mohanty BP, Behera BK, Sharma AP (2011) Nutritional significance of small indigenous fishes in human health. Bulletin No 162. CIFRI, Barrackpore. https://www.cifri.res.in/Bulletins/Bulletin%20No.185.pdf

  43. Mondal DK, Kaviraj A (2010) Feeding and reproductive biology of Indian shad Gudusia chapra in two floodplain lakes of India. Electron J Biol 6(4):98–102

    Google Scholar 

  44. Mondal G, Saha S, Islam MM, Kundu GK, Paul B, Hasan MF, Mustafa MG (2019) Reassessment of the threatened status of IUCN red listed Indian river shad Gudusia chapra (Hamilton, 1822) from Bangladesh. Dhaka Univ J Biol Sci 28(1):83–91. https://doi.org/10.3329/dujbs.v28i1.46495

    Article  Google Scholar 

  45. Murase H, Nagashima H, Yonezaki S, Matsukura R, Kitakado T (2009) Application of a generalized additive model (GAM) to reveal relationships between environmental factors and distributions of pelagic fish and krill: a case study in Sendai Bay, Japan. ICES J Mar Sci 66:1417–1424. https://doi.org/10.1093/icesjms/fsp105

    Article  Google Scholar 

  46. Myers BJE, Lynch AJ, Bunnell DB, Chu C, Falke JA, Kovach RP, Krabbenhoft TJ, Kwak TJ, Paukert CP (2017) Global synthesis of the documented and projected effects of climate change on inland fishes. Rev Fish Biol Fish 27:339–361. https://doi.org/10.1007/s11160-017-9476-z

    Article  Google Scholar 

  47. Narejo NT, Lashari PK, Laghari MY, Mastoi AM, Khoso HB (2006) Fecundity of Palri, Gudusia chapra (Hamilton) from fishponds of Chilya Hatchery (Distt. Thatta), Sindh, Pakistan. Pak J Zool 38:269

    Google Scholar 

  48. Naskar M, Roy K, Karnatak G, Nandy SK, Roy A (2018) Quantifying climate change induced threats to wetland fisheries: a stakeholder-driven approach. Environ Dev Sustain 20:2811–2830. https://doi.org/10.1007/s10668-017-0018-6

    Article  Google Scholar 

  49. Neuheimer AB, Grønkjaer P (2012) Climate effects on size-at-age: growth in warming waters compensates for earlier maturity in an exploited marine fish. Glob Chang Biol 18:1812–1822. https://doi.org/10.1111/j.1365-2486.2012.02673.x

    Article  Google Scholar 

  50. Ojaveer H, Tomkiewicz J, Arula T, Klais R (2015) Female ovarian abnormalities and reproductive failure of autumn-spawning herring (Clupea harengus membras) in the Baltic Sea. ICES J Mar Sci 72:2332–2340. https://doi.org/10.1093/icesjms/fsv103

    Article  Google Scholar 

  51. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935. https://doi.org/10.1038/nature02430

    CAS  Article  Google Scholar 

  52. Rahman MA, Haque MM (2006) Population dynamics and stock assessment of Gudusia chapra (Hamilton-Buchanan) in the Rajdhala reservoir, Netrakona, Bangladesh. Asian Fish Sci 19:281–292. Available online at http://www.cifri.res.in/ifsi/journal/year_2008_Volume40_1.htm

  53. Rahman MA, Haque MM, Khan S (2008) Food and feeding habits of Chapila, Gudusia chapra (Hamilton-Buchanan) from Rajdhala reservoir. J Inland Fish Soc India 40:13–20

    Google Scholar 

  54. Ricker WE (1981) Changes in the average size and average age of pacific salmon. Can J Fish Aquat Sci 38:1636–1656. https://doi.org/10.1139/f81-213

    Article  Google Scholar 

  55. Sahoo AK, Wahab MA, Phillips M, Rahman A, Padiyar A, Puvanendran V, Bangera R, Belton B, De DK, Meena DK, Behera BK, Sharma AP, Bhaumik U, Mohanty BP, Choudhury SR, Mohan CV (2018) Breeding and culture status of Hilsa (Tenualosa ilisha, Ham. 1822) in South Asia: a review. Rev Aquac 10:96–110. https://doi.org/10.1111/raq.12149

    Article  Google Scholar 

  56. Sandhya KM, Hassan MA, Kumari S, Mishal P, Lianthuamluaia L, Kumar V, Aftabuddin M, Meena DK (2016) Length-weight relationships of four indigenous freshwater fish species from Khalsi wetland in lower Ganga basin, West Bengal, India. J Appl Ichthyol 32:505–506. https://doi.org/10.1111/jai.13005

    Article  Google Scholar 

  57. Sandhya KM, Roy A, Hassan MA, Kumari S, Mishal P, Kumar LLV, Aftabuddin M, Bhattacharjya BK, Meena DK, Ali Y, Naskar B (2019) Traditional fishing gears, fish catch and species composition of selected floodplain wetlands of lower Gangetic plains, West Bengal, India. Fish Technol 56:101–109

    Google Scholar 

  58. Sarkar UK, Naskar M, Roy K, Sudeeshan D, Srivastava P, Gupta S, Bose AK, Verma VK, Sarkar SD, Karnatak G, Nandy SK (2017) Benchmarking pre-spawning fitness, climate preferendum of some catfishes from river Ganga and its proposed utility in climate research. Environ Monit Assess 189:491. https://doi.org/10.1007/s10661-017-6201-2

    Article  Google Scholar 

  59. Sarkar UK, Naskar M, Roy K, Sudheesan D, Gupta S, Bose AK, Srivastava PK, Nandy SK, Verma VK, Sarkar SD, Karnatak G (2018a) Baseline information of reproduction parameters of an amphidromous croaker Johnius coitor (Hamilton, 1822) from Ganga river basin, India with special reference to potential influence of climatic variability. Aquat Living Resour 31:4. https://doi.org/10.1051/alr/2017042

    Article  Google Scholar 

  60. Sarkar UK, Roy K, Karnatak G, Nandy SK (2018b) Adaptive climate change resilient indigenous fisheries strategies in the floodplain wetlands of West Bengal, India. J Water Clim Chang 9:449–462. https://doi.org/10.2166/wcc.2018.271

    Article  Google Scholar 

  61. Sarkar UK, Naskar M, Srivastava PK, Roy K, Das Sarkar S, Gupta S, Bose AK, Nandy SK, Verma VK, Sudheesan D, Karnatak G (2019a) Climato-environmental influence on breeding phenology of native catfishes in River Ganga and modeling species response to climatic variability for their conservation. Int J Biometeorol 63:991–1004. https://doi.org/10.1007/s00484-019-01703-3

    Article  Google Scholar 

  62. Sarkar UK, Roy K, Naskar M, Srivastava PK, Bose AK, Verma VK, Gupta S, Nandy SK, Sarkar SD, Karnatak G, Sudheesan D, Das BK (2019b) Minnows may be more reproductively resilient to climatic variability than anticipated: synthesis from a reproductive vulnerability assessment of Gangetic pool barbs (Puntius sophore). Ecol Indic 105:727–736. https://doi.org/10.1016/j.ecolind.2019.03.037

    Article  Google Scholar 

  63. Sarkar SD, Sarkar UK, Lianthuamluaia L, Ghosh BD, Roy K, Mishal P, Das BK (2020) Pattern of the state of eutrophication in the floodplain wetlands of eastern India in context of climate change: a comparative evaluation of 27 wetlands. Environ Monit Assess 192:183. https://doi.org/10.1007/s10661-020-8114-8

    Article  Google Scholar 

  64. Shackell NL, Frank KT, Fisher JAD, Petrie B, Leggett WC (2010) Decline in top predator body size and changing climate alter trophic structure in an oceanic ecosystem. Proc R Soc B Biol Sci 277:1353–1360. https://doi.org/10.1098/rspb.2009.1020

    Article  Google Scholar 

  65. Tu C-Y, Chen K-T, Hsieh C (2018) Fishing and temperature effects on the size structure of exploited fish stocks. Sci Rep 8:7132. https://doi.org/10.1038/s41598-018-25403-x

    CAS  Article  Google Scholar 

  66. Vinci GK, Suresh VR, Bandyopadhyaya MK (2005) Biology of Gudusia chapra (Hamilton-Buchanan) from a floodplain wetland in West Bengal. Indian J Fish 52:73–79

    Google Scholar 

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Acknowledgements

The authors are thankful to the Director, ICAR-Central Inland Fisheries Research Institute, Barrackpore. The financial help of Indian Council of Agricultural Research, New Delhi (ICAR) for funding in the project National Innovations in Climate Resilient Agriculture (NICRA) is gratefully acknowledged for this study. The second and joint author separately acknowledges the funds from Projects CENAKVA (LM2018099), Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370) for supporting him during manuscript preparation. The authors gratefully acknowledge the help of anonymous reviewers for improving this article.

Funding

The Indian Council of Agricultural Research, New Delhi (ICAR) funded the present study (financial support 100%) under the project National Innovations in Climate Resilient Agriculture (NICRA).

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Conceptualization: UKS, KR; methodology: MN, UKS, KR; formal analysis and visualization KR; investigation: GK, MP, UKS, LL, SB, SK, BDG; data collection and curation: SB, BDG, GK, MP, LL; writing - original draft preparation: KR; writing - review and editing: UKS; funding acquisition: UKS, BKD; resources: UKS, BKD; supervision: UKS.

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Correspondence to Uttam Kumar Sarkar.

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The study was a part of the national project (Government of India) – project NICRA (National Innovations in Climate Resilient Agriculture) through Indian Council of Agricultural Research (ICAR).

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All procedures performed in studies involving animals were in accordance with the ethical standards of the institution (ICAR-Central Inland Fisheries Research Institute).

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Sarkar, U.K., Roy, K., Karnatak, G. et al. Reproductive environment of the decreasing Indian river shad in Asian inland waters: disentangling the climate change and indiscriminative fishing threats. Environ Sci Pollut Res (2021). https://doi.org/10.1007/s11356-021-12852-7

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Keywords

  • Breeding thresholds
  • Breeding phenology
  • Mesh size
  • Pre-spawning girth
  • Gudusia chapra
  • Freshwater clupeids