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    Short- and long-term effects of culling invasive corallivorous gastropods

    AbstractEradicating invasive species and maintaining their populations at acceptable densities is both costly and challenging in marine environments, primarily due to the open water connectivity between culled and non-culled areas. This research aims to evaluate the short- and long-term effects of culling invasive species, considering the invasive gastropod Drupella rugosa (Born, 1778) from the coral reefs of Koh Tao (Gulf of Thailand) as a case study. Ecological, logistical, and behavioural factors that influenced the removal efforts were identified, highlighting key components that can inform future strategies aimed at managing outbreak events. Specific objectives included: (1) estimating gastropod densities and to study the behaviour of D. rugosa on Acropora-dominated reefs; (2) assessing short-term effects of D. rugosa removal by monitoring the fate of grazed corals; (3) examining the long-term impact of culling by analysing data from a removal campaign spanning over a decade, including an evaluation of the effort in terms of time and diver involvement. The relationship between damselfish and the feeding activity of corallivorous gastropods was also investigated. A key finding of this study is that poorly planned culling is ineffective in controlling outbreaks of invasive species such as those belonging to the genus Drupella. Long-term data from culling campaigns conducted between 2010 and 2024 revealed that the number of removed specimens remained relatively constant, despite significant differences in effort. This disparity underscores the lack of strategic coordination in the implementation of removal activities. Following a critical comparison with cases reported in the literature, common issues and transferable strategies were identified and thoroughly analyzed. Directions for management were provided, with the understanding that future actions should be grounded in a thorough knowledge of the species’ ecological traits, the biotic and abiotic drivers of outbreak events, a quantitative assessment of its impact on Acropora reefs, and integration into with well-established international removal and prevention programs.

    Data availability

    Data available on request by contacting both the correspondent Author ([email protected]) and the New Heaven Reef Conservation Program ([email protected]).
    ReferencesRotjan, R. & Lewis, S. Impact of coral predators on tropical reefs. Mar. Ecol. Prog. Ser. 367, 73–91. https://doi.org/10.3354/meps07531 (2008).
    Google Scholar 
    Lenihan, H. S., Holbrook, S. J., Schmitt, R. J. & Brooks, A. J. Influence of corallivory, competition, and habitat structure on coral community shifts. Ecology 92(10), 1959–1971. https://doi.org/10.1890/11-0108.1 (2011).
    Google Scholar 
    Ladd, M. C. & Shantz, A. A. Trophic interactions in coral reef restoration: A review. Food Webs. 24, e00149. https://doi.org/10.1016/j.fooweb.2020.e00149 (2020).
    Google Scholar 
    Cumming, G. S., Einarsson, L. B. & Jones, G. P. Crown-of-thorns starfish promote additional fine-grained habitat fragmentation in a coral reef ecosystem. Landsc. Ecol. 40 (5), 95. https://doi.org/10.1007/s10980-025-02107-y (2025).
    Google Scholar 
    Nicolet, K. J., Hoogenboom, M. O., Gardiner, N. M., Pratchett, M. S. & Willis, B. L. The corallivorous invertebrate Drupella aids in transmission of brown band disease on the Great Barrier Reef. Coral Reefs 32(2), 585–595. https://doi.org/10.1007/s00338-013-1010-8 (2013).
    Google Scholar 
    Sussman, S. W. & Siegal, W. S. Informational influence in organizations: an integrated approach to knowledge adoption. Inf. Syst. Res. 14 (1), 47–65. https://doi.org/10.1287/isre.14.1.47.14767 (2003).
    Google Scholar 
    Turner, S. Spatial variability in the abundance of the corallivorous gastropod Drupella cornus. Coral Reefs 13, 41–48. https://doi.org/10.1007/BF00426434 (1994).
    Google Scholar 
    Zhang, F., Jia, X., Lin, Z., Jiang, Y. & Qu, M. The outbreak of drupella snails and its catastrophic effects on coral reefs: a comprehensive review. Front. Mar. Sci. 10, 1290001. https://doi.org/10.3389/fmars.2023.1290001 (2024).
    Google Scholar 
    Ayling, A. M. & Ayling, A. L. Ningaloo Marine Park: Preliminary Fish Density Assessment and Habitat Survey (Sea Research, 1987).Taylor, J. D. & Reid, D. G. The abundance and trophic classification of molluscs upon coral reefs in the Sudanese Red Sea. J. Nat. Hist. 18(2), 175–209. https://doi.org/10.1080/00222938400770151 (1984).
    Google Scholar 
    Johnson, M. S. & Cumming, R. L. Genetic distinctness of three widespread and morphologically variable species of Drupella (Gastropoda, Muricidae). Coral Reefs 14(2), 71–78. https://doi.org/10.1007/BF00303426 (1995).
    Google Scholar 
    Claremont, M., Reid, D. G. & Williams, S. T. Evolution of corallivory in the gastropod genus Drupella. Coral Reefs. 30, 977–990. https://doi.org/10.1007/s00338-011-0788-5 (2011).
    Google Scholar 
    Kita, M. et al. Feeding attractants for the muricid gastropod Drupella cornus, a coral predator. Tetrahedron Lett. 46(49), 8583–8585. https://doi.org/10.1016/j.tetlet.2005.09.182 (2005).
    Google Scholar 
    Bessey, C., Babcock, R. C., Thomson, D. P. & Haywood, M. D. E. Outbreak densities of the coral predator Drupella in relation to in situ Acropora growth rates on Ningaloo Reef, Western Australia. Coral Reefs 37(4), 985–993. https://doi.org/10.1007/s00338-018-01748-7 (2018).
    Google Scholar 
    Morton, B., Blackmore, G. & Kwok, C. T. Corallivory and prey choice by Drupella rugosa (Gastropoda:Muricidae) in Hong Kong. J. Molluscan Stud. 68(3), 217–223. https://doi.org/10.1093/mollus/68.3.217 (2002).
    Google Scholar 
    Moerland, M. S., Scott, C. M. & Hoeksema, B. W. Prey selection of corallivorous muricids at Koh Tao (Gulf of Thailand) four years after a major coral bleaching event. Contrib. Zool. 85 (3), 291–309. https://doi.org/10.1163/18759866-08503003 (2016).
    Google Scholar 
    Scott, C. M., Mehrotra, R., Cabral, M. & Arunrugstichai, S. Changes in hard coral abundance and composition on Koh Tao, Thailand, 2006–2014. Coast Ecosyst. 4, 26–38 (2017).
    Google Scholar 
    Hsieh, H. J. et al. Establishment of a no-take area (NTA) could not guarantee the preservation of coral communities in Chinwan inner Bay, Penghu, Taiwan. Zool. Stud. 50, 443–453 (2011).
    Google Scholar 
    Kaullysing, D., Taleb-Hossenkhan, N., Kulkarni, B. G. & Bhagooli, R. A first field report of various coral-eating gastropods and associated infestations around Mauritius Island, Western Indian ocean. West Indian Ocean. J. Mar. Sci. (1), 73–75 (2017).Bruckner, A. W. Priorities for Effective Management of Coral Diseases (U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, 2002).Samsuri, A. N. et al. The effectiveness of Trapezia cymodoce in defending its host coral Pocillopora acuta against corallivorous Drupella. Mar. Biol. 165(4), 70. https://doi.org/10.1007/s00227-018-3330-2 (2018).
    Google Scholar 
    Forde, F. J. M. Populations, behaviour and effects of drupella cornus on the Ningaloo reef. Conserv. Land. Manage. 92, 45–50 (1992).
    Google Scholar 
    Schoepf, V., Herler, J. & Zuschin, M. Microhabitat use and prey selection of the coral-feeding snail Drupella cornus in the northern Red Sea. Hydrobiologia 641(1), 45–57. https://doi.org/10.1007/s10750-009-0053-x (2010).
    Google Scholar 
    Hoeksema, B. W., Scott, C. & True, J. D. Dietary shift in corallivorous drupella snails following a major bleaching event at Koh Tao, Gulf of Thailand. Coral Reefs. 32 (2), 423–428. https://doi.org/10.1007/s00338-012-1005-x (2013).
    Google Scholar 
    Lei, X. et al. Spatial variability In the abundance and prey selection of the corallivorous snail drupella spp. In the southeastern Hainan Island, China. Front. Mar. Sci. 9, 990113. https://doi.org/10.3389/fmars.2022.990113 (2022).
    Google Scholar 
    Moore, R. J. Is Acanthaster planci an r-strategist?. Nature 271(5640), 56–57. https://doi.org/10.1038/271056a0 (1978).
    Google Scholar 
    Levitan, D. R. ‘The ecology of fertilization in free-spawning invertebrates.’ In Ecology of Marine Invertebrate Larvae 123–156 (CRC, 2020).
    Google Scholar 
    Pechenik, J. On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar. Ecol. Prog Ser. 177, 269–297. https://doi.org/10.3354/meps177269 (1999).
    Google Scholar 
    Underwood, A. J. Supply-side ecology: The natural and consequences of variations in recruitment of intertidal organisms. Mar. Community Ecol. (2001).Kitamura, T., Shigematsu, Y., Iwai, T., Miura, C. & Miura, T. The spawning season of Drupella fragum in southwestern Shikoku. Biogeography. https://doi.org/10.11358/biogeo.24.32 (2022).
    Google Scholar 
    Scott, C. M., Mehrotra, R., Hein, M. Y., Moerland, M. S. & Hoeksema, B. W. Population dynamics of corallivores (Drupella and Acanthaster) on coral reefs of Koh Tao, a diving destination in the Gulf of Thailand. Raffles Bull. Zool. 65 (2017).Canteri, B. Investigating climate change and nutrient pollution effects on Drupella rugosa coral reef destruction in Koh-Tao, Thailand. Plymouth Stud. Sci. 17 (2), 14. https://doi.org/10.70156/1754-2383.1494 (2024).
    Google Scholar 
    Pratchett, M. S. & Cumming, G. S. Managing cross-scale dynamics in marine conservation: Pest irruptions and lessons from culling of crown-of-thorns starfish (Acanthaster spp). Biol. Conserv. 238, 108211. https://doi.org/10.1016/j.biocon.2019.108211 (2019).
    Google Scholar 
    Giakoumi, S. et al. Management priorities for marine invasive species. Sci. Total Environ. 688, 976–982. https://doi.org/10.1016/j.scitotenv.2019.06.282 (2019).
    Google Scholar 
    Simberloff, D. Maintenance management and eradication of established aquatic invaders. Hydrobiologia 848(9), 2399–2420. https://doi.org/10.1007/s10750-020-04352-5 (2021).
    Google Scholar 
    Thresher, R. E. & Kuris, A. M. Options for managing invasive marine species. Biol. Invasions 6(3), 295–300. https://doi.org/10.1023/B:BINV.0000034598.28718.2e (2004).
    Google Scholar 
    Baruffaldi, M. et al. Coral health status before and after the tourism halt caused by the COVID-19 pandemic in Koh Tao (Thailand). Coral Reefs https://doi.org/10.1007/s00338-025-02706-w (2025).
    Google Scholar 
    Saponari, L., Dehnert, I., Galli, P. & Montano, S. Assessing population collapse of Drupella spp. (Mollusca: Gastropoda) 2 years after a coral bleaching event in the Republic of Maldives. Hydrobiologia 848(11), 2653–2666. https://doi.org/10.1007/s10750-021-04546-5 (2021).
    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag New York, 2016). https://ggplot2.tidyverse.orgFox, J. & Weisberg, S. An R Companion to Applied Regression, Third (Sage, 2019). https://www.john-fox.ca/CompanionKassambara, A. ‘rstatix: pipe-friendly framework for basic statistical tests (R package version 0.7.0)’. (2021). https://CRAN.R-project.org/package=rstatixCore Team, R. R: a language and environment for statistical com- puting. R Foundation for Statistical Computing, Vienna, Austria. (2025). https://www.R-project.orgFontoura-da-Silva, V., Cardoso, R. S. & Caetano, C. H. S. Mark–recapture versus length–frequency based methods: evaluation using a marine gastropod as a model. J. Exp. Mar. Biol. Ecol. 474, 171–179. https://doi.org/10.1016/j.jembe.2015.10.013 (2016).
    Google Scholar 
    Rempel, H. S., Bodwin, K. N. & Ruttenberg, B. I. Impacts of parrotfish predation on a major reef-building coral: quantifying healing rates and thresholds of coral recovery. Coral Reefs 39(5), 1441–1452. https://doi.org/10.1007/s00338-020-01977-9 (2020).
    Google Scholar 
    Cumming, R. L. Case Study: Impact of Drupella spp. On reef-building Corals of the Great Barrier Reef (Great Barrier Reef Marine Park Authority, 2009).Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9(7), 671–675. https://doi.org/10.1038/nmeth.2089 (2012).
    Google Scholar 
    Tiddy, I. C. et al. Outplanting of branching acropora enhances recolonization of a fish species and protects massive corals from predation. Coral Reefs. 40 (5), 1549–1561. https://doi.org/10.1007/s00338-021-02147-1 (2021).
    Google Scholar 
    Schopmeyer, S. A. & Lirman, D. Occupation dynamics and impacts of damselfish territoriality on recovering populations of the threatened Staghorn coral, Acropora cervicornis. PLoS ONE. 10 (11), e0141302. https://doi.org/10.1371/journal.pone.0141302 (2015).
    Google Scholar 
    Losey, G. S. Jr. The ecological importance of cleaning symbiosis. Copeia https://doi.org/10.2307/1442741 (1972).
    Google Scholar 
    Sam, S. et al. First observation of Drupella rugosa egg capsules on scleractinian coral Pocillopora damicornis. Bull. Mar. Sci. 92(3), 353–354. https://doi.org/10.5343/bms.2016.1062 (2016).
    Google Scholar 
    Sam, S. Q. et al. Egg capsules and veligers of the corallivorous muricid gastropod Drupella rugosa (Born, 1778). Invertebr Reprod. Dev. 61(3), 164–171. https://doi.org/10.1080/07924259.2017.1315343 (2017).
    Google Scholar 
    Ben-Ari, H., Paz, M. & Sher, D. The chemical armament of reef-building corals: inter- and intra-specific variation and the identification of an unusual actinoporin in Stylophora pistilata. Sci. Rep. 8 (1), 1–13. https://doi.org/10.1038/s41598-017-18355-1 (2018).
    Google Scholar 
    Potts, D. C. Suppression of coral populations by filamentous algae within damselfish territories. J. Exp. Mar. Biol. Ecol. 28(3), 207–216. https://doi.org/10.1016/0022-0981(77)90092-2 (1977).
    Google Scholar 
    Reinthal, P. N. & Macintyre, I. G. Spatial and Temporal variations in grazing pressure by herbivorous fishes: tobacco Reef, Belize. Atoll Res. Bull. 425, 1–11. https://doi.org/10.5479/si.00775630.425.1 (1994).
    Google Scholar 
    Monchanin, C., Desmolles, M. & Mehrotra, R. Homogenization and distinction of coral recruit communities between natural and artificial substrates at Koh Tao a decade after deployment. Aquat. Ecol. 59 (2), 597–608. https://doi.org/10.1007/s10452-025-10182-1 (2025).
    Google Scholar 
    Zavaleta, E. S., Hobbs, R. J. & Mooney, H. A. Viewing invasive species removal in a whole-ecosystem context. Trends Ecol. Evol. 16, 454–459. https://doi.org/10.1016/S0169-5347(01)02194-2 (2001).
    Google Scholar 
    Côté, I. M., Akins, L., Underwood, E., Curtis-Quick, J. & Green, S. J. Setting the record straight on invasive lionfish control: culling works. PeerJ Prepr. 2, e398v1 (2014).
    Google Scholar 
    Weterings, R. ‘A GIS-based assessment of threats to the natural environment on Koh Tao, Thailand. Agric. Nat. Resour. 45(4), 743–755 (2011).
    Google Scholar 
    Haslam, V. M., Bessey, C., Chaplin, J. A. & van Keulen, M. Evidence of corallivorous gastropod drupella cornus breeding on the higher latitude reefs of Rottnest Island (32° S), Western Australia. Mar. Biol. 171 (1), 28. https://doi.org/10.1007/s00227-023-04352-8 (2024).
    Google Scholar 
    Costello, M. J. et al. Biological and ecological traits of marine species. PeerJ 3, e1201. https://doi.org/10.7717/peerj.1201 (2015).
    Google Scholar 
    Marchesi, V. et al. A baseline for the conservation of the native and protected Centrostephanus longispinus (Philippi, 1845) and the management of the invasive Diadema setosum (Leske, 1778) (Echinoidea: diadematidae) in the mediterranean sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 35 (5), 1–12. https://doi.org/10.1002/aqc.70155 (2025).
    Google Scholar 
    Green, S. J. & Grosholz, E. D. Functional eradication as a framework for invasive species control. Front. Ecol. Environ. 19 (2), 98–107. https://doi.org/10.1002/fee.2277 (2021).
    Google Scholar 
    Hulme, P. E. Beyond control: wider implications for the management of biological invasions. J. Appl. Ecol. 43 (5), 835–847. https://doi.org/10.1111/j.1365-2664.2006.01227.x (2006).
    Google Scholar 
    Pluess, T. et al. When are eradication campaigns successful? A test of common assumptions. Biol. Invasions 14(7), 1365–1378. https://doi.org/10.1007/s10530-011-0160-2 (2012).
    Google Scholar 
    Osborne, S. & Williams, M. R. A preliminary summary of the effects of hand removal of Drupella cornus on Ningaloo Reef. In Drupella cornus: A Synopsis, 83–90 (1992).Williams, D. E., Miller, M. W., Bright, A. J. & Cameron, C. M. Removal of corallivorous snails as a proactive tool for the conservation of acroporid corals. PeerJ 2, e680. https://doi.org/10.7717/peerj.680 (2014).
    Google Scholar 
    Williams, S. L. & Grosholz, E. D. The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries Coasts 31(1), 3–20. https://doi.org/10.1007/s12237-007-9031-6 (2008).
    Google Scholar 
    Ojaveer, H. et al. Classification of non-indigenous species based on their impacts: considerations for application in marine management. PLoS Biol. 13 (4), e1002130. https://doi.org/10.1371/journal.pbio.1002130 (2015).
    Google Scholar 
    Yamaguchi, M. Acanthaster planci infestations of reefs and coral assemblages in japan: a retrospective analysis of control efforts. Coral Reefs. 5, 23–30. https://doi.org/10.1007/BF00302168 (1986).
    Google Scholar 
    Rivera-Posada, J. Size-related variation in arm damage frequency in the crown-of-thorns sea star, Acanthaster planci. J. Coast Life Med. https://doi.org/10.12980/JCLM.2.2014J52 (2014).
    Google Scholar 
    Westcott, D. A. et al. Relative efficacy of three approaches to mitigate Crown-of-Thorns starfish outbreaks on australia’s great barrier reef. Sci. Rep. 10 (1), 12594. https://doi.org/10.1038/s41598-020-69466-1 (2020).
    Google Scholar 
    Strand, H. K., Christie, H., Fagerli, C. W., Mengede, M. & Moy, F. Optimizing the use of quicklime (CaO) for sea urchin management—a lab and field study. Ecol. Eng. 143, 100018. https://doi.org/10.1016/j.ecoena.2020.100018 (2020).
    Google Scholar 
    Christie, H. et al. Successful large-scale and long-term Kelp forest restoration by culling sea urchins with quicklime and supported by crab predation. Mar. Biol. 171 (11), 211. https://doi.org/10.1007/s00227-024-04540-0 (2024).
    Google Scholar 
    Miller, M. W. Corallivorous snail removal: evaluation of impact on Acropora palmata. Coral Reefs 19(3), 293–295. https://doi.org/10.1007/PL00006963 (2001).
    Google Scholar 
    Tracey, S. R. et al. Systematic culling controls a climate driven, habitat modifying invader. Biol. Invasions. 17 (6), 1885–1896. https://doi.org/10.1007/s10530-015-0845-z (2015).
    Google Scholar 
    Ling, S. D. & Keane, J. P. Resurvey of the longspined sea urchin (Centrostephanus rodgersii) and associated barren reef in Tasmania. (2018). https://doi.org/10.13140/RG.2.2.16363.80162Sanderson, J. C., Ling, S. D., Dominguez, J. G. & Johnson, C. R. Limited effectiveness of divers to mitigate barrens formation by culling sea urchins while fishing for abalone. Mar. Freshw. Res. 67(1), 84–95. https://doi.org/10.1071/MF14255 (2015).
    Google Scholar 
    Usseglio, P., Selwyn, J. D., Downey-Wall, A. M. & Hogan, J. D. Effectiveness of removals of the invasive lionfish: how many dives are needed to deplete a reef? PeerJ 5, e3043. https://doi.org/10.7717/peerj.3043 (2017).
    Google Scholar 
    Morris, J. A., Sullivan, C. V. & Govoni, J. J. Oogenesis and spawn formation in the invasive lionfish, Pterois miles and Pterois volitans. Sci. Mar. 75(1), 147–154. https://doi.org/10.3989/scimar.2011.75n1147 (2011).
    Google Scholar 
    Bohn, K., Richardson, C. A. & Jenkins, S. R. The importance of larval supply, larval habitat selection and post-settlement mortality in determining intertidal adult abundance of the invasive gastropod Crepidula fornicata. J. Exp. Mar. Biol. Ecol. 440, 132–140. https://doi.org/10.1016/j.jembe.2012.12.008 (2013).
    Google Scholar 
    Phillips, W. N. Tourism threats to coral reef resilience at Koh Sak, Pattaya Bay. Environ. Nat. Resour. J. https://doi.org/10.14456/ENNRJ.2015.3 (2015).
    Google Scholar 
    Artificial intelligence in invasive species management: Transforming detection and response. Trends Anim. Plant. Sci. 4, 82–96. https://doi.org/10.62324/TAPS/2024.050 (2024).Katsanevakis, S. et al. Marine invasive alien species in europe: 9 years after the IAS regulation. Front. Mar. Sci. 10, 1271755. https://doi.org/10.3389/fmars.2023.1271755 (2023).
    Google Scholar 
    Holmes, R. B., Matchette, S. R. & Herbert-Read, J. E. Citizen science reveals relationships between human hunting pressure and the abundance and behaviour of invasive lionfish (Pterois spp.). Biol. Invasions 27(6), 141. https://doi.org/10.1007/s10530-025-03596-3 (2025).
    Google Scholar 
    Malpica-Cruz, L. et al. Trying to collapse a population for conservation: commercial trade of a marine invasive species by artisanal fishers. Rev. Fish. Biol. Fish. 31 (3), 667–683. https://doi.org/10.1007/s11160-021-09660-0 (2021).
    Google Scholar 
    Download referencesAcknowledgementsWe would like to thank New Heaven Reef Conservation and above all Kirsty Magson, the program manager, for providing part of the data and making this study possible. We are also deeply grateful to all the volunteers who, over the years, have contributed to the collection of data and to the implementation of the research.FundingNo Funding.Author informationAuthors and AffiliationsNew Heaven Reef Conservation Program, 48 Moo 3, Chalok Ban Kao, Koh Tao, 84360, ThailandBaruffaldi MatildeDepartment of Life and Environmental Sciences (DiSVA), Università Politecnica delle Marche, Via Brecce Bianche s.n.c, 60131, Ancona, ItalyBaruffaldi Matilde, Roveta Camilla, Tonolini Rosita, Pulido Mantas Torcuato & Cristina Gioia Di CamilloNational Biodiversity Future Center (NBFC), Piazza Marina 61, 90133, Palermo, ItalyRoveta Camilla, Pulido Mantas Torcuato & Cristina Gioia Di CamilloConsorzio Nazionale Interuniversitario per le Scienze del Mare (CoNISMa), Piazzale Flaminio 9, 00196, Rome, ItalyCristina Gioia Di CamilloAuthorsBaruffaldi MatildeView author publicationsSearch author on:PubMed Google ScholarRoveta CamillaView author publicationsSearch author on:PubMed Google ScholarTonolini RositaView author publicationsSearch author on:PubMed Google ScholarPulido Mantas TorcuatoView author publicationsSearch author on:PubMed Google ScholarCristina Gioia Di CamilloView author publicationsSearch author on:PubMed Google ScholarContributionsDi Camillo CG and Baruffaldi M contributed to the study conception and design. Baruffaldi M and Di Camillo CG wrote the first draft of the paper and provided figures. Baruffaldi M and Tonolini R performed samplings and collected data. Roveta C, Baruffaldi M, Pulido Mantas T analyzed data. All authors contributed to improve and revise the manuscript.Corresponding authorCorrespondence to
    Cristina Gioia Di Camillo.Ethics declarations

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    Reprints and permissionsAbout this articleCite this articleMatilde, B., Camilla, R., Rosita, T. et al. Short- and long-term effects of culling invasive corallivorous gastropods.
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    Evidence for dilution effect by Gobio gobio, a dead-end host in the Unio crassus–Cyprinidae coevolutionary system

    AbstractFreshwater mussels (Unionidae) depend on specific fish hosts to complete their life cycle. Glochidia, their parasitic larvae, must attach to the gills or fins of suitable fish species to metamorphose. However, non-host fish may intercept glochidia, reducing larval availability for competent hosts—a phenomenon known as the dilution effect. We investigated this mechanism in a natural population of the endangered mussel Unio crassus, focusing on the interaction between the dominating host Phoxinus phoxinus and the non-host Gobio gobio. Field surveys across three separate reaches of the Warkocz River (2015–2016) and a controlled infestation experiment demonstrated that G. gobio removes a substantial proportion of glochidia without supporting their metamorphosis. Co-occurrence analysis showed a negative relation between infestation levels of G. gobio vs. P. phoxinus, with a significant interaction modulated by U. crassus density. At low mussel densities, the impact of G. gobio on parasitic success was strongest. Gobio gobio was recorded at 90% of the known U. crassus localities in Poland, and in all of these sites it formed a dominant component of the fish assemblage. Our findings provide direct evidence of a context-dependent dilution effect and highlight the importance of fish community composition and behaviour in conservation of unionid mussels. The presence of non-host fish in habitats with low mussel abundance may undermine recruitment and increase extinction risk in fragmented populations.

    Data availability

    The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

    References
    Buckingham, L. J. & Ashby, B. Coevolutionary theory of hosts and parasites. J. Evol. Biol. 35, 205–224 (2022).
    Google Scholar 
    Colwell, R. K., Dunn, R. R. & Harris, N. C. Coextinction and persistence of dependent species in a changing world. Annu. Rev. Ecol. Evol. Syst. 43, 183–203 (2012).
    Google Scholar 
    Johnson, P. T. J. & Thieltges, D. W. Diversity, decoys and the Dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 213, 961–970 (2010).
    Google Scholar 
    Chase, J. M., Blowes, S. A., Knight, T. M., Gerstner, K. & May, F. Ecosystem decay exacerbates biodiversity loss with habitat loss. Nature 584, 238–243 (2020).
    Google Scholar 
    Lagrue, C. & Poulin, R. Local diversity reduces infection risk across multiple freshwater host-parasite associations. Freshw. Biol. 60, 2445–2454 (2015).
    Google Scholar 
    Ostfeld, R. S. & Keesing, F. Biodiversity and disease risk: the case of Lyme disease. Conserv. Biol. 14, 722–728 (2000).
    Google Scholar 
    Combes, C. & Moné, H. Possible mechanisms of the decoy effect in schistosoma mansoni transmission. Int. J. Parasitol. 17, 971–975 (1987).
    Google Scholar 
    Kat, P. W. Parasitism and the Unionacea (Bivalvia). Biol. Rev. 59, 189–207 (1984).
    Google Scholar 
    Modesto, V. et al. Fish and mussels: importance of fish for freshwater mussel conservation. Fish. Fish. 19, 244–259 (2018).
    Google Scholar 
    Zając, K. et al. On the reintroduction of the endangered thick-shelled river mussel Unio crassus: the importance of the river’s longitudinal profile. Sci. Total Environ. 624, 273–282 (2018).
    Google Scholar 
    Aldridge, D. C. et al. Fishing for hosts: larval spurting by the endangered thick-shelled river mussel. Ecology 104, e4026 (2023).
    Google Scholar 
    Ćmiel, A. M., Zając, K., Lipińska, A. M. & Zając, T. Glochidial infestation of fish by the endangered thick-shelled river mussel Unio crassus. Aquat. Conserv. 28, 535–544 (2018).
    Google Scholar 
    Ćmiel, A. M. et al. The size and shape of parasitic larvae of naiads (Unionidae) are not dependent on female size. Sci. Rep. 11, 23755 (2021).
    Google Scholar 
    Zając, K., Zając, T. & Ćmiel, A. What can we infer from the shell dimensions of the thick-shelled river mussel Unio crassus? Hydrobiologia 810, 415–431 (2018).
    Google Scholar 
    Strayer, D. L. Freshwater Mussel Ecology: A Multifactor Approach To Distribution and Abundance. (University of California Press, 2008).Taeubert, J. E., Martinez, A. M. P., Gum, B. & Geist, J. The relationship between endangered thick-shelled river mussel (Unio crassus) and its host fishes. Biol. Conserv. 155, 94–103 (2012).
    Google Scholar 
    Barnhart, M. C., Haag, W. R. & Roston, W. N. Adaptations to host infection and larval parasitism in Unionoida. J. N Am. Benthol Soc. 27, 370–394 (2008).
    Google Scholar 
    Jansen, W., Bauer, G. & Zahner-Meike, E. Glochidial mortality in freshwater mussels. In: Bauer, G. & Wachtler, K. (eds) Ecology and Evolutionary Biology of the Freshwater Mussels Unionoidea. Ecological Studies. 145 185–211 (Springer, 2001).Culp, J. J., Haag, W. R., Arrington, D. A. & Kennedy, T. B. Seasonal and species-specific patterns in abundance of freshwater mussel glochidia in stream drift. J. N Am. Benthol Soc. 30, 436–445 (2011).
    Google Scholar 
    Dartnall, H. J. G. & Walkey, M. The distribution of glochidia of the Swan mussel, Anodonta cygnea (Mollusca), on the three-spined stickleback Gasterosteus aculeatus (Pisces). J. Zool. 189, 31–37 (1979).
    Google Scholar 
    Zale, A. V. & Neves, R. J. Fish hosts of four species of lampsiline mussels (Mollusca: Unionidae) in big moccasin Creek, Virginia. Can. J. Zool. 60, 2535–2542 (1982).
    Google Scholar 
    Neves, R. J., Weaver, L. R. & Zale, A. V. An evaluation of host suitability for glochidia of Villosa vanuxemi and V. nebulosa (Pelecypoda: Unionidae). Am. Midl. Nat. 113, 13–19 (1985).
    Google Scholar 
    Nicholson, A. J. An outline of the dynamics of animal populations. Aust J. Zool. 2, 9–65 (1954).
    Google Scholar 
    Terui, A., Miyazaki, Y., Yoshioka, A. & Matsuzaki, S. I. S. A cryptic allee effect: Spatial contexts mask an existing fitness–density relationship. R Soc. Open. Sci. 2, 150034 (2015).
    Google Scholar 
    Zając, T. A. & Zając, K. Spawning in a threatened freshwater mussel shifts to earlier dates as a result of increasing summer mortality. Sci. Rep. 15, 7733 (2025).
    Google Scholar 
    Zając, K. & Zając, T. A. The role of active individual movement in habitat selection in the endangered freshwater mussel Unio crassus Philipsson 1788. J. Conchol. 40, 446–461 (2011).
    Google Scholar 
    Denic, M., Stoeckl, K., Gum, B. & Geist, J. Physicochemical assessment of Unio crassus habitat quality in a small upland stream and implications for conservation. Hydrobiologia 735, 111–122 (2014).
    Google Scholar 
    Wanzenböck, J. Ontogeny of prey capture in the minnow, Phoxinus Phoxinus. Environ. Biol. Fish. 42, 61–74 (1995).
    Google Scholar 
    Museth, J., Borgstrøm, R., Brittain, J. E. & Herberg, I. Diet of the minnow (Phoxinus phoxinus) in humic lakes: food resource partitioning in species-poor fish communities. Hydrobiologia 477, 31–39 (2002).
    Google Scholar 
    Vinyoles, D., De Sostoa, A. & Lobón-Cerviá, J. Ecology of Gobio Gobio in Iberian streams: life history traits, diet, and habitat use. Folia Zool. 56, 57–70 (2007).
    Google Scholar 
    Aldridge, D. C. & McIvor, A. L. Gill evacuation and release of glochidia by Unio pictorum and Unio tumidus (Bivalvia: Unionidae) under thermal and hypoxic stress. J. Molluscan Stud. 69, 55–59 (2003).
    Google Scholar 
    Eby, L. A., Roach, W. J., Crowder, L. B. & Stanford, J. A. Effects of stocking-up freshwater food webs. Trends Ecol. Evol. 21, 576–584 (2006).
    Google Scholar 
    Gimenez, M., Villéger, S., Grenouillet, G. & Cucherousset, J. Stocking practices shape the taxonomic and functional diversity of fish communities in gravel pit lakes. Fish. Manag Ecol. 30, 603–614 (2023).
    Google Scholar 
    Moore, T. P. & Clearwater, S. J. Non-native fish as glochidial sinks: elucidating disruption pathways for echyridella menziesii recruitment. Hydrobiologia 848, 3191–3207 (2021).
    Google Scholar 
    Elosegi, A., Diez, J. R. & Mutz, M. Effects of hydromorphological integrity on biodiversity and functioning of river ecosystems. Hydrobiologia 657, 199–215 (2010).
    Google Scholar 
    Stoeckl, K., Taeubert, J. E. & Geist, J. Fish species composition and host fish density in streams of the thick-shelled river mussel (Unio crassus) – implications for conservation. Aquat. Conserv. 25, 276–287 (2015).
    Google Scholar 
    Douda, K. et al. Host compatibility as a critical factor in management unit recognition: Population‐level differences in mussel–fish relationships. J. Appl. Ecol. 51, 1085–1095 (2014).
    Google Scholar 
    Keesing, F., Holt, R. D. & Ostfeld, R. S. Effects of species diversity on disease risk. Ecol. Lett. 9, 485–498 (2006).
    Google Scholar 
    Zając, K. & Zając, T. A. Seasonal patterns in the developmental rate of glochidia in the endangered thick-shelled river mussel, Unio crassus Philipsson, 1788. Hydrobiologia 848, 3077–3091 (2021).
    Google Scholar 
    Taeubert, J. E., El-Nobi, G. & Geist, J. Effects of water temperature on the larval parasitic stage of the thick‐shelled river mussel (Unio crassus). Aquat. Conserv. 24, 231–237 (2014).
    Google Scholar 
    Lopes-Lima, M. et al. A curated dataset on the distribution of West Palaearctic freshwater bivalves. Scientific Data 12, 1139 (2025).
    Google Scholar 
    Download referencesAcknowledgementsThe study was supported by statutory funds of the Institute of Nature Conservation, Polish Academy of Sciences. The study was conducted on the basis of permit WNP.6401.190.2014.RN-2, granted to study a protected species (U. crassus). J.D. and K.T. holds a license for conducting electrofishing in accordance with Polish legal requirements.Author informationAuthors and AffiliationsInstitute of Nature Conservation, Polish Academy of Sciences, Al. Adama Mickiewicza 33, Kraków, 31-120, PolandJacek Dołęga, Tadeusz A. Zając, Adam Ćmiel, Anna Lipińska, Krzysztof Tatoj & Katarzyna ZającAuthorsJacek DołęgaView author publicationsSearch author on:PubMed Google ScholarTadeusz A. ZającView author publicationsSearch author on:PubMed Google ScholarAdam ĆmielView author publicationsSearch author on:PubMed Google ScholarAnna LipińskaView author publicationsSearch author on:PubMed Google ScholarKrzysztof TatojView author publicationsSearch author on:PubMed Google ScholarKatarzyna ZającView author publicationsSearch author on:PubMed Google ScholarContributionsJ.D. and T.A.Z. conceived the idea and designed the study. A.M.Ć., J.D., A.L., K.T., K.Z. and T.A.Z. collected the data. J.D., T.A.Z. A.M.Ć., and K.Z. analysed, interpreted and visualised the data. J.D. and T.A.Z. wrote the main text of the manuscript. All authors reviewed the manuscript.Corresponding authorCorrespondence to
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    Reprints and permissionsAbout this articleCite this articleDołęga, J., Zając, T.A., Ćmiel, A. et al. Evidence for dilution effect by Gobio gobio, a dead-end host in the Unio crassus–Cyprinidae coevolutionary system.
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    Computational analysis and modeling of climate impact on Pteridium aquilinum (L.) populations

    AbstractPteridium aquilinum is a medicinally important fern with a limited range in northern Iran, increasingly threatened by climate change. Using morphological, genetic, and environmental data, we assessed differentiation, adaptive capacity, and vulnerability across 11 populations. Factor analysis of mixed data (FAMD) identified stipe indument, pinnule shape, and pinnae number as key traits distinguishing populations. Redundancy and association analyses (RDA/CCA) revealed strong links between both morphological and genetic variation and climatic gradients, particularly temperature and humidity, indicating local adaptation. Several SCoT loci were detected as adaptive outliers. Spatial PCA showed that variation is shaped by both global and local spatial factors, forming clines and local variants. Populations varied in sensitivity and adaptive capacity; populations 2, 3, 7, and 8 exhibited the lowest adaptive indices and highest vulnerability. Connectivity modeling suggested that while some populations (e.g., 2, 4, and 6) may maintain or slightly improve connectivity, others risk isolation under future climates. Structural equation modeling (SEM) indicated a positive genetic contribution to adaptation, while differential equation modeling (DEM) predicted logistic growth with temporary instability and genetic decline in vulnerable groups. Overall, findings highlight spatially uneven adaptive responses and recommend targeted conservation through connectivity enhancement, assisted gene flow, and ex-situ preservation of adaptive genotypes.

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    The datasets used and/ or analyzed during the current study available from the corresponding author on reasonable request.
    ReferencesIPCC. Climate Change 2022: Impacts, Adaptation and Vulnerability (Cambridge University Press, 2022).Kelly, S. A., Panhuis, T. M. & Stoehr, A. M. Phenotypic plasticity: molecular mechanisms and adaptive significance. Compreh Physiol. 9 (2), 259–303 (2019).
    Google Scholar 
    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).
    Google Scholar 
    Scheiner, S. M., Barfield, M. & Holt, R. D. The genetics of phenotypic plasticity. XVII. Response to climate change. Ecol. Evol. 9 (22), 12375–12389 (2019).
    Google Scholar 
    Christmas, M. J., Breed, M. F. & Lowe, A. J. Constraints to and conservation implications for climate change adaptation in plants. Conserv. Genet. 17 (2), 305–320 (2016).
    Google Scholar 
    Corlett, R. T. Climate change and the evolution of the next generation of tropical forest trees. Perspect. Plant. Ecol. Evol. Syst. 13 (1), 163–172 (2011).
    Google Scholar 
    Guan, B., Gao, J., Chen, W., Gong, X. & Ge, G. The effects of climate change on landscape connectivity and genetic clusters in a small subtropical and warm-temperate tree. Front. Plant. Sci. 12, 671336 (2021).
    Google Scholar 
    Foden, W. B. et al. Climate change vulnerability assessment of species. Wiley Interdiscip Rev. Clim. Change. 4 (3), 159–181 (2013).
    Google Scholar 
    Mair, L., O’Brien, G. S. D. W. & Purvis, A. The forgotten half of the species-area relationship. Ecol. Appl. 31 (8), e02447 (2021).Guisan, A., Edwards, T. C. & Hastie, T. Generalized linear and non-linear models for predicting species distributions. Ecol. Modell. 257, 1–17 (2013).
    Google Scholar 
    Moran, R. C. Diversity, biogeography, and floristics. In Biology and Evolution of Ferns and Lycophytes, 367–395 (Cambridge University Press, Cambridge, (2008).
    Google Scholar 
    Higgins, M. A. et al. Geological control of floristic composition in Amazonian forests. J. Biogeogr. 38 (11), 2136–2149 (2011).
    Google Scholar 
    Karst, J., Gilbert, B. & Lechowicz, M. J. Fern community assembly. Ecology 86 (9), 2473–2486 (2005).
    Google Scholar 
    Della, A. P. & Falkenberg, D. D. B. Pteridophytes as ecological indicators: an overview. Hoehnea 46 (1), e522018 (2019).
    Google Scholar 
    Sheidai, M., Alaeifar, M. & Koohdar, F. Integrating Geostatistical approaches into landscape genetics. Plant Mol. Biol. Rep. 1–12 (2025).Christenhusz, M. et al. Pteridium Pinetorum (The IUCN Red List of Threatened Species, 2017).CABI. Pteridium aquilinum (bracken). CABI Compendium. (2020).Davis, M. B. & Shaw, R. G. Range shifts and adaptive responses to quaternary climate change. Science 292 (5517), 673–679 (2001).
    Google Scholar 
    Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant. Sci. 15 (12), 684–692 (2010).
    Google Scholar 
    Bradshaw, A. D. Unraveling phenotypic plasticity. New. Phytol. 170 (4), 644–648 (2006).
    Google Scholar 
    Reed, T. E., Schindler, D. E. & Waples, R. S. Phenotypic plasticity and evolution in population persistence. Conserv. Biol. 25 (1), 56–63 (2011).
    Google Scholar 
    Sheidai, M., Alaeifar, M. & Koohdar, F. PLS-SEM in plant ecological studies. Ecol. Modell. 500, 110–125 (2024).
    Google Scholar 
    Cruzan, M. B. & Hendrickson, E. C. Landscape genetics of plants. Plant. Commun. 1 (6), 100100 (2020).
    Google Scholar 
    Thurman, L. L., Stein, B. & Beever, E. A. Adaptive capacity of species to climate change. Front. Ecol. Environ. 18 (9), 499–507 (2020).
    Google Scholar 
    Fortini, L., Loehman, R. A. & Holsinger, L. M. Adaptive capacity of Pinus radiata. Glob Change Biol. 23 (1), 160–170 (2017).
    Google Scholar 
    Arnold, P. A., Kruuk, L. E. B. & Nicotra, A. B. Analyzing plant phenotypic plasticity. New. Phytol. 22 (3), 1235–1241 (2019).
    Google Scholar 
    Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).
    Google Scholar 
    Thuiller, W. et al. Predicting global change impacts on plants. Perspect. Plant. Ecol. Evol. Syst. 9 (3–4), 137–152 (2008).
    Google Scholar 
    Jones, M. M. et al. Environmental heterogeneity and ferns. J. Ecol. 94 (1), 181–195 (2006).
    Google Scholar 
    FAO. GIEWS Country Brief: Iran (FAO, 2020).Zohary, M. Geobotanical Foundations of the Middle East (Gustav Fischer, 1973).Alaeifar, M., Sheidai, M. & Koohdar, F. Genetic diversity of Pteridium aquilinum. Plant Genet. Resour. 1–8 (2025).Ahmed, N. et al. Purchase intention toward organic food. J. Environ. Plan. Manag. 64 (5), 796–822 (2021).
    Google Scholar 
    Pagès, J. Multiple Factor Analysis by Example Using R (CRC, 2014).Lê, S., Josse, J. & Husson, F. FactoMineR: an R package. J. Stat. Softw. 25, 1–18 (2008).
    Google Scholar 
    Husson, F., Lê, S. & Pagès, J. Exploratory Multivariate Analysis Using R (CRC, 2011).Jolliffe, I. Principal component analysis. In International Encyclopedia of Statistical Science, 1094–1096 (Springer, (2011).
    Google Scholar 
    Legendre, P. & Legendre, L. F. L. Numerical Ecology (Elsevier, 2012).Forester, B. R. et al. Detecting multilocus adaptation. Mol. Ecol. 27 (9), 2215–2233 (2018).
    Google Scholar 
    Zuur, A. F. et al. Data exploration protocol. Methods Ecol. Evol. 1 (1), 3–14 (2010).
    Google Scholar 
    Jombart, T., Devillard, S. & Balloux, F. Spatial analysis of genetic variation. Genetics 178 (3), 1679–1691 (2008).
    Google Scholar 
    Hoban, S. et al. Genomic basis of local adaptation. Am. Nat. 188 (4), 379–397 (2016).
    Google Scholar 
    François, O. et al. Controlling false discoveries. Mol. Ecol. 25 (2), 454–469 (2016).
    Google Scholar 
    Andrews, K. R. et al. RADseq in genomics. Nat. Rev. Genet. 17 (2), 81–92 (2016).
    Google Scholar 
    Nussey, D. H. et al. Phenotypic plasticity in natural populations. J. Evol. Biol. 20 (2), 891–903 (2007).
    Google Scholar 
    Hadfield, J. D. MCMC methods for GLMM. (2009).Sexton, J. P. et al. Isolation by environment or distance. Evolution 68 (1), 1–15 (2014).
    Google Scholar 
    Sunday, J. M. et al. Thermal tolerance in ectotherms. Proc. R Soc. B. 278 (1713), 1823–1830 (2011).
    Google Scholar 
    Valladares, F., Matesanz, S. & Niinemets, Ü. Environmental stress and evolution. Biol. Rev. 89 (3), 564–582 (2014).
    Google Scholar 
    Dawson, T. P. et al. Biodiversity conservation in changing climate. Science 332 (6025), 53–58 (2011).
    Google Scholar 
    Young, B. E. et al. Climate change vulnerability index. Wildl. Soc. Bull. 39 (1), 174–181 (2015).
    Google Scholar 
    Wessels, C., Merow, C. & Trisos, C. H. Climate change risk to wild food plants. Reg. Environ. Change. 21 (2), 29 (2021).
    Google Scholar 
    Rinnan, D. S. & Lawler, J. Climate-niche factor analysis. Ecography 42 (9), 1494–1503 (2019).
    Google Scholar 
    Gienapp, P. et al. Environmental vs. genetic effects. Ecol. Lett. 11 (7), 633–643 (2008).
    Google Scholar 
    Wasserman, D. et al. EPA guidance on suicide treatment. Eur. Psychiatry. 27 (2), 129–141 (2012).
    Google Scholar 
    Krosby, M. et al. Ecological connectivity. Conserv. Biol. 24 (6), 1686–1689 (2010).
    Google Scholar 
    Fick, S. E. & Hijmans, R. J. WorldClim 2. Int. J. Climatol. 37 (12), 4302–4315 (2017).
    Google Scholar 
    Dormann, C. F. et al. Collinearity Rev. Ecography 36 (1), 27–46 (2013).
    Google Scholar 
    Dijkstra, E. W. A note on two problems in connection with graphs. Numer. Math. 1 (1), 269–271 (1959).
    Google Scholar 
    Inoue, K. & Berg, D. J. Climate change and Cumberlandia monodonta. Glob Change Biol. 23 (1), 94–107 (2017).
    Google Scholar 
    McRae, B. H. Isolation by resistance. Evolution 60 (8), 1551–1561 (2006).
    Google Scholar 
    Manel, S. et al. Landscape genetics. Trends Ecol. Evol. 18 (4), 189–197 (2003).
    Google Scholar 
    Balkenhol, N. et al. Landscape Genetics: Concepts, Methods, Applications (Wiley-Blackwell, 2015).Hoffmann, A. A. & Sgrò, C. M. Climate change and evolutionary adaptation. Nature 470 (7335), 479–485 (2011).
    Google Scholar 
    Spear, S. F. et al. Resistance surfaces in landscape genetics. Mol. Ecol. 19 (17), 3576–3591 (2010).
    Google Scholar 
    Grace, J. B. Structural Equation Modeling and Natural Systems (Cambridge University Press, 2010).Soetaert, K. et al. DeSolve package. J. Stat. Softw. 33 (9), 1–25 (2010).
    Google Scholar 
    Ixaru, L. G. & Vanden Berghe, G. Runge–Kutta solvers. In Exponential Fitting, 165–186 (Springer, 2004).
    Google Scholar 
    Transtrum, M. K. & Sethna, J. P. Improvements to Levenberg–Marquardt. https://arxiv.org/abs/1201.5885 (2012).Moré, J. J. The Levenberg–Marquardt algorithm. In Numerical Analysis, 105–116 (Springer, 1978).
    Google Scholar 
    Gao, X. et al. Climate change and firmiana Kwangsiensis. Ecol. Evol. 12 (8), e9165 (2022).
    Google Scholar 
    Mittal, S. Threats to biodiversity. Global Biodiversity Outlook 2 (United Nations Environment Programme, Nairobi, (2019).
    Google Scholar 
    Spathelf, P. et al. Adaptive forest management. Ann. Sci. 75, 55 (2018).
    Google Scholar 
    Li, Y. et al. Landscape genomics. Front. Plant. Sci. 8, 2136 (2017).
    Google Scholar 
    Buzatti, R. S. O. et al. Leaf trait variation. Front. Plant. Sci. 10, 1580 (2019).
    Google Scholar 
    Sexton, J. P. et al. Adaptive responses to climate change. Evol. Appl. 2 (2), 185–197 (2009).
    Google Scholar 
    Hampe, A. & Petit, R. J. Conserving biodiversity. Front. Ecol. Environ. 3 (10), 542–550 (2005).
    Google Scholar 
    Ghasemian, S. et al. Persian squirrel genetics. Ecol. Evol. 13 (7), e10318582 (2023).
    Google Scholar 
    Gholamali-Fard, N. et al. Gene flow barriers in lizards. Zool. Scr. 49 (6), 738–751 (2020).
    Google Scholar 
    Dolatkhahi, F. et al. Genetic diversity of Dracocephalum kotschyi. Hort Environ. Biotechnol. 60 (5), 767–777 (2019).
    Google Scholar 
    Matesanz, S., Gianoli, E. & Valladares, F. Global change and plant plasticity. Ann. N Y Acad. Sci. 1206 (1), 35–55 (2010).
    Google Scholar 
    Sultan, S. E. Phenotypic plasticity. Trends Plant. Sci. 5 (12), 537–542 (2000).
    Google Scholar 
    Agustí, J. & Blázquez, M. A. Plant vascular development. Cell. Mol. Life Sci. 77 (19), 3711–3728 (2020).
    Google Scholar 
    Ehleringer, J. R. Leaf morphology and stress. Oecologia 47 (3), 307–310 (1980).
    Google Scholar 
    Johnson, H. B. Plant pubescence. Bot. Rev. 41 (3), 233–258 (1975).
    Google Scholar 
    Levin, D. A. Role of trichomes. Q. Rev. Biol. 48 (1), 3–15 (1973).
    Google Scholar 
    Read, J., Sanson, G. D. & Watt, A. D. Leaf shape and function. New. Phytol. 204 (2), 263–278 (2014).
    Google Scholar 
    Nicotra, A. B. et al. Plasticity in changing climate. Funct. Ecol. 25 (1), 237–251 (2011).
    Google Scholar 
    Givnish, T. J. Leaf form significance. In Topics in Plant Population Biology. 375–404 (Cambridge University Press, 1979).
    Google Scholar 
    Vogel, S. Convective cooling and leaf shape. J. Exp. Bot. 21 (4), 91–101 (1970).
    Google Scholar 
    Nobel, P. S. Physicochemical and Environmental Plant Physiology (Academic, 2009).Parkhurst, D. F. & Mott, K. A. Gas exchange within leaves. Plant. Cell. Environ. 13 (7), 697–707 (1990).
    Google Scholar 
    Whitmore, T. C. Tropical Rain Forests of the Far East (Oxford University Press, 1984).Givnish, T. J. Leaf form. In Topics in Plant Population Biology. 375–407 (Cambridge University Press, 1978).
    Google Scholar 
    Habel, J. C. et al. Genetic drift in orchids. Biol. Conserv. 144 (12), 3020–3027 (2011).
    Google Scholar 
    Row, J. R. et al. Landscape features and salamander genetics. Conserv. Genet. 15 (3), 667–680 (2014).
    Google Scholar 
    Geffen, E., Anderson, M. J. & Wayne, R. K. Dispersal barriers in wolves. Mol. Ecol. 13 (10), 2481–2490 (2004).
    Google Scholar 
    Gosper, C. R. et al. Flora conservation and OCBIL theory. Biol. J. Linn. Soc. 133 (2), 373–393 (2021).
    Google Scholar 
    Download referencesAuthor informationAuthors and AffiliationsDepartment of Plant Sciences and Biotechnology, Faculty of Life Sciences & Biotechnology, Shahid Beheshti University, Tehran, IranMasoud Sheidai, Maedeh Alaeifar & Fahimeh KoohdarAuthorsMasoud SheidaiView author publicationsSearch author on:PubMed Google ScholarMaedeh AlaeifarView author publicationsSearch author on:PubMed Google ScholarFahimeh KoohdarView author publicationsSearch author on:PubMed Google ScholarContributionsM. Sh. and F. K. Conceptualization of the project, designed the research, analysis and wrote the manuscript and M. A. collected the samples and lab work. All authors reviewed the manuscript.Corresponding authorCorrespondence to
    Masoud Sheidai.Ethics declarations

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    The authors declare no competing interests.

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    Long-term effects of nitrogen fertilization on methane emissions in drained tropical peatland

    Abstract

    Nitrogen (N) fertilization improves crop productivity. However, the long-term effects of N application on methane (CH4) emissions in drained peat soils, particularly under different hydrological conditions, remain poorly understood. Accurate quantification of CH4 emissions from peatlands is essential for assessing carbon losses and formulating effective climate change mitigation strategies. This study was conducted to investigate the impact of N fertilization on CH4 emissions and identify the main factors influencing CH4 emissions from drained tropical peatlands. This study was conducted on an oil palm plantation in Sarawak, Malaysia, a randomized block design included four N fertilizer treatments: Control (0 kg N ha− 1 yr− 1) (T1); low (31.1 kg N ha⁻¹ yr⁻¹) (T2), moderate (62.2 kg N ha⁻¹ yr⁻¹) (T3), and high (124.3 kg N ha⁻¹ yr⁻¹) (T4). Soil CH4 fluxes showed no statistically significant differences between treatments or across years, with emissions ranging from − 163.6 to 320.7 µg C m− 2 hr− 1 at T1, -86.7 to 285.8 µg C m− 2 hr− 1 at T2, -131.6 to 274.1 µg C m− 2 hr− 1 at T3 and − 125.7 to 185.9 µg C m− 2 hr− 1 at T4 (p > 0.05). Although ammonium sulfate fertilization did not significantly alter CH4 emissions, its pronounced acidifying effect on soil pH, particularly at application rates above 62.2 kg N ha⁻¹ yr⁻¹ along with elevated sulfate (SO42−) inputs and nitrogen pools exceeding the critical threshold (> 400 ppm), likely suppressed methanogenic activity and constrained soil organic matter decomposition. Water-filled pore space (WFPS) influenced CH4 emissions more than groundwater level (GWL), with the low GWL at the site limiting its impact. Increased WFPS (60–80%) reduced nitrate (NO3−) through enhanced denitrification, lowering its inhibition on CH4 production and thus increasing emissions. This study highlights the key role of soil moisture and nitrogen cycling in regulating CH4 emissions in peatland.

    Data availability

    The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.
    ReferencesIPCC, A. Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, 1535. (2013). Wang, Z., Zeng, D. & Patrick, W. H. Methane emissions from natural wetlands. Environ. Monit. Assess. 42, 143–161. https://doi.org/10.1007/BF00394047 (1996).
    Google Scholar 
    Li, C., Grayson, R., Holden, J. & Li, P. Erosion in peatlands: recent research progress and future directions. Earth Sci. Rev. 185, 870–886. https://doi.org/10.1016/j.earscirev.2018.08.005 (2018).
    Google Scholar 
    Xu, J., Morris, P. J., Liu, J. & Holden, J. P. E. A. T. M. A. P. Refining estimates of global peatland distribution based on a meta-analysis. Catena 160, 134–140. https://doi.org/10.1016/j.catena.2017.09.010 (2018).
    Google Scholar 
    Ribeiro, K. et al. Tropical peatlands and their contribution to the global carbon cycle and climate change. Glob. Change Biol. 27 (3), 489–505. https://doi.org/10.1111/gcb.15408 (2021).
    Google Scholar 
    Mishra, S. et al. Degradation of Southeast Asian tropical peatlands and integrated strategies for their better management and restoration. J. Applied Ecology. 58 (7), 1370–1387. https://doi.org/10.1111/1365-2664.13905 (2021).
    Google Scholar 
    Omar, M. S. et al. Peatlands in Southeast asia: A comprehensive geological review. Earth Sci. Rev. 104149 https://doi.org/10.1016/j.earscirev.2022.104149 (2022).Page, S. et al. Anthropogenic impacts on lowland tropical peatland biogeochemistry. Nat. Reviews Earth Environ. 3 (7), 426–443. https://doi.org/10.1038/s43017-022-00289-6 (2022).
    Google Scholar 
    Hooijer, A. et al. Current and future CO2 emissions from drained peatlands in Southeast Asia. Biogeosciences 7 (5), 1505–1514. https://doi.org/10.5194/bg-7-1505-2010 (2010).
    Google Scholar 
    Oktarita, S., Hergoualc’h, K., Anwar, S. & Verchot, L. V. Substantial N2O emissions from peat decomposition and N fertilization in an oil palm plantation exacerbated by hotspots. Environ. Res. Lett. 12 (10), 104007. https://doi.org/10.1088/1748-9326/aa80f1 (2017).
    Google Scholar 
    Hergoualc’h, K. A. & Verchot, L. V. Changes in soil CH4 fluxes from the conversion of tropical peat swamp forests: a meta-analysis. J. Integr. Environ. Sci. 9 (2), 93–101. https://doi.org/10.1080/1943815X.2012.747252 (2012).
    Google Scholar 
    Hirano, T., Jauhiainen, J., Inoue, T. & Takahashi, H. Controls on the carbon balance of tropical peatlands. Ecosystems 12, 873–887. https://doi.org/10.1007/s10021-008-9209-1 (2009).
    Google Scholar 
    Deshmukh, C. S. et al. Impact of forest plantation on methane emissions from tropical peatland. Glob. Change Biol. 26 (4), 2477–2495. https://doi.org/10.1111/gcb.15019 (2020).
    Google Scholar 
    Le Mer, J. & Roger, P. Production, oxidation, emission and consumption of methane by soils: a review. Eur. J. Soil Biol. 37 (1), 25–50. https://doi.org/10.1016/S1164-5563(01)01067-6 (2001).
    Google Scholar 
    van Lent, J., Hergoualc’h, K., Verchot, L., Oenema, O. & van Groenigen, J. W. Greenhouse gas emissions along a peat swamp forest degradation gradient in the Peruvian amazon: soil moisture and palm roots effects. Mitig. Adapt. Strat. Glob. Change. 24, 625–643. https://doi.org/10.1007/s11027-018-9796-x (2019).
    Google Scholar 
    Watanabe, A. et al. CO2 fluxes from an Indonesian peatland used for Sago palm (Metroxylon Sagu Rottb.) cultivation: effects of fertilizer and groundwater level management. Agric. Ecosyst. Environ. 134 (1–2), 14–18. https://doi.org/10.1016/j.agee.2009.06.015 (2009).
    Google Scholar 
    Swails, E., Hergoualc’h, K., Verchot, L., Novita, N. & Lawrence, D. Spatio-temporal variability of peat CH4 and N2O fluxes and their contribution to peat GHG budgets in Indonesian forests and oil palm plantations. Front. Environ. Sci. 9, 617828. https://doi.org/10.3389/fenvs.2021.617828 (2021).
    Google Scholar 
    Luta, W. et al. Water table fluctuation and methane emission in pineapples (Ananas comosus (L.) Merr.) cultivated on a tropical peatland. Agronomy 11 (8), 1448. https://doi.org/10.3390/agronomy11081448 (2021).
    Google Scholar 
    Couwenberg, J., Dommain, R. & Joosten, H. Greenhouse gas fluxes from tropical peatlands in south-east Asia. Glob. Change Biol. 16 (6), 1715–1732. https://doi.org/10.1111/j.1365-2486.2009.02016.x (2010).
    Google Scholar 
    Hatano, R. Impact of land use change on greenhouse gases emissions in peatland: a review. Int. Agrophys. 33 (2), 167–173. https://doi.org/10.31545/intagr/109238 (2019).
    Google Scholar 
    Chaddy, A. et al. Effects of long-term nitrogen fertilization and ground water level changes on soil CO2 fluxes from oil palm plantation on tropical peatland. Atmosphere 12 (10), 1340. https://doi.org/10.3390/atmos12101340 (2021).
    Google Scholar 
    Hadi, A. et al. Greenhouse gas emissions from tropical peatlands of Kalimantan, Indonesia. Nutr. Cycl. Agrosyst. 71, 73–80. https://doi.org/10.1007/s10705-004-0380-2 (2005).
    Google Scholar 
    Li, Q., Peng, C., Zhang, J., Li, Y. & Song, X. Nitrogen addition decreases methane uptake caused by methanotroph and methanogen imbalances in a Moso bamboo forest. Sci. Rep. 11 (1), 1–14. https://doi.org/10.1038/s41598-021-84422-3 (2021).
    Google Scholar 
    Banger, K., Tian, H. & Lu, C. Do nitrogen fertilizers stimulate or inhibit methane emissions from rice fields? Glob. Change Biol. 18 (10), 3259–3267. https://doi.org/10.1111/j.1365-2486.2012.02762.x (2012).
    Google Scholar 
    Sun, B., Zhao, H., Lu, F. & Wang, X. The effects of nitrogen fertilizer application on methane and nitrous oxide emission/uptake in Chinese croplands. J. Integr. Agric. 15 (2), 440–450. https://doi.org/10.1016/S2095-3119(15)61063-2 (2016).
    Google Scholar 
    Conrad, R. Microbial ecology of methanogens and methanotrophs. Adv. Agron. 96, 1–63. https://doi.org/10.1016/S0065-2113(07)96005-8 (2007).
    Google Scholar 
    Laanbroek, H. J. Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. Mini-Review Annals Bot. 105 (1), 141–153. https://doi.org/10.1093/aob/mcp201 (2010).
    Google Scholar 
    Bodelier, P. L. E. & Laanbroek, H. J. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol. Ecol. 47 (3), 265–277. https://doi.org/10.1016/S0168-6496(03)00304-0 (2004).
    Google Scholar 
    Kambara, H. et al. Environmental factors affecting the community of methane-oxidizing bacteria. Microbes Environ. 37 (1), ME21074. https://doi.org/10.1264/jsme2.ME21074 (2022).
    Google Scholar 
    Aulakh, M. S., Wassmann, R. & Rennenberg, H. Methane emissions from rice fields—quantification, mechanisms, role of management, and mitigation options. Adv. Agron. 70, 193–260. https://doi.org/10.1016/S0065-2113(01)70006-5 (2001).
    Google Scholar 
    Steudler, P. A., Bowden, R. D., Melillo, J. M. & Aber, J. D. Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341 (6240), 314–316. https://doi.org/10.1038/341314a0 (1989).
    Google Scholar 
    Mosier, A. R. & Delgado, J. A. Methane and nitrous oxide fluxes in grasslands in Western Puerto Rico. Chemosphere 35 (9), 2059–2082. https://doi.org/10.1016/S0045-6535(97)00231-2 (1997).
    Google Scholar 
    Wang, J. et al. Nitrate addition inhibited methanogenesis in paddy soils under long-term managements. Plant. Soil. Environ. 64 (8), 393–399. https://doi.org/10.17221/231/2018-PSE (2018).
    Google Scholar 
    Basiron, Y. Palm oil production through sustainable plantations. Eur. J. Lipid Sci. Technol. 109 (4), 289–295. https://doi.org/10.1002/ejlt.200600223 (2007).
    Google Scholar 
    Chaddy, A., Melling, L., Ishikura, K. & Hatano, R. Soil N2O emissions under different N rates in an oil palm plantation on tropical peatland. Agriculture 9 (10), 213. https://doi.org/10.3390/agriculture9100213 (2019).
    Google Scholar 
    Hasnol, O., Farawahida, M. D., Mohd, H. & Samsudin A Re-evaluation of nutrients requirements for oil palm planting on peat soil. Planter 90 (1056), 161–177 (2014).
    Google Scholar 
    Keeney, D. R. & Nelson, D. W. Nitrogen in organic forms. In (eds Page, A. L., Miller, R. H. & Keeney, D. R.) Methods of Soil Analysis. Part 2. Agronomy No. 9, American Society of Agronomy, Madison, WI, 643–698. (1982).
    Google Scholar 
    Salehi, M. H., Beni, O. H., Harchegani, H. B., Borujeni, I. E. & Motaghian, H. R. Refining soil organic matter determination by loss-on-ignition. Pedosphere 21 (4), 473–482. https://doi.org/10.1016/S1002-0160(11)60149-5 (2011).
    Google Scholar 
    Melling, L., Goh, K. J. & Hatano, R. Short-term effect of Urea on CH4 flux under the oil palm (Elaeis guineensis) on tropical peatland in Sarawak, Malaysia. Soil. Sci. Plant. Nutr. 52 (6), 788–792. https://doi.org/10.1111/j.1747-0765.2006.00092.x (2006).
    Google Scholar 
    Fageria, N. K., Dos Santos, A. B. & Moraes, M. F. Influence of Urea and ammonium sulfate on soil acidity indices in lowland rice production. Commun. Soil Sci. Plant Anal. 41 (13), 1565–1575. https://doi.org/10.1080/00103624.2010.485237 (2010).
    Google Scholar 
    Wang, Z. P., Delaune, R. D., Patrick, W. H. Jr & Masscheleyn, P. H. Soil redox and pH effects on methane production in a flooded rice soil. Soil Sci. Soc. Am. J. 57 (2), 382–385. https://doi.org/10.2136/sssaj1993.03615995005700020016x (1993).
    Google Scholar 
    Cai, Z. et al. Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilizers and water management. Plant. Soil. 196, 7–14. https://doi.org/10.1023/A:1004263405020 (1997).
    Google Scholar 
    Minamikawa, K., Sakai, N. & Yagi, K. Methane emission from paddy fields and its mitigation options on a field scale. Microbes Environ. 21 (3), 135–147. https://doi.org/10.1264/jsme2.21.135 (2006).
    Google Scholar 
    Ro, S., Seanjan, P., Tulaphitak, T. & Inubushi, K. Sulfate content influencing methane production and emission from incubated soil and rice-planted soil in Northeast Thailand. Soil. Sci. Plant. Nutr. 57 (6), 833–842. https://doi.org/10.1080/00380768.2011.637302 (2011).
    Google Scholar 
    Kim, S. Y., Veraart, A. J., Meima-Franke, M. & Bodelier, P. L. Combined effects of carbon, nitrogen and phosphorus on CH4 production and denitrification in wetland sediments. Geoderma 259, 354–361. https://doi.org/10.1016/j.geoderma.2015.03.015 (2015).
    Google Scholar 
    Cai, Z., Shan, Y. & Xu, H. Effects of nitrogen fertilization on CH4 emissions from rice fields. Soil. Sci. Plant. Nutr. 53 (4), 353–361. https://doi.org/10.1111/j.1747-0765.2007.00153.x (2007).
    Google Scholar 
    Girkin, N. T., Turner, B. L., Ostle, N., Craigon, J. & Sjögersten, S. Root exudate analogues accelerate CO2 and CH4 production in tropical peat. Soil Biol. Biochem. 117, 48–55. https://doi.org/10.1016/j.soilbio.2017.11.008 (2018).
    Google Scholar 
    Ishikura, K. et al. Carbon dioxide and methane emissions from peat soil in an undrained tropical peat swamp forest. Ecosystems 22, 1852–1868. https://doi.org/10.1007/s10021-019-00376-8 (2019).
    Google Scholar 
    Azizan, S. N. F. et al. Comparing GHG emissions from drained oil palm and recovering tropical peatland forests in Malaysia. Water 13, 3372. https://doi.org/10.3390/w13233372 (2021).
    Google Scholar 
    Busman, N. A. et al. Soil CO2 and CH4 fluxes from different forest types in tropical peat swamp forest. Sci. Total Environ. 858, 159973. https://doi.org/10.1016/j.scitotenv.2022.159973 (2023).
    Google Scholar 
    Melling, L. & Hatano, R. Goh. K.J. Methane fluxes from three ecosystems in tropical peatland of Sarawak, Malaysia. Soil Biol. Biochem. 37 (8), 1445–1453. https://doi.org/10.1016/j.soilbio.2005.01.001 (2005).
    Google Scholar 
    Jovani-Sancho, A. J. et al. CH4 and N2O emissions from smallholder agricultural systems on tropical peatlands in Southeast Asia. Glob. Change Biol. 29 (15), 4279–4297. https://doi.org/10.1111/gcb.16747 (2023).
    Google Scholar 
    Murdiyarso, D., Hergoualc’h, K. & Verchot, L. V. Opportunities for reducing greenhouse gas emissions in tropical peatlands. Proc. Natl. Acad. Sci. 107 (46), 19655–19660. https://doi.org/10.1073/pnas.0911966107 (2010).
    Google Scholar 
    Sjögersten, S. et al. Temperature response of ex-situ greenhouse gas emissions from tropical peatlands: interactions between forest type and peat moisture conditions. Geoderma 324, 47–55. https://doi.org/10.1016/j.geoderma.2018.02.029 (2018).
    Google Scholar 
    Download referencesAcknowledgementsWe would like to express our sincere gratitude for the generous support from the Sarawak State Government and the Federal Government of Malaysia for making this research possible. We would also like to express our sincere appreciation to the dedicated staff of the Sarawak Tropical Peat Research Institute (TROPI) for their invaluable technical assistance and unwavering support throughout every phase of this study, including the challenging fieldwork. Their expertise and dedication contributed greatly to the successful completion of this study.FundingThis research was funded by the Federal Government of Malaysia and the Sarawak State Government.Author informationAuthors and AffiliationsSarawak Tropical Peat Research Institute, Kuching-Samarahan Expressway, Kota Samarahan, Sarawak, 94300, MalaysiaAuldry Chaddy, Faustina Elfrida Sangok, Sharon Yu Ling Lau & Lulie MellingAuthorsAuldry ChaddyView author publicationsSearch author on:PubMed Google ScholarFaustina Elfrida SangokView author publicationsSearch author on:PubMed Google ScholarSharon Yu Ling LauView author publicationsSearch author on:PubMed Google ScholarLulie MellingView author publicationsSearch author on:PubMed Google ScholarContributionsLiterature collection, data collection and analysis were performed by Auldry Chaddy, Faustina Elfrida Sangok, and Sharon Yu Ling Lau. The first draft of the manuscript was written by Auldry Chaddy. Faustina Elfrida Sangok, Sharon Lau Yu Ling and Lulie Melling revised the draft. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.Corresponding authorCorrespondence to
    Auldry Chaddy.Ethics declarations

    Competing interests
    The authors declare no competing interests.

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    Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
    Reprints and permissionsAbout this articleCite this articleChaddy, A., Sangok, F.E., Lau, S.Y.L. et al. Long-term effects of nitrogen fertilization on methane emissions in drained tropical peatland.
    Sci Rep (2025). https://doi.org/10.1038/s41598-025-32378-zDownload citationReceived: 24 May 2025Accepted: 09 December 2025Published: 18 December 2025DOI: https://doi.org/10.1038/s41598-025-32378-zShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy shareable link to clipboard
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    Bridging agriculture, health and industry through plant molecular farming in the bioeconomic era

    AbstractGlobal food production requires a major upheaval to feed a burgeoning human population despite multiple disruptors, ranging from climate change to geopolitical instability. Innovation and a policy shift that focuses on the Bioeconomy could address these challenges. This Perspective highlights plant cellular agriculture, molecular farming, and plant cell culture as a potential “fourth pillar” that could diversify supply and produce high-value compounds associated with regulatory uncertainty, cost, and energy constraints.

    IntroductionEvery person deserves appropriate nutrition. Our world approaches a human population of 10 billion within the next 30 years, with global food demand increasing by more than 50% during this time period1.By 2050, global food demand is projected to increase by 50–60% compared to 2010 levels, with protein demand expected to double in some regions2. This growing demand encompasses diverse nutritional needs, including high-energy staples such as rice, wheat, and maize to ensure calorie sufficiency; high-quality proteins from sources like meat, dairy, plant-based alternatives, and novel proteins to support nutrition security3; and high-value foods such as functional ingredients and specialty crops that contribute to economic diversification. Global food systems are undergoing an upheaval, with vulnerabilities such as economic shocks due to tariff changes, the risk of zoonotic infectious diseases such as bovine influenza in the US, and geopolitical conflict such as grain shortages due to the Russian- Ukraine war. Collectively, these disruptions have greatly affected food prices and availability4. However, scaling up supply across these categories is challenged by the impacts of climate change, dietary shifts driven by urbanization and rising affluence, as well as policy and trade uncertainties5.In response, and due to concerns about global food security issues, many nations such as the US are trying to change the way they produce food, to mitigate global shocks of all nature, and to decentralize yet strengthen food supply chains to reduce their vulnerabilities6. The most noteworthy way this is taking place is by investing in novel strategies to produce alternative proteins. Alternative proteins, then, refer to those made that are equally as nutritious as conventional animal proteins, but are cheaper, require fewer inputs, have a lower carbon footprint, and are resilient to climate shocks7.Alternative protein production should reduce the load of zoonotic diseases as well as agricultural pest pressures and other exacerbating problems associated with livestock production, ranging from antimicrobial resistance to animal cruelty, from fair trade to bioterrorism8. Decentralizing our food production to an abundance of smaller locations would mitigate these problems substantially. The overall effect will be a shift in trade relations from one that is fixed due to geography, to one that is fluid and unconstrained.Alternative protein technologies for food are often placed into three main categories: cultivated meat, plant-based protein, and precision fermentation9. Cultivated, or cell-based meat, refers to the production of meat cells in culture to produce a food product such as hamburger, sausage or chicken nuggets. Plant-based proteins can be defined as proteins which have been processed in such a way that they resemble animal sourced products, such as oat milk. Precision fermentation covers the use of microbial fermentation systems to produce individual animal protein in a manner that more closely resembles the technology used in the past to produce pharmaceutical proteins. This synthetic biology approach includes the incorporation of a gene encoding an animal protein into the genome of a bacterial or fungal strain, which is then cultivated in a bioreactor to produce large amounts of target proteins, such as casein and whey. These three pillars represent the fundamentals of alternative protein production.A fourth ‘pillar’ has been defined as a facet of cellular agriculture based on plant molecular farming and plant cell culture technologies. Plant molecular farming refers to the use of plants themselves to replace microbial bioreactors, in such a way that a gene of interest is expressed and extracted from plants instead of from microbes10. Plant cellular agriculture, on the other hand, makes use of plant cell culture to produce large amounts of plant biomass which can be processed into food products, analogous to some of the cultivated meat production technologies11. Plant molecular farming and plant cell culture have been proposed as a potential “fourth pillar” of alternative proteins, though their precise definition and boundaries remain debated within the field.The following Perspective presents various examples of this fourth pillar of alternative plant cell-based technologies and describes the advantages that it has over the others. The Perspective concludes with a prediction of the prospects of plant cellular agriculture to address the widening cracks found within our current food system.Plant molecular farmingPlant molecular farming can be defined as the use of plants as a production platform to express a target protein12. Originally a production platform for pharmaceutical proteins (molecular pharming) that was developed over a quarter of a century ago, the technology has matured to such an extent that animal food proteins found in dairy, meat and eggs have become a more recent series of products under development. A great advantage of plant molecular farming is that in place of costly bioreactors, greenhouses or farm fields can be used to produce the protein of interest, thus mitigating the economic and environmental costs associated with farming livestock13. Plant molecular farming thus does not encounter scaling challenges the way other protein production platforms, such as precision fermentation, must face. Plants can perform post translational modifications that more resemble their animal counterparts, thus enabling them to follow a form and functionality that is superior to proteins produced in many microbial systems14. Animal proteins can be produced and stored in a wide diversity of plant tissues, such as potato tubers, rice grains, and legumes such as peas and soybeans15. Since these are edible tissues, it is feasible that partial purification of the protein in question may be sufficient, or, depending on the circumstances, completely unnecessary. Originally, this technology was adapted by companies such as Medicago, iBio and Kentucky Bioprocessing Co, to produce vaccines, monoclonal antibodies and other biologics16. Today, over 30 molecular farming companies can be found which produce different animal food proteins. Examples include Argentinian company Moolec (recently merged with Bioceres group limited), which produces the heme protein myoglobin in soybean and pea that can be processed into iron loaded products such as textured vegetable protein (valorasoy.com). Alpine Bio (formally Nobell Foods), based in San Francisco produces dairy proteins such as casein for cheese in soybean (alpbio.com). PoloPo is an Israeli company which produces the egg protein ovalbumin in potato tubers (PoLopo.tech). In Europe, molecular farming company Nambawan Spain produces and purifies sweet proteins such as thaumatin in transgenic tobacco seed (namba-wan.com).The key steps to plant molecular farming include determining the appropriate mode of animal gene delivery to crops, then optimizing expression levels, scaling-up to produce the desired amount of protein and finally, purification of protein, if required. Animal genes can be introduced via stable transformation to produce transgenic plants, or transiently, using replicating constructs based on virus expression vectors17. To date, largely transgenic plants have been created which express the target protein; these crops can be produced in the field or greenhouse and the protein extracted using standard agricultural techniques. Limitations for these processes include regulatory issues for GMOs (for plants grown in the open field) and scale up limitations (for plants grown in the greenhouse). Transient expression performed in the greenhouse using virus expression vectors can increase yield considerably and can be introduced to field crops using novel spray technologies, which are currently under development18.Expression levels can vary depending on the type of protein being produced (this problem exists for precision fermentation as well) and the tissue that it is expressed in, as well as environmental factors such as temperature and humidity. Oilseed crops, like soy, for example, have been shown to express myoglobin at 26.6% of the total soluble protein in the legume19; this can be easily stored at ambient temperatures and extracted later, whereas the level of protein expressed in a leafy crop like lettuce or tobacco may be considerably lower, but may not require extensive purification, depending on its future use. Existing agricultural infrastructure can be used whether the plants are produced in the greenhouse or in open field, and both farming practices can support local rural economies in a fashion that is more environmentally sustainable than livestock agriculture10.A comparison between plant molecular farming and precision fermentation indicates that on average, plant molecular farming requires a much lower initial investment, Capex and scaleup costs than precision fermentation. Precision fermentation, on the other hand, has lower land use requirements but also relies on sugar and other carbon sources, as well as continuous power to run the bioreactors13. These limitations make it more challenging to scale up to global demand, due to the inhibitory costs of bioreactors and in fact sufficient access to global steel to produce them20. While transgenic plants in the open field remain subject to GMO concerns (although protein purified from such sources is not considered to be a GMO), plants do not harbor mammalian pathogens and thus contain lower safety concerns than some microbial expression systems.Artificial intelligence (AI) and machine learning (ML) are now accelerating breakthroughs in plant molecular farming by enabling high-throughput strain optimization, metabolic pathway prediction, and the identification of gene-editing targets21,22. AI-driven algorithms are increasingly used to analyze large-scale omics datasets, predict optimal gene regulatory networks, and guide the design of synthetic constructs for enhanced metabolite production23. For instance, deep learning frameworks can assist in optimizing codon usage, protein folding stability, and promoter strength for cell factory development in plants or plant cells. When combined with CRISPR-based genome editing, these tools can significantly reduce the trial-and-error cycle in engineering high-yielding production strains, paving the way for scalable and cost-effective plant-based biofactories. Integrating AI into strain design thus not only enhances precision and efficiency but also supports predictive modeling for sustainable and economically viable molecular farming systems24.Plant cell-based productsCellular agriculture, a rising field focused on producing a plant-based product directly from a single cell rather than using whole organisms in their natural habitat, offers a transformative approach for the sustainable production of ingredients used in food, cosmetics, and nutraceuticals11. Within this framework, plant cell culture serves as a powerful platform for generating high-value bioactive compounds, flavors, pigments, and even staple ingredients through controlled, in vitro methods. Techniques such as micropropagation, adventitious shoot or root formation, and somatic embryogenesis are widely applied for the regeneration of whole plants and the production of targeted compounds from cultured cells25. The commercialization of these processes using bioreactor systems helps overcome major limitations of conventional methods, which are often labor-intensive and difficult to scale. Bioreactors enable precise control of physical and chemical conditions, improve nutrient distribution, reduce physiological disorders such as hyperhydricity, and support automation, making large-scale production more efficient and economically viable26.Thus, plant-based cellular agriculture not only reduces reliance on land, water, and traditional farming practices, but also supports global efforts toward a circular and sustainable bioeconomy, where biologically derived, renewable resources drive industrial innovation, environmental sustainability, and inclusive economic growth27.Plant tissue culture involves the sterile cultivation of plant parts under controlled conditions, first conceptualized by Gottlieb Haberlandt in 1902, and based on his pioneering work with single-cell cultures28. Initially developed at the beginning of the 20th Century, plant tissue culture has come a long way since then, and includes technologies that make use of root cultures, embryonic cultures, and many others29. Plant cell culture can assist in the production of a plethora of secondary metabolites, and their yields can be vastly improved using genome editing technologies for an increasing number of plant species30. Resembling a cross between cell-based meat and precision fermentation in terms of technology, plant cell culture will facilitate the production of ingredients which would reduce supply chain disruptions. Today, plant cell culture can be produced in bioreactors as great as 100,000 L31.The number of food products that can be produced in plant cell culture has exploded and will continue to expand as concerns about supply chain disruptions grow. For example, cocoa production in cell culture is now being explored as a viable option by several different cellular agriculture companies. Current cocoa production is restricted to tropical regions and is under pressure in terms of loss of land, human rights issues, pest pressures, and is not particularly environmentally friendly32. While these issues, when combined with predictive models of climate change, will undoubtedly reduce our future global cocoa supplies, the demand for cocoa is increasing at a rate that cannot be met using traditional manufacturing processes.Plant cell culture technology is emerging as a transformative platform for the sustainable production of high-value food ingredients. Cultivation of specific plant tissues or cells in a controlled system bypasses traditional agricultural constraints such as seasonal variation, climate vulnerability, and ethical concerns related to labor practices.A notable example is California Cultured (cacultured.com), a U.S.-based biotechnology company that is producing cocoa from cell cultures. Cocoa bean cell cultivation, rapid cell growth and maturation are all possible as well as scalable. This method also minimizes the use of water and labor. It avoids environmental and social issues commonly associated with cocoa farming in West Africa, where most global cocoa is sourced.Due to increasing cocoa demand and the vulnerability of the supply chain, cell culture-based cocoa offers a scalable and ethical alternative, providing substantial reductions in land use, water consumption, and labor requirements compared to conventional cultivation. To truly understand whether plant-based or cell-culture cocoa is more sustainable, the industry needs to apply life-cycle assessment (LCA) more widely. Future LCA studies on chocolate should clearly define their system boundaries, select functional units that are relevant to the purpose, and, where possible, combine both established and newer assessment methods. Adding steps such as uncertainty and sensitivity analysis can help ensure that the results are not only accurate but also reliable for guiding decisions33.Beyond cocoa, similar cellular agriculture technologies are also being applied to coffee production. Arabica coffee is the most widely consumed variety, and is threatened by climate-induced stress and fungal pathogens34. Pluri Biotech (pluri-biotech.com), an Israeli company, is developing coffee from plant cell cultures. Using bioreactors designed to support structured cell growth, the company cultivates coffee cells capable of synthesizing key bioactive compounds such as caffeine. The resulting biomass is harvested, dried, and roasted, yielding a product that visually and sensorial resembles conventional ground coffee.In Europe, the French startup Stem (s-tem.fr) is also working with coffee cell cultures. The cultured coffee powder with natural flavor extracts derived from coffee processing byproducts creates a final product that maintains the sensory characteristics of traditionally harvested beans35.Like cocoa and coffee, cellular agriculture is now an attractive alternative for the production of other bioactive and commercially valuable compounds, including vanillin, saffron, natural colorants, flavor compounds, and dietary supplements30. Growing consumer demand for traceable, sustainable and ethically produced food sources worldwide has fueled the development of plant cell-cultured products. Plant cell culture offers a promising platform for localized, scalable, and clean-label production of essential ingredients for food, cosmetics, and nutraceuticals, addressing both environmental challenges and evolving consumer expectations. Recent advances in plant cell culture and molecular farming are driving a growing number of startups to translate the science into commercial progress. These companies illustrate the technology’s potential through measurable funding rounds, strategic partnerships, and scale-up milestones (Table 1).Table 1 Key startups in plant cell culture and molecular farming with funding and progress metricsFull size tablePlant cell culture offers reduced land use and zero exposure to pests compared to open-field agriculture; however, it requires substantial energy, high-purity water, and refined media components, including sucrose and hormones, enabling the development of heterotrophic cultures. Life-cycle assessments indicate that although emissions per biomass unit may be lower, energy consumption remains a key barrier to economic scalability without renewable energy and media recycling15,36. Techno-economic analyses further emphasize electricity and sugar sourcing as critical factors that need optimization for commercial viability37.Regulatory and ethical considerations in molecular farmingRegulatory frameworks remain a critical consideration for the deployment of products derived from plant biotechnology. While open-field genetically modified (GM) crops typically undergo approval through distinct regulatory pathways, such as the Novel Food Regulation of European Union (EU 2015/2283) and the U.S. FDA approved Generally Recognized as Safe (GRAS) process, plant cell culture–derived products from controlled environments may follow different routes with unique timelines, transparency requirements, and public consultations38. Moreover, societal concerns regarding “laboratory-grown” or “genetically modified” ingredients could impact consumer acceptance and market adoption, highlighting the importance of proactive engagement and clear communication strategies to address public perception and ethical considerations39. Specifically, the molecular farming of animal proteins in plants raises additional public health, stewardship, religious, and ethical questions, underscoring the need for collaborative dialog among scientists, regulators, industry, and religious leaders to ensure responsible development and societal acceptance40.ConclusionsThe rise of cellular agriculture and plant molecular farming has the promise to transform global food systems by producing high-quality alternative proteins and novel ingredients with reduced land and water demands. The success of this growth is hindered by the cost, scalability, consumer acceptance, technical, regulatory, and societal hurdles. Life-cycle assessments and policy frameworks can facilitate the adoption of these technologies, which can complement alternative protein, fermentation, and conventional agriculture to form a resilient and diversified landscape of plant-based products. Strategic innovation, integrating advanced breeding, AI-driven optimization, genome editing, or other breakthrough modern technologies, helps scientists select better cell lines, tweak metabolic processes, and automate production steps, along with supportive policy, to accelerate their path to scale. Combining these advances as part of sustainable food production will ensure they complement, rather than compete with, other alternative protein pillars, positioning them to play a decisive role in meeting the nutritional and environmental challenges of the coming decades for both people and the planet.

    Data availability

    No datasets were generated or analysed during the current study.
    ReferencesFalcon, W. P., Naylor, R. L. & Shankar, N. D. Rethinking global food demand for 2050. Popul. Dev. Rev. 48, 921–957 (2022).Article 

    Google Scholar 
    Willett, W. et al. Food in the anthropocene: the EAT–Lancet Commission on healthy diets from sustainable food systems. Lancet 393, 447–492 (2019).Article 
    PubMed 

    Google Scholar 
    Béné, C. et al. When food systems meet sustainability—current narratives and implications for actions. World Dev. 113, 116–130 (2018).Article 

    Google Scholar 
    Hodgson, A., Alper, J. & Maxon, M. E. The U.S. bioeconomy: Charting a course for a resilient and competitive future. Ind. Biotechnol. 18, 115–136 (2022).Article 

    Google Scholar 
    Springmann, M., Godfray, H. C., Rayner, M. & Scarborough, P. Analysis and valuation of the health and climate change cobenefits of dietary change. Proc. Natl. Acad. Sci. USA 113, 4146–4151, https://doi.org/10.1073/pnas.1523119113 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kemp, L. et al. Point of view: Bioengineering horizon scan 2020. eLife 9, e54489 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Swanson, Z., Welsh, C. & Majkut, J. Mitigating risk and capturing opportunity: The future of alternative proteins. Center for Strategic & International Studies. Sponsored by The Good Food Institute (2023).Marsian, J. et al. Plant-made nervous necrosis virus-like particles protect fish against disease. Front. Plant Sci. 10, 880, https://doi.org/10.3389/fpls.2019.00880 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sim, S. Y. J., SRV, A., Chiang, J. H. & Henry, C. J. Plant proteins for future foods: a roadmap. Foods 10, 1967, https://doi.org/10.3390/foods10081967 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bresnahan, K. A. et al. Closed-loop systems for plants expressing animal proteins: a modernized framework to safeguard the future of agricultural innovation. Front. Plant Sci. 16, 1426290. https://doi.org/10.3389/fpls.2025.1426290 (2025).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rischer, H., Szilvay, G. R. & Oksman-Caldentey, K.-M. Cellular agriculture — Industrial biotechnology for food and materials. Curr. Opin. Biotechnol. 61, 128–134, https://doi.org/10.1016/j.copbio.2019.12.003 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Shanmugaraj, B., Bulaon, C. J. I. & Phoolcharoen, W. Plant molecular farming: a viable platform for recombinant biopharmaceutical production. Plants 9, 842, https://doi.org/10.3390/plants9070842 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    The Good Food Institute. The state of alternative protein series (2025). https://gfi.org/state-of-alternative-protein/.Webster, D. E. & Thomas, M. C. Post-translational modification of plant-made foreign proteins; glycosylation and beyond. Biotechnol. Adv. 30, 410–418 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Buyel, J. F. Plant molecular farming—integration and exploitation of side streams to achieve sustainable biomanufacturing. Front. Plant Sci. 9, 1893 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Benvenuto, E. et al. Plant molecular farming in the wake of the closure of Medicago Inc. Nat. Biotechnol. 41, 893–894, https://doi.org/10.1038/s41587-023-01812-w (2023).Article 
    CAS 
    PubMed 

    Google Scholar 
    Nosaki, S., Hoshikawa, K., Ezura, H. & Miura, K. Transient protein expression systems in plants and their applications. Plant Biotechnol. (Tokyo) 38, 297–304, https://doi.org/10.5511/plantbiotechnology.21.0610a (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Torti, S. et al. Transient reprogramming of crop plants for agronomic performance. Nat. Plants 7, 159–171, https://doi.org/10.1038/s41477-021-00851-y (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    LePage, M. Soya beans made more meat-like by adding genes for pig proteins. New Scientist https://www.newscientist.com/article/2345678-soya-beans-made-more-meat-like-by-adding-genes-for-pig-proteins/ (2023).Tubb, C., & Seba, T. Rethinking Food and Agriculture 2020-2030: A Rethinkx Sector Disruption Report https://www.rethinkx.com/food-and-agriculture (2019).Gupta, D. K., Pagani, A., Zamboni, P. & Singh, A. K. AI-powered revolution in plant sciences: advancements, applications, and challenges for sustainable agriculture and food security. Exploratory Foods Foodomics 2, 443–459 (2024).Article 

    Google Scholar 
    Jafar, A., Bibi, N., Naqvi, R. A., Sadeghi-Niaraki, A. & Jeong, D. Revolutionizing agriculture with artificial intelligence: plant disease detection methods, applications, and their limitations. Front. Plant Sci. 15, 1356260. https://doi.org/10.3389/fpls.2024.1356260 (2024).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dublino, R., & Ercolano, M. Artificial intelligence redefines agricultural genetics by unlocking the enigma of genomic complexity. Crop J. https://doi.org/10.1016/j.cj.2025.05.008 (2025).Li, Z. et al. From code to life: the AI-driven revolution in genome editing. Adv. Sci. e17029 https://doi.org/10.1002/advs.202417029 (2025).Krasteva, G., Georgiev, V. & Pavlov, A. Recent applications of plant cell culture technology in cosmetics and foods. Eng. Life Sci. 21, 68–76 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Polivanova, O. B. & Bedarev, V. A. Hyperhydricity in plant tissue culture. Plants 11, 3313, https://doi.org/10.3390/plants11233313 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Engineering Biology Research Consortium (EBRC). Moonshots for the 21st-century bioeconomy: A policy paper. Compiled and edited by Emily R. Aurand (2022).Thorpe, T. A. History of plant tissue culture. Mol. Biotechnol. 37, 169–180, https://doi.org/10.1007/s12033-007-0031-3 (2007).Article 
    CAS 
    PubMed 

    Google Scholar 
    Ramírez-Mosqueda, M. A. Overview of somatic embryogenesis. In Methods in Molecular Biology (Vol. 2527, pp. 1–8). https://doi.org/10.1007/978-1-0716-2485-2_1 (2022).Wu, T., Kerbler, S. M., Fernie, A. R. & Zhang, Y. Plant cell cultures as heterologous bio-factories for secondary metabolite production. Plant Commun. 2, 100235 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Titova, M., Popova, E. & Nosov, A. Bioreactor systems for plant cell cultivation at the Institute of Plant Physiology of the Russian Academy of Sciences: 50 years of technology evolution from laboratory to industrial implications. Plants 13, 430, https://doi.org/10.3390/plants13030430 (2024).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chen, E. Bittersweet: The harsh realities of chocolate production in West Africa. Harvard International Review (2025).Wang, S. & Dong, Y. Applications of life cycle assessment in the chocolate industry: a state-of-the-art analysis based on systematic review. Foods 13, 915 (2024).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wright, D. R. et al. Sustainable coffee: a review of the diverse initiatives and governance dimensions of global coffee supply chains. Ambio 53, 984–1001 (2024).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Turrell, C. Cell-based coffee future-proofs world’s favorite brew. Nat. Biotechnol. 42, 350 (2024).Article 
    CAS 
    PubMed 

    Google Scholar 
    Puzanskiy, R. K., Romanyuk, D. A., Kirpichnikova, A. A., Yemelyanov, V. V. & Shishova, M. F. Plant heterotrophic cultures: No food, no growth. Plants 13, 277, https://doi.org/10.3390/plants13020277 (2024).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    McNulty, M. J. et al. Techno-economic analysis of a plant-based platform for manufacturing antimicrobial proteins for food safety. Biotechnol. Prog. 36, e2896. https://doi.org/10.1002/btpr.2896 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Lucht, J. M. Public acceptance of plant biotechnology and GM crops. Viruses 7, 4254–4281, https://doi.org/10.3390/v7082819 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Frewer, L. J., Scholderer, J. & Bredahl, L. Communicating about the risks and benefits of genetically modified foods: the mediating role of trust. Risk Anal. 23, 1117–1133 (2003).Article 
    PubMed 

    Google Scholar 
    Bobo, J. Molecular farming navigates a complex regulatory landscape. Front. Plant Sci. 15, 1411943, https://doi.org/10.3389/fpls.2024.1411943 (2024).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Download referencesAuthor informationAuthors and AffiliationsDepartment of Microbiology, Cornell University, Ithaca, NY, USAKathleen HefferonSchool of Integrative Plant Sciences, Cornell University, Ithaca, NY, USAAdam GannonDepartment of Biotechnology and Genetic Engineering, Jahangirnagar University, Dhaka, BangladeshAbdullah Mohammad ShohaelAuthorsKathleen HefferonView author publicationsSearch author on:PubMed Google ScholarAdam GannonView author publicationsSearch author on:PubMed Google ScholarAbdullah Mohammad ShohaelView author publicationsSearch author on:PubMed Google ScholarContributionsK.H. and A.S. wrote the main manuscript. A.G. revised and updated. All authors reviewed the manuscript.Corresponding authorCorrespondence to
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    Stochastic growth marks in Crocodylus niloticus

    Abstract

    Skeletochronology combined with growth curve reconstruction is routinely used to assess the age and growth dynamics of extinct and extant vertebrates. Here we performed in vivo labelling studies of the bone histology of four 2 years-old Crocodylus niloticus individuals. We found that all the crocodiles have more growth marks in their compacta than expected for their age, i.e., they deposited stochastic growth marks in their bones. Using the fluorochrome markers we determined that these stochastic growth marks were deposited during their favourable season of growth. The variable preservation of growth marks in the crocodile bones highlights developmental plasticity in their growth, which can be extrapolated to extinct archosaurs, and other reptiles. We caution the use of growth marks in fossil bones as a reliable estimator of age and discuss the far-reaching implications this has for growth curve reconstruction and life history assessments of extinct vertebrates, such as nonavian dinosaurs.

    Data availability

    High resolution images will be uploaded onto Morphobank. All thin sections will be deposited in the Vertebrate Comparative Collections of Iziko Museums of Cape Town.
    ReferencesCastanet, J., Newman, D. & Girons, H. S. Skeletochronological data on the growth, age, and population structure of the tuatara, Sphenodon punctatus, on Stephens and lady Alice Islands, New Zealand. Herpetologica 44, 25–37 (1988).
    Google Scholar 
    Castanet, J., Vieillot, H. F., Meunier, F. J. & De Ricqlès, A. Bone and individual aging. Bone 7, 245–283 (1993).
    Google Scholar 
    Chinsamy-Turan, A. The Microstructure of Dinosaur Bones: Deciphering Biology Through Fine Scale Techniques (John Hopkins University, 2005).Buffrenil, V. Q. & Castanet, A. J. in Vertebrate Skeletal Histology and Paleohistology. (eds de Buffrenil, V., de Ricqles, A. J., Zylberberg, L., Padian, K.) Ch. 31, 626–644 (CRC Press, 2021).Castanet, J., Francillon-Vieillot, H., Meunier, F., De Ricqles, A. & Hall, B. Bone and individual aging. Bone 7, 245–283 (1993).
    Google Scholar 
    Kohler, M., Marin-Moratalla, N., Jordana, X. & Aanes, R. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358–361 (2012). https://doi.org/10.1038/nature11264
    Google Scholar 
    Hutton, J. M. Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia 2, 332–341 (1986).
    Google Scholar 
    Roberts, E., Matlock, C., Joanen, T., McNease, L. & Bowen, M. Bone morphometrics and Tetracycline marking patterns in young growing American alligators (Alligator mississippiensis). J. Wildl. Dis. 24, 67–70 (1988).
    Google Scholar 
    Snover, M. L. & Hohn, A. A. Validation and interpretation of annual skeletal marks in loggerhead (Caretta caretta) and kemp’s ridley (Lepidochelys kempii) sea turtles. Fish. Bull. 102 (4), 682–693 (2004).
    Google Scholar 
    Cubo, J. et al. Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evol. Dev. 10, 217–227 (2008).
    Google Scholar 
    Ricqlès, A., Meunier, F. J., Castanet, J. & Francillon-Viellot, H. in Bone Matrix and Bone Specific Products, Vol. 31–78 (ed Hall B. K.) (CRC Press, Inc., 1991).Chinsamy, A. Palaeoecological deductions from osteohistology. Biol. Lett. 19, 20230245 (2023).
    Google Scholar 
    Caetano, M. & Castanet, J. Variability and microevolutionary patterns in Triturus marmoratus from Portugal: Age, size, longevity and individual growth. Amphibia-reptilia 14, 117–129 (1993).
    Google Scholar 
    Erismis, U. C. & Chinsamy, A. Ontogenetic changes in the epiphyseal cartilage of Rana (Pelophylax) Caralitana (Anura: Ranidae). Anat. Rec (Hoboken). 293, 1825–1837 (2010). https://doi.org/10.1002/ar.21241
    Google Scholar 
    Mattox, N. T. Annular rings in the long bones of turtles and their correlation with size. Trans. Ill. State Acad. Sci. 28, 255–256 (1936).
    Google Scholar 
    Avens, L., Taylor, J. C., Goshe, L. R., Jones, T. T. & Hastings, M. Use of skeletochronological analysis to estimate the age of leatherback sea turtles Dermochelys coriacea in the Western North Atlantic. Endanger. Species Res. 8, 165–177 (2009). https://doi.org/10.3354/esr00202
    Google Scholar 
    Pereyra, M. E. et al. Growth dynamics and body size evolution of South American long-necked chelid turtles: A bone histology approach. Acta Palaeontol. Pol. 65, 535–545 (2020).
    Google Scholar 
    Pereyra, M. E. Comparative postcranial osteohistology and bone histovariability of aquatic and terrestrial turtles: The case of the South American Phrynops hilarii, Hydromedusa tectifera (Pleurodira, Chelidae), and Chelonoidis Chilensis (Cryptodira, Testudinidae). Anat. Rec. 306, 1304–1322 (2023).
    Google Scholar 
    Bhat, M. S., Chinsamy, A. & Parkington, J. Long bone histology of Chersina angulata: Interelement variation and life history data. J. Morphol. 280, 1881–1899 (2019).
    Google Scholar 
    Bhat, M. S., Chinsamy, A. & Parkington, J. Bone histology of neogene angulate tortoises (Testudines: Testudinidae) from South africa: Palaeobiological and skeletochronological implications. R. Soc. Open. Sci. 10, 230064 (2023).
    Google Scholar 
    Bhat, M. S. & Cullen, T. M. Growth and life history of freshwater chelydrid turtles (Testudines: Cryptodira): A bone histological approach. J. Anat., 247(3-4), 518–541 .
    Google Scholar 
    Castanet, J. & Naulleau, G. Données expérimentales sur la Valeur des Marques squelettiques comme indicateur de l ‘âge Chez Vipera Aspis (L.)(Ophidia, Viperidae). Zoolog. Scr. 3, 201–208 (1974).
    Google Scholar 
    Castanet, J. & Baez, M. Data on age and longevity in Gallotia Galloti (Sauria, Lacertidae) assessed by skeletochronology. Herpetol. J. 1, 218–222 (1988).
    Google Scholar 
    Castanet, J. & Baez, M. Adaptation and evolution in Gallotia Lizard from the Canary islands: Age, growth, maturity and longevity. Amphibia-Reptilia 12, 81–102 (1991).
    Google Scholar 
    Chinsamy, A., Hanrahan, S. A., Neto, M. & Seely, M. Skeletochronological assessment of age in Angolosaurus skoogi, a cordylid Lizard living in an aseasonal environment. J. Herpetol. 29, 457–460 (1995).
    Google Scholar 
    Chinsamy, A. The Osteohistology of Femoral Growth within a Clade: A Comparison of the Crocodile, Crocodylus niloticus, the Dinosaurs, Massospondylus and Syntarsus, and the Birds, Struthio and Sagittarius, (Witwatersrand, 1991).Woodward, H. N., Horner, J. R. & Farlow, J. O. Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ 2, e422 (2014).
    Google Scholar 
    Pereyra, M. E., Bona, P., Siroski, P. & Chinsamy, A. Ontogenetic and interelemental study of appendicular bones of Caiman latirostris Daudin, 1802 sheds light on osteohistological variability in crocodylians. J. Morphol. 285, e21687 (2024).
    Google Scholar 
    Pereyra, M. E., Bona, P., Siroski, P. & Chinsamy, A. Analyzing the life history of caimans: the growth dynamics of Caiman latirostris from an osteohistological approach. J. Morphol. 286, e70010 (2025).
    Google Scholar 
    Audije-Gil, J., Barroso‐Barcenilla, F. & Cambra‐Moo, O. Mapping histovariability and growth patterns of Crocodylus niloticus bred in captivity and their Paleobiological implications. Ruling Reptiles: Crocodylian Biology Archosaur Paleobiology, 284–299 (2023).Castanet, J. et al. Lines of arrested growth in bone and age Estimation in a small primate: Microcebus murinus. J. Zool. 263, 31–39 (2004). https://doi.org/10.1017/s0952836904004844
    Google Scholar 
    Morris, P. A. A method for determinng absolute age in the Hedgehog. J. Zool. 20, 277–281 (1970).
    Google Scholar 
    Bourdon, E. et al. Bone growth marks reveal protracted growth in New Zealand Kiwi (Aves, Apterygidae). Biol. Lett. 5, 639–642. (2009). https://doi.org/10.1098/rsbl.2009.0310
    Google Scholar 
    Chinsamy, A., Angst, D., Canoville, A. & Göhlich, U. B. Bone histology yields insights into the biology of the extinct elephant birds (Aepyornithidae) from Madagascar. Biol. J. Linn. Soc. 130, 268–295 (2020).
    Google Scholar 
    Chinsamy, A., Handley, W. D. & Worthy, T. H. Osteohistology of Dromornis stirtoni (Aves: Dromornithidae) and the biological implications of the bone histology of the Australian Mihirung birds. Anat. Rec. 306 (7), 1842–1863 (2022).
    Google Scholar 
    Weiss, B. M., Dollman, K. N., Choiniere, J. N., Browning, C. & Botha, J. The osteohistology of Orthosuchus stormbergi using synchrotron radiation microcomputed tomography. J. Anat. 247 (3-4), 587–607 (2024).
    Google Scholar 
    Fernández Dumont, M. L., Pereyra, M. E., Bona, P. & Apesteguía, S. New data on the palaeosteohistology and growth dynamic of the notosuchian Araripesuchus Price, 1959. Lethaia 54, 578–590 (2021).
    Google Scholar 
    Hoffman, D. et al. Evolution of growth strategy in alligators and Caimans informed by osteohistology of the late eocene early-diverging alligatoroid crocodylian Diplocynodon hantoniensis. J. Anat. 247, 165 (2025).
    Google Scholar 
    Chinsamy, A. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Mod. Geol. 18, 319–329 (1993).
    Google Scholar 
    Varricchio, D. J. Bone microstructure of the upper cretaceous theropod dinosaur Troodon formosus. J. Vertebr. Paleontol. 13, 99–104 (1993).
    Google Scholar 
    Horner, J. R., De Ricqlès, A. & Padian, K. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: Growth dynamics and physiology based on an ontogenetic series of skeletal elements. J. Vertebr. Paleontol. 20 (1), 115–129 (2000).
    Google Scholar 
    Erickson, G. M. Assessing dinosaur growth patterns: A microscopic revolution. Trends Ecol. Evol. 20, 677–684. (2005). https://doi.org/10.1016/j.tree.2005.08.012
    Google Scholar 
    Sander, M. Long bone histology of the Tendaguru sauropods: Implications for growth and biology. Paleobiology 26 (3), 466–488 (2000).
    Google Scholar 
    Woodward, H. N., Fowler, E. A. F., Farlow, J. O. & Horner, J. R. Maiasaura, a model organism for extinct vertebrate population biology: A large sample statistical assessment of growth dynamics and survivorship. Paleobiology 41, 503–527 (2015).
    Google Scholar 
    Bybee, P. J., Lee, A. H. & Lamm, E. T. Sizing the jurassic theropod dinosaur Allosaurus: Assessing growth strategy and evolution of ontogenetic scaling of limbs. J. Morphol. 267, 347–359. (2006). https://doi.org/10.1002/jmor.10406
    Google Scholar 
    Cullen, T. M. et al. Growth variability, dimensional scaling, and the interpretation of osteohistological growth data. Biol. Lett. 17, 20210383 (2021).
    Google Scholar 
    Cullen, T. M., Evans, D. C., Ryan, M. J., Currie, P. J. & Kobayashi, Y. Osteohistological variation in growth marks and osteocyte lacunar density in a theropod dinosaur (Coelurosauria: Ornithomimidae). BMC Evol. Biol. 14, 231 (2014).
    Google Scholar 
    Cerda, I. A., Pol, D., Otero, A. & Chinsamy, A. Palaeobiology of the early sauropodomorph Mussaurus patagonicus inferred from its long bone histology. Palaeontology 65, e12614 (2022).
    Google Scholar 
    SchuchtP.J., Klein, N. & Lambertz, M. What’s my age again? On the ambiguity of histology-based skeletochronology. Proc. R. Soc. B. 288, 20211166 (2021).
    Google Scholar 
    Bruce, R. C., Castanet, J. & Francillon-Vieillot, H. Skeletochronological analysis of variation in age structure, body size, and life history in three species of desmognathine salamanders. Herpetologica 58, 181–193 (2002).
    Google Scholar 
    Nacarino-Meneses, C. & Köhler, M. Limb bone histology records birth in mammals. PloS One. 13, e0198511 (2018).
    Google Scholar 
    Woolley, M. R., Chinsamy, A., Govender, R. & Bester, M. N. Microanatomy and histology of bone pathologies of extant and extinct phocid seals. Hist. Biol. 33 (8), 1231–1246 (2019).
    Google Scholar 
    Calderón, T., Arnold, W., Stalder, G., Painer, J. & Köhler, M. Labelling experiments in red deer provide a general model for early bone growth dynamics in ruminants. Sci. Rep. 11, 14074 (2021).
    Google Scholar 
    Klevezal, G. A. & Kleinenberg, S. E. Age Determination of Mammals from Annual Layers in Teeth and Bones. (Translated from Russian by Salkind J.) (Israel Program for Scientific Translations Press, Jerusalem, 1969).Köhler, M. et al. Insular giant leporid matured later than predicted by scaling. Iscience 26, 107654 (2023).
    Google Scholar 
    D’Emic, M. D. et al. Developmental strategies underlying gigantism and miniaturization in non-avialan theropod dinosaurs. Science 379, 811–814 (2023).
    Google Scholar 
    Chinsamy, A. R. Preparation of fossil bone for histological examination. Palaeontol. Afr. 29, 39–44 (1992).
    Google Scholar 
    Castanet, J. & Baez, M. Adaptation and evolution in Gallotia lizards from the Canary islands: Age, growth, maturity and longevity. Amphibia-Reptilia 12, 81–102 (1991).
    Google Scholar 
    Larriera, A. & Imhof, A. Proyecto yacaré. Manejo de Fauna Silvestre en Argentina. Ministerio de Salud y Ambiente de la Nación, Buenos Aires, 51–64 (2006).Viotto, E. V., Simoncini, M. S., Verdade, L. M., Navarro, J. L. & Piña, C. Winter survivorship of hatchling broad-snouted Caimans (Caiman latirostris) in Argentina. Ethnobiol. Conserv. 11 (2022).Petter-Rousseaux, A. Recherches Sur La croissance et Le cycle d’activité testiculaire de natrix natrix helvetica (Lacépède). Revue d’Écologie (La Terre Et La. Vie). 7, 175–223 (1953).
    Google Scholar 
    Saint Girons, H. Les critères d’âge Chez les reptiles et leurs applications à l’étude de La structure des populations sauvages. Revue d’Écologie, 342–358 (1965).Heck, C. T. & Woodward, H. N. Intraskeletal bone growth patterns in the North Island brown Kiwi (Apteryx mantelli): Growth mark discrepancy and implications for extinct taxa. J. Anat. 239, 1075–1095 (2021).
    Google Scholar 
    Collins, E. P. & Rodda, G. H. Bone layers associated with ecdysis in laboratory-reared Boiga irregularis (Colubridae). J. Herpetol. 28, 378–381 (1994).
    Google Scholar 
    Castanet, J. Les méthodes d’estimation de l’age Chez les chéloniens. Mesogee 48, 21–28 (1988).
    Google Scholar 
    de Buffrénil, V. & Castanet, J. Age Estimation by skeletochronology in the Nile monitor (Varanus niloticus), a highly exploited species. J. Herpetol. 34, 414–424 (2000).
    Google Scholar 
    Castanet, J., Rogers, K. C., Cubo, J. & Boisard, J. J. Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs. C. R. Acad. Sci. 323, 543–550 (2000).
    Google Scholar 
    Starck, J. M. & Chinsamy, A. Bone microsructure and developmental plasticity in birds and other dinosaurs. J. Morphol. 254, 232–246 (2002).
    Google Scholar 
    Montes, L., Castanet, J. & Cubo, J. Relationship between bone growth rate and bone tissue organization in amniotes: First test of Amprino’s rule in a phylogenetic context. Anim. Biol. 60, 25–41 (2010).
    Google Scholar 
    Cubo, J. & Laurin, M. Perspectives on vertebrate evolution: Topics and problems. C.R. Palevol. 10, 285–292. (2011). https://doi.org/10.1016/j.crpv.2011.05.007
    Google Scholar 
    Montoya-Sanhueza, G., Bennett, N. C., Oosthuizen, M. K., Dengler‐Crish, C. M. & Chinsamy, A. Bone remodeling in the longest living rodent, the naked mole‐rat: Interelement variation and the effects of reproduction. J. Anat. 239 (1), 81–100 (2021).
    Google Scholar 
    Schlief, S. C., Richman, J. M. & Brink, K. S. Bone labeling experiments and intraskeletal growth patterns in captive Leopard geckos (Eublepharis macularius). J. Anat. 247 (3-4), 542–555 (2024).
    Google Scholar 
    Maloney, S. K. et al. Minimum daily core body temperature in Western grey kangaroos decreases as summer advances: A seasonal pattern, or a direct response to water, heat or energy supply? J. Exp. Biol. 214, 1813–1820 (2011).
    Google Scholar 
    Jacobsen, T. & Kushlan, J. A. Growth dynamics in the American alligator (Alligator mississippiensis). J. Zool. Lond. 219, 309–328 (1989).
    Google Scholar 
    Wilkinson, P. M. & Rhodes, W. E. Growth rates of American alligators in coastal South Carolina. J. Wildl. Manag. 61, 397–402 (1997).
    Google Scholar 
    Brito, J. C., Martinez-Freiria, F., Sierra, P., Sillero, N. & Tarroso, P. Crocodiles in the Sahara desert: An update of distribution, habitats and population status for conservation planning in Mauritania. PLoS One. 6, e14734 (2011).
    Google Scholar 
    Caetano, M. H. Use and results of skeletochronology in some urodeles (Triturus marmoratus, Latreille 1800 and Triturus boscai, lataste 1879. Ann. des. Sci. Nat. Zool. 11, 197–199 (1990).
    Google Scholar 
    Webb, G., Manolis, S. & Buckworth, R. Crocodylus Johnstoni in the McKinlay river area N. T, III.* Growth, movement and the population age structure. Wildl. Res. 10, 383–401 (1983).
    Google Scholar 
    Sander, P. M. & Klein, N. Developmental plasticity in the life history of a prosauropod dinosaur. Science 310, 1800–1802 (2005).
    Google Scholar 
    Chapelle, K. E., Botha, J. & Choiniere, J. N. Extreme growth plasticity in the early branching sauropodomorph Massospondylus carinatus. Biol. Lett. 17, 20200843 (2021).
    Google Scholar 
    Chinsamy, A., Marugán-Lobón, J., Serrano, F. J. & Chiappe, L. Osteohistology and Life History of the Basal Pygostylian, Confuciusornis sanctus. Anat. Record 303(4), 949–962 (2019).
    Google Scholar 
    Spiekman, S. N., Butler, R. J. & Maidment, S. C. The postcranial anatomy and osteohistology of Terrestrisuchus gracilis (Archosauria, Crocodylomorpha) from the late triassic of Wales. Papers Palaeontol. 10, e1577 (2024).
    Google Scholar 
    Pereyra, E. M., Bona, P., Siroski, P. & Chinsamy, A. Analyzing the life history of caimans: The growth dynamics of Caiman latirostris from an osteohistological approach. J. Morphol. 286, e70010 (2025).
    Google Scholar 
    Chinsamy, A. in Fifth Symposium on Mesozoic Terrestrial Ecosystems and Biota. (ed Z. Kielan-Jaworoska, Natascha Heitz and Hans Arne Nakrem) 13 (Paleontological Museum).Erickson, G. Growth curve of Psittacosaurus mongoliensis Osborn (Ceratopsia: Psittacosauridae) inferred from long bone histology. Zool. J. Linn. Soc. 130, 551–566 (2000). https://doi.org/10.1111/j.1096-3642.2000.tb02201.x
    Google Scholar 
    Erickson, G. M. et al. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772–775 (2004).
    Google Scholar 
    Woodward, H. N. Maiasaura (Dinosauria: Hadrosauridae) tibia osteohistology reveals Non-annual cortical vascular rings in young of the year. Front. Earth Sci. 7, 50 (2019). https://doi.org/10.3389/feart.2019.00050
    Google Scholar 
    Horner, J. R. & Padian, K. Age and growth dynamics of Tyrannosaurus. Rex. Proc. Biol. Sci. 271, 1875–1880 (2004). https://doi.org/10.1098/rspb.2004.2829
    Google Scholar 
    Cullen, T. M., Simon, D. J., Benner, E. K. & Evans, D. C. Morphology and osteohistology of a large-bodied caenagnathid (Theropoda, Oviraptorosauria) from the hell creek formation (Montana): implications for size‐based classifications and growth reconstruction in theropods. Papers Palaeontol. 7, 751–767 (2021).
    Google Scholar 
    Kolb, C. et al. Growth in fossil and extant deer and implications for body size and life history evolution. BMC Evol. Biol. 15, 19 (2015). https://doi.org/10.1186/s12862-015-0295-3
    Google Scholar 
    Curry Rogers, K., Whitney, M., D’Emic, M. & Bagley, B. Precocity in a tiny titanosaur from the cretaceous of Madagascar. Science 352, 450–453 (2016).
    Google Scholar 
    Horner, J. R., Ricqlès, A. & Padian, K. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25 (3), 295–304 (1999).
    Google Scholar 
    Campbell, D. L., Hewitt, L., Lee, C., Timmerhues, C. A. & Small, A. H. Behaviours of farmed saltwater crocodiles (Crocodylus porosus) housed individually or in groups. Front. Veterinary Sci. 11, 1394198 (2024).
    Google Scholar 
    Morpurgo, B., Gvaryahu, G. & Robinzon, B. Aggressive behaviour in immature captive nile crocodiles, Crocodylus niloticus, in relation to feeding. Physiol. Behav. 53, 1157–1161 (1993).
    Google Scholar 
    Download referencesAcknowledgementsWe are grateful to Le Bonheur Reptiles and Adventures for permitting access to the crocodiles investigated here. Aurore Canoville and Andrea Plos are warmly thanked for assisting with fieldwork. Vidushi Dabee is acknowledged for having prepared some of the thin sections. We thank Viantha Naidoo and Dirk Lang at the Confocal and Light Microscope Imaging Facility of the Faculty of Health Sciences at UCT. Shafi M. Bhat of the Department of Geosciences at Auburn University, Alabama, is acknowledged for having read an earlier draft of this manuscript. Devin Hoffman and two additional anonymous reviewers are thanked for their comments. The University of Cape Town Research Committee (URC) is thanked for the postdoctoral fellowship awarded to the second author.Author informationAuthors and AffiliationsDepartment of Biological Sciences, University of Cape Town, Private Bag, Rhodes Gift, Rondebosch, 7700, South AfricaAnusuya Chinsamy & Maria-Eugenia PereyraAuthorsAnusuya ChinsamyView author publicationsSearch author on:PubMed Google ScholarMaria-Eugenia PereyraView author publicationsSearch author on:PubMed Google ScholarContributionsAC conceived and designed the project and administered the fluorochrome labelling to the crocodiles. M-EP and AC analysed the histological thin sections, and both contributed to the data interpretation and analysis.  M-EP did the confocal and petrographic micrographs and figures for the manuscript. AC wrote the first draft, and M-EP contributed to the write up and made important suggestions. Both authors approved the final version of the manuscript.Corresponding authorCorrespondence to
    Anusuya Chinsamy.Ethics declarations

    Competing interests
    The authors declare no competing interests.

    Additional informationPublisher’s noteSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary InformationBelow is the link to the electronic supplementary material.Supplementary Material 1Supplementary Material 2Rights and permissions
    Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
    Reprints and permissionsAbout this articleCite this articleChinsamy, A., Pereyra, ME. Stochastic growth marks in Crocodylus niloticus.
    Sci Rep (2025). https://doi.org/10.1038/s41598-025-31384-5Download citationReceived: 28 July 2025Accepted: 02 December 2025Published: 18 December 2025DOI: https://doi.org/10.1038/s41598-025-31384-5Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy shareable link to clipboard
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    Author Correction: Sociality predicts orangutan vocal phenotype

    Correction to: Nature Ecology & Evolution https://doi.org/10.1038/s41559-022-01689-z, published online 21 March 2022.After publication of the article, an error was identified in the data entry of the maximum frequency parameter for the Suaq orangutan population. Recalculation of entropy measures and reanalysis of the mixed models revealed that, for maximum frequency, the previously reported effect of sociality is no longer statistically supported (Emergence and self-organization: F = 0.321, P = 0.573; Complexity: F = 0.009, P = 0.927). The original results for duration remain unchanged and continue to show a significant effect of sociality. While the loss of statistical support for one parameter is regrettable, the revised findings are scientifically meaningful. They align with recent findings in chimpanzees1, showing that control over vocal parameters such as frequency and duration may operate independently. This suggests that social influences on vocal phenotypes may target specific acoustic features, and that specific populations may deploy features of vocal novelty in culturally localized ways.The corrected analysis further reaffirms key methodological points raised in our original paper. In entropy-based analyses of behavioural novelty, low-probability events—sometimes mischaracterized as ‘outliers’—are not statistical noise but the core phenomena of interest. Their removal would bias entropy estimates and undermine the capacity to detect innovation. Given the nature of our study—multi-year, multi-site, and focused on a critically endangered species—each data point represents an irreplaceable behavioural observation. Removing such points without clear justification raises ethical concerns, including violation of IUCN data integrity guidelines and FAIR/TRUST data stewardship principles2,3. Our approach illustrates how ethical and methodological rigour must go hand-in-hand when working with vulnerable wild populations.For the calculation of entropy values from continuous acoustic data, equal-width binning at the individual level remains a necessary and appropriate step4. Our binning approach was selected to capture vocal originality at the level of individual phenotypes—what we term “vocal personalities”—in response to social input. Other binning choices, such as a global binning, would be unable to distinguish between individual differences and novelty; benchmarking individuals against each other would be an analysis of group conformity, not of individual originality or vocal personality.The Supplementary Information accompanying this amendment includes the original, uncorrected article for comparison (changes have been made to the Results and discussion, Methods, Table 1 and Fig. 2). Supplementary Data 3–5 have also been corrected and are available alongside the original article.The authors would like to thank Peng-Fei Fan and Zi-Di Wang for intially bringing the issue to their attention.

    ReferencesLameira, A. R., Caneco, B., Kershenbaum, A., Santamaría-Bonfil, G. & Call, J. Generative vocal plasticity in chimpanzees. iScience 112381 (2025).Wilkinson, M. D. et al. The FAIR Guiding Principles for scientific data management and stewardship. Sci. Data 3, 160018 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lin, D. et al. The TRUST Principles for digital repositories. Sci. Data 7, 144 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Santamaría-Bonfil, G., Fernández, N. & Gershenson, C. Measuring the complexity of continuous distributions. Entropy 18, 72 (2016).Article 

    Google Scholar 
    Download referencesAuthor informationAuthors and AffiliationsDepartment of Psychology, University of Warwick, Coventry, UKAdriano R. LameiraSchool of Psychology and Neuroscience, University of St Andrews, St Andrews, UKAdriano R. LameiraInstituto Nacional de Electricidad y Energías Limpias, Gerencia de Tecnologías de la Información, Cuernavaca, MéxicoGuillermo Santamaría-BonfilDepartment of Life Sciences and Systems Biology, University of Torino, Turin, ItalyDeborah Galeone & Marco GambaIndependent researcher, Warwick, UKMadeleine E. HardusDepartment of Anthropology, Boston University, Boston, MA, USACheryl D. KnottBorneo Nature Foundation, Palangka Raya, IndonesiaHelen Morrogh-BernardCollege of Life and Environmental Sciences, University of Exeter, Penryn, UKHelen Morrogh-BernardThe PanEco Foundation—Sumatran Orangutan Conservation Programme, Berg am Irchel, SwitzerlandMatthew G. NowakDepartment of Anthropology, Southern Illinois University, Carbondale, IL, USAMatthew G. NowakYayasan Inisiasi Alam Rehabilitasi Indonesia, International Animal Rescue, Ketapang, IndonesiaGail Campbell-SmithSchool of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UKSerge A. WichFaculty of Science, University of Amsterdam, Amsterdam, NetherlandsSerge A. WichAuthorsAdriano R. LameiraView author publicationsSearch author on:PubMed Google ScholarGuillermo Santamaría-BonfilView author publicationsSearch author on:PubMed Google ScholarDeborah GaleoneView author publicationsSearch author on:PubMed Google ScholarMarco GambaView author publicationsSearch author on:PubMed Google ScholarMadeleine E. HardusView author publicationsSearch author on:PubMed Google ScholarCheryl D. KnottView author publicationsSearch author on:PubMed Google ScholarHelen Morrogh-BernardView author publicationsSearch author on:PubMed Google ScholarMatthew G. NowakView author publicationsSearch author on:PubMed Google ScholarGail Campbell-SmithView author publicationsSearch author on:PubMed Google ScholarSerge A. WichView author publicationsSearch author on:PubMed Google ScholarCorresponding authorCorrespondence to
    Adriano R. Lameira.Supplementary informationOriginal, uncorrected articleRights and permissions
    Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
    Reprints and permissionsAbout this articleCite this articleLameira, A.R., Santamaría-Bonfil, G., Galeone, D. et al. Author Correction: Sociality predicts orangutan vocal phenotype.
    Nat Ecol Evol (2025). https://doi.org/10.1038/s41559-025-02954-7Download citationPublished: 18 December 2025Version of record: 18 December 2025DOI: https://doi.org/10.1038/s41559-025-02954-7Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy shareable link to clipboard
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    De novo assembly of complete circular mitochondrial genomes from 2,695 fungal species

    AbstractFungal mitochondrial genomes are critical for understanding phylogenetics, evolution, and ecology of the Kingdom Fungi, yet they remain underrepresented in public databases. To address this, we developed a workflow to recover mitochondrial genomes from 12,902 fungal short read sequencing data housed in the Sequence Read Archive (SRA) records, assembling complete circular genomes from 2,695 species. This effort expanded fungal mitochondrial genome diversity by nearly 2.3X particularly in understudied phyla such as Mucoromycota (11X increase) and Zoopagomycota (8X increase). The new dataset contains novel yet undescribed mitochondrial genomes at numerous taxonomic levels, including 15 classes, 64 orders, 178 families, and 544 genera. Taxonomic analysis revealed broad ecological representation among the top-assembled species, including human pathogens (e.g., Cryptococcus tetragattii), plant pathogens (e.g., Melampsora larici-populina), edible mushrooms (e.g., Suillus luteus), and industrial fungi. By leveraging the not yet fully exploited SRA sequencing data, this study fills critical gaps in fungal mitochondrial genomics, tripling the currently known mitochondrial genome diversity of the Kingdom Fungi, and provides an extensive resource for phylogenetic and evolutionary research.

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    Code availability

    The assembly workflow was implemented in a python script (assembly_workflow.py) passing SRA run accession as input and outputting the assembly contigs and graphs, which are used by GetOrganelle for mitochondrial genome extraction (Methods). The script uses already published tools and explained in the Methods section. The script is available on GitHub at https://github.com/msabrysarhan/fungal_mtDNA.
    Data availability

    Nucleotide sequence data reported are available in the Third Party Annotation Section of the DDBJ/ENA/GenBank databases under the BioProject PRJNA1367877 and the accession numbers TPA: BK072095-BK074789, and the metadata is available at https://doi.org/10.6084/m9.figshare.28750034.
    ReferencesHawksworth, D. L. & Lücking, R. J. M. s. Fungal diversity revisited: 2.2 to 3.8 million species. 5, https://doi.org/10.1128/microbiolspec. funk-0052-2016 (2017).Paterson, R. R. M., Solaiman, Z. & Santamaria, O. J. S. R. Guest edited collection: fungal evolution and diversity. 13, 21438 (2023).James, T. Y., Stajich, J. E., Hittinger, C. T. & Rokas, A. J. A. R. O. M. Toward a fully resolved fungal tree of life. 74, 291-313 (2020).Chethana, K. T. et al. What are fungal species and how to delineate them? 109, 1-25 (2021).Li, Y. et al. A genome-scale phylogeny of the kingdom Fungi. 31, 1653-1665. e1655 (2021).Kouvelis, V. N., Kortsinoglou, A. M., James, T. Y. J. E. o. F. & Organisms, F.-L. The evolution of mitochondrial genomes in fungi. 65-90 (2023).Kulik, T., Van Diepeningen, A. D. & Hausner, G. J. F. i. M. Vol. 11 628579 (Frontiers Media SA, 2021).Song, N., Geng, Y. & Li, X. J. F. i. M. The mitochondrial genome of the phytopathogenic fungus Bipolaris sorokiniana and the utility of mitochondrial genome to infer phylogeny of Dothideomycetes. 11, 863 (2020).Zhang, S. et al. Dynamic evolution of eukaryotic mitochondrial and nuclear genomes: a case study in the gourmet pine mushroom Tricholoma matsutake. 23, 7214-7230 (2021).Sauters, T. J. & Rokas, A. J. C. B. Patterns and mechanisms of fungal genome plasticity. 35, R527-R544 (2025).Jung, H. et al. Twelve quick steps for genome assembly and annotation in the classroom. 16, e1008325 (2020).Persoons, A. et al. Patterns of genomic variation in the poplar rust fungus Melampsora larici-populina identify pathogenesis-related factors. 5, 450 (2014).Schoch, C. L. et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. 2020, baaa062 (2020).Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890, https://doi.org/10.1093/bioinformatics/bty560 (2018).
    Google Scholar 
    Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome research 27, 824–834 (2017).
    Google Scholar 
    Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21, 241, https://doi.org/10.1186/s13059-020-02154-5 (2020).
    Google Scholar 
    Lang, B. F. et al. Mitochondrial genome annotation with MFannot: a critical analysis of gene identification and gene model prediction. 14, 1222186 (2023).Katoh, K. & Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution 30, 772–780, https://doi.org/10.1093/molbev/mst010 (2013).
    Google Scholar 
    Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. J. B. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. 25, 1972-1973 (2009).Borowiec, M. L. J. P. AMAS: a fast tool for alignment manipulation and computing of summary statistics. 4, e1660 (2016).Price, M. N., Dehal, P. S. & Arkin, A. P. J. P. O. FastTree 2–approximately maximum-likelihood trees for large alignments. 5, e9490 (2010).Sarhan, M. S., Abdalrahem, A., Maixner, F. & Fuchsberger, C. NCBI GenBank https://identifiers.org/ncbi/bioproject:PRJNA1367877 (2025).Sarhan, M. S., Abdalrahem, A., Maixner, F. & Fuchsberger, C. De novo assembly of complete circular mitochondrial genomes from 2,695 fungal species. figshare https://doi.org/10.6084/m9.figshare.28750034 (2025).Fonseca, P. L. et al. Global characterization of fungal mitogenomes: new insights on genomic diversity and dynamism of coding genes and accessory elements. 12, 787283 (2021).Wijayawardene, N. N. et al. Classes and phyla of the kingdom Fungi. 128, 1-165 (2024).Download referencesAcknowledgementsThis work was supported by the “MOC – MultiOmics Centre for Food and Health” project. The MOC project is co-funded by the European Union (European Regional Development Fund – EFRE). Ammar Abdalrahem was supported by a PhD fellowship from the French Ministry of Education and Research (MESR) and by the French Plan Investissement d’Avenir (PIA) Lab of Excellence ARBRE [ANR-11-LABX-0002- 01]. The authors thank the Department of Innovation, Research and University of the Autonomous Province of Bozen/Bolzano, Italy for covering the Open Access publication costs.Author informationAuthors and AffiliationsInstitute for Biomedicine, Eurac Research, Bolzano, 39100, ItalyMohamed S. Sarhan & Christian FuchsbergerDepartment CIBIO, University of Trento, Trento, ItalyMohamed S. SarhanUniversité de Lorraine, INRAE, IAM, F-54000, Nancy, FranceAmmar AbdalrahemPHIM, Université de Montpellier, IRD, CIRAD, INRAE, Institut Agro, Montpellier, FranceAmmar AbdalrahemInstitute for Mummy Studies, Eurac Research, Bolzano, 39100, ItalyFrank MaixnerAuthorsMohamed S. SarhanView author publicationsSearch author on:PubMed Google ScholarAmmar AbdalrahemView author publicationsSearch author on:PubMed Google ScholarFrank MaixnerView author publicationsSearch author on:PubMed Google ScholarChristian FuchsbergerView author publicationsSearch author on:PubMed Google ScholarContributionsM.S.S. conceived the original idea. M.S.S. and A.A. designed and performed the computational analysis. M.S.S. performed the data visualization and wrote the first draft of the manuscript. M.S.S. and A.A. curated the data for public deposition. F.M. and C.F. edited and revised the manuscript. All authors read and approved the final version of the manuscript.Corresponding authorCorrespondence to
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    Reprints and permissionsAbout this articleCite this articleSarhan, M.S., Abdalrahem, A., Maixner, F. et al. De novo assembly of complete circular mitochondrial genomes from 2,695 fungal species.
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