Differential elemental accumulation of the signal crayfish (Pacifastacus leniusculus) along an invasion gradient
Authors/Creators
- 1. University of Minho, Braga, Portugal
- 2. Adam Mickiewicz University, Poznań, Poland
- 3. Instituto Politécnico de Bragança, Bragança, Portugal
Description
The non-native signal crayfish (Pacifastacus leniusculus) can influence elemental cycling in aquatic ecosystems through bioaccumulation and transfer of chemical elements, with potential spatial variation along invasion gradients. In this study, we investigate the differences in elemental exposure in signal crayfish in the Rabaçal River, Portugal. We focus on potential intra-population differences along a well-defined invasion gradient, comparing individuals from the invasion core (upstream) and the downstream expanding front (n = 30 each). We examined 57 elements in the muscle of the signal crayfish, including essential elements (EEs): Mn, Co, Ni, Cu, Zn, Mg, Ca, Fe, Se, V, S; non-essential and potentially toxic elements (PTEs): Cd, Hg, Pb, U, As, Sr, Ba, Cr, Zr, Cs, Tl; and technology-critical elements (TCEs): Ti, Rb, La, Ce, Pr, Gd, Dy, Ho, Er, Yb, Ga, Ge, Hf, Ta, In, Re, Te, Pt. We explored the relationship between element concentrations and signal crayfish trophic ecology, inferred through stable isotope analysis (δ13C and δ15N), behaviour, and epibiotic associate load – factors known to shape invasion success through their effects on resource acquisition, competition, and physiological stress. Significant differences in element concentrations were found between individuals from the core and front. Individuals from the front showed higher levels (mean µg/kg, dry weight) of Co: (476 vs. 297), V: (390 vs. 262), Mn: (2.6 × 104 vs. 1.0 × 104), Hg: (2526 vs.1658), and Ta: (21 vs. 11). These patterns suggest that front individuals, with higher δ15N values and more exploratory behaviour, feed at higher trophic levels (e.g., macroinvertebrates), which may explain the elevated concentrations of biomagnifying elements such as Hg and Ta. On the other hand, individuals from the core had higher levels of Pb: (361 vs. 234), and Sr: (39772 vs. 20018), likely due to a diet based on basal resources, as supported by the strong negative correlation between Pb and δ13C, indicating reliance on benthic sources more prone to lead accumulation. This study increases our understanding of contaminant accumulation along an invasion gradient, offering insights for management practices – such as targeted removal of highly contaminated individuals, improved monitoring of metal levels in invaded areas, and public awareness campaigns – to minimise ecological impacts on higher trophic levels.
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References
- Adeel M, Lee JY, Zain M, Rizwan M, Nawab A, Ahmad MA, Shafiq M, Yi H, Jilani G, Javed R, Horton R, Rui Yukui Tsang CWD, Xing B (2019) Cryptic footprints of rare earth elements on natural resources and living organisms. Environment International 127: 785–800. https://doi.org/10.1016/j.envint.2019.03.022
- Alves H, Gonçalves D, Nogueira AB, Teixeira A, Padilha J, Sousa R (2025) Intrapopulation differences in biological traits and impacts in a highly invasive freshwater species. NeoBiota 97: 325–349. https://doi.org/10.3897/neobiota.97.127861
- Aquiloni L, Gherardi F (2010) Crayfish females eavesdrop on fighting males and use smell and sight to recognize the identity of the winner. Animal Behaviour 79(2): 265–269. https://doi.org/10.1016/j.anbehav.2009.09.024
- Balaram V (2019) Rare earth elements: A review of applications, occurrence, exploration, analysis, recycling, and environmental impact. Geoscience Frontiers 10(4): 1285–1303. https://doi.org/10.1016/j.gsf.2018.12.005
- Balzani P, Vizzini S, Frizzi F, Masoni A, Lessard JP, Bernasconi C, Santini G (2021) Plasticity in the trophic niche of an invasive ant explains establishment success and long‐term coexistence. Oikos 130(5): 691–696. https://doi.org/10.1111/oik.08217
- Balzani P, Kouba A, Tricarico E, Kourantidou M, Haubrock PJ (2022) Metal accumulation in relation to size and body condition in an all-alien species community. Environmental Science and Pollution Research International 29(17): 25848–25857. https://doi.org/10.1007/s11356-021-17621-0
- Bellante A, Maccarone V, Buscaino G, Buffa G, Filiciotto F, Traina A, Del Core M, Mazzola S, Sprovieri M (2015) Trace element concentrations in red swamp crayfish (2015) and surface sediments in Lake Preola and Gorghi Tondi natural reserve, SW Sicily. Environmental Monitoring and Assessment 187: 1–18. https://doi.org/10.1007/s10661-015-4613-4
- Bernardo JM, Costa AM, Bruxelas S, Teixeira A (2011) Dispersal and coexistence of two non-native crayfish species (Pacifastacus leniusculus and Procambarus clarkii) in NE Portugal over a 10-year period. Knowledge and Management of Aquatic Ecosystems (401): 28. https://doi.org/10.1051/kmae/2011047
- Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends in Ecology & Evolution 23(7): 361–368. https://doi.org/10.1016/j.tree.2008.04.003
- Breithaupt T, Eger P (2002) Urine makes the difference: Chemical communication in fighting crayfish made visible. The Journal of Experimental Biology 205(9): 1221–1231. https://doi.org/10.1242/jeb.205.9.1221
- Brown C, Burgess F, Braithwaite VA (2007) Heritable and experiential effects on boldness in a tropical poeciliid. Behavioral Ecology and Sociobiology 62: 237–243. https://doi.org/10.1007/s00265-007-0458-3
- Capurro M, Galli L, Mori M, Salvidio S, Arillo A (2015) Reproductive cycle of Pacifastacus leniusculus (Dana) (Crustacea: Decapoda) from the Brugneto Lake (Liguria, northwest Italy). The Italian Journal of Zoology 82(3): 366–377. https://doi.org/10.1080/11250003.2015.1022235
- Carvalho F, Pascoal C, Cássio F, Teixeira A, Sousa R (2022) Combined per‐capita and abundance effects of an invasive species on native invertebrate diversity and a key ecosystem process. Freshwater Biology 67(5): 828–841. https://doi.org/10.1111/fwb.13884
- Carvalho F, Alves H, Pascoal C, Castro P, Miranda F, Teixeira A, Sousa R (2025) Invasive dynamics of the signal crayfish Pacifastacus leniusculus in a protected area. Hydrobiologia 852(3): 705–720. https://doi.org/10.1007/s10750-024-05717-w
- Castro J, de Figueiredo T, Fonseca F, Castro JP, Nobre S, Pires LC (2010) Montesinho Natural Park: general description and natural values. Natural heritage from East to West: case studies from 6 EU countries, 119–132. https://doi.org/10.1007/978-3-642-01577-9_15
- de Almeida Rodrigues P, Ferrari RG, Dos Santos LN, Junior CAC (2019) Mercury in aquatic fauna contamination: a systematic review on its dynamics and potential health risks. Journal of Environmental Sciences 84: 205–218. https://doi.org/10.1016/j.jes.2019.02.018
- DeWitt PD, Williams BW, Lu ZQ, Fard AN, Gelder SR (2013) Effects of environmental and host physical characteristics on an aquatic symbiont. Limnologica 43(3): 151–156. https://doi.org/10.1016/j.limno.2012.07.009
- Dobrzycka-Krahel A, Skóra ME, Malek M (2024) Human consumption of non-native species in a circular economy: determination of persistent organic pollutants in the invasive signal crayfish from a Baltic Coastal River and its assessment for consumption. Sustainability 16(9): 3532. https://doi.org/10.3390/su16093532
- Dudgeon D (2019) Multiple threats imperil freshwater biodiversity in the Anthropocene. Current Biology 29(19): R960–R967. https://doi.org/10.1016/j.cub.2019.08.002
- Dung LV, Tue NT, Lam PV, Quy TD, Canh VM, Tam ND, Nhuan MT (2023) Stable isotopes (δ13C and δ15N) and trace elements of invertebrates and fish from the coastal waters of Ha Tinh Province, central Vietnam. Archives of Environmental Contamination and Toxicology 85(3): 229–244. https://doi.org/10.1007/s00244-023-00992-5
- Espejo W, Kitamura D, Kidd KA, Celis JE, Kashiwada S, Galbán-Malagón C, Barra R, Chiang G (2018) Biomagnification of Tantalum through Diverse Aquatic Food Webs. Environmental Science & Technology Letters 5(4): 196–201. https://doi.org/10.1021/acs.estlett.8b00051
- Espejo W, Chiang G, Kitamura D, Kashiwada S, O'Driscoll NJ, Celis JE (2023) Occurrence of rare earth elements (REEs) and trace elements (TEs) in feathers of adult and young Gentoo penguins from King George Island, Antarctica. Marine Pollution Bulletin 187: 114575. https://doi.org/10.1016/j.marpolbul.2023.114575
- Esposito M, De Roma A, D'Alessio N, Danese A, Gallo P, Galiero G, Santoro M (2020) First study on PCBs, organochlorine pesticides, and trace elements in the Eurasian otter (Lutra lutra) from southern Italy. The Science of the Total Environment 749: 141452. https://doi.org/10.1016/j.scitotenv.2020.141452
- Ficetola GF, Siesa ME, De Bernardi F, Padoa-Schioppa E (2012) Complex impact of an invasive crayfish on freshwater food webs. Biodiversity and Conservation 21: 2641–2651. https://doi.org/10.1007/s10531-012-0323-1
- Galib SM, Sun J, Twiss SD, Lucas MC (2022) Personality, density and habitat drive the dispersal of invasive crayfish. Scientific Reports 12(1): 1114. https://doi.org/10.1038/s41598-021-04228-1
- Gedik K, Kongchum M, DeLaune RD, Sonnier JJ (2017) Distribution of arsenic other metals in crayfish tissues (2017) under different production practices. The Science of the Total Environment 574: 322–331. https://doi.org/10.1016/j.scitotenv.2016.09.060
- Gherardi F, Aquiloni L, Diéguez-Uribeondo J, Tricarico E (2011) Managing invasive crayfish: Is there a hope? Aquatic Sciences 73(2): 185–200. https://doi.org/10.1007/s00027-011-0181-z
- Groen M, Sopinka NM, Marentette JR, Reddon AR, Brownscombe JW, Fox MG, Marsh Rollo SE, Balshine S (2012) Is there a role for aggression in round goby invasion fronts? Behaviour 149(7): 685–703. https://doi.org/10.1163/1568539X-00002998
- Gruber J, Brown G, Whiting MJ, Shine R (2018) Behavioural divergence during biological invasions: A study of cane toads (Rhinella marina) from contrasting environments in Hawai'i. Royal Society Open Science 5(4): 180197. https://doi.org/10.1098/rsos.180197
- Guan RZ, Wiles P (1997) The home range of the signal crayfish in a British lowland river. Freshwater forum 8: 45–54.
- Güner U (2010) Heavy metal effects on P, Ca, Mg, and total protein contents in embryonic pleopodal eggs and stage-1 juveniles of freshwater crayfish Astacus leptodactylus (Eschscholtz, 1823). Turkish Journal of Biology 34(4): 405–412. https://doi.org/10.3906/biy-0811-19
- Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends in Ecology & Evolution 19(9): 470–474. https://doi.org/10.1016/j.tree.2004.07.005
- Gutiérrez JL, Jones CG, Sousa R (2014) Toward an integrated ecosystem perspective of invasive species impacts. Acta Oecologica 54: 131–138. https://doi.org/10.1016/j.actao.2013.10.003
- Gwenzi W, Mangori L, Danha C, Chaukura N, Dunjana N, Sanganyado E (2018) Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. The Science of the Total Environment 636: 299–313. https://doi.org/10.1016/j.scitotenv.2018.04.235
- Haubrock PJ, Soto I, Ahmed DA, Ansari AR, Tarkan AS, Kurtul I, Macêdo RL, Lázaro‐Lobo A, Toutain M, Parker B, Błońska D, Guareschi S, Cano-Barbacil S, Almela VD, Andreou D, Moyano J, Akalın S, Kaya C, Bayçelebi E, Yoğurtçuoğlu B, Briski E, Aksu S, Emiroğlu O, Mammola S, Santis SD, Kourantidou M, Pincheira-Donoso D, Britton JR, Kouba A, Dolan EJ, Kirichenko NI, García-Berthou E, Renault D, Fernandez RD, Yapıcı S, Giannetto D, Nuñez MA, Hudgins EJ, Pergl J, Milardi M, Musolin DL, Cuthbert RN (2024) Biological invasions are a population-level rather 836 than a species-level phenomenon. Global Change Biology 30: e17312. https://doi.org/10.1111/gcb.17312
- Herse MR, With KA, Boyle WA (2018) The importance of core habitat for a threatened species in changing landscapes. Journal of Applied Ecology 55(5): 2241–2252. https://doi.org/10.1111/1365-2664.13234
- Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal. Biometrische Zeitschrift 50(3): 346–363. https://doi.org/10.1002/bimj.200810425
- Hudina S, Žganec K, Hock K (2015) Differences in aggressive behaviour along the expanding range of an invasive crayfish: An important component of invasion dynamics. Biological Invasions 17: 3101–3112. https://doi.org/10.1007/s10530-015-0936-x
- Islam MR, Akash S, Jony MH, Alam MN, Nowrin FT, Rahman MM, Thiruvengadam M (2023) Exploring the potential function of trace elements in human health: A therapeutic perspective. Molecular and Cellular Biochemistry 478(10): 2141–2171. https://doi.org/10.1007/s11010-022-04638-3
- Jackson MC, Britton JR (2014) Divergence in the trophic niche of sympatric freshwater invaders. Biological Invasions 16: 1095–1103. https://doi.org/10.1007/s10530-013-0563-3
- Jackson A, Parnell A (2023) SIBER: Stable Isotope Bayesian Ellipses in R (Version 2.1.9). [R package]
- Johnson BL, Willacker JJ, Eagles‐Smith CA, Pearl CA, Adams MJ (2014) Invasive crayfish as vectors of mercury in freshwater food webs of the Pacific Northwest. Environmental Toxicology and Chemistry 33(11): 2639–2645. https://doi.org/10.1002/etc.2727
- Kouba A, Buřič M, Kozák P (2010) Bioaccumulation and effects of heavy metals in crayfish: A review. Water, Air, and Soil Pollution 211: 5–16. https://doi.org/10.1007/s11270-009-0273-8
- Lee JH, Kim TW, Choe JC (2009) Commensalism or mutualism: Conditional outcomes in a branchiobdellid–crayfish symbiosis. Oecologia 159: 217–224. https://doi.org/10.1007/s00442-008-1195-7
- Let M, Ložek F, Kouba A, Buřič M, Bláha M (2023) Signal crayfish as a threat for European ectosymbionts: Overlooked biodiversity losses. Aquatic Sciences 85(1): 30. https://doi.org/10.1007/s00027-022-00932-w
- Li H, Li H, Zhang H, Cao J, Ge T, Gao J, Fang Yan Ye W, Fang T, Shi Y, Zhang R, Dong X, Guo X, Zhang Y (2023) Trace elements in red swamp crayfish (Procambarus clarkii) in China: Spatiotemporal variation and human health implications. The Science of the Total Environment 857: 159749. https://doi.org/10.1016/j.scitotenv.2022.159749
- Malhotra N, Hsu HS, Liang ST, Roldan MJM, Lee JS, Ger TR, Hsiao CD (2020) An updated review of toxicity effect of the rare earth elements (REEs) on aquatic organisms. Animals (Basel) 10(9): 1663. https://doi.org/10.3390/ani10091663
- Mistri M, Munari C, Pagnoni A, Chenet T, Pasti L, Cavazzini A (2020) Accumulation of trace metals in crayfish tissues: Is Procambarus clarkii a vector of pollutants in Po Delta inland waters? The European Zoological Journal 87(1): 46–57. https://doi.org/10.1080/24750263.2020.1717653
- Morales F (2004) Metapopulation structure of the queen conch, Strombus gigas (Linne, 1758) throughout the Intra-Americas Sea. Florida Institute of Technology.
- Myles-Gonzalez E, Burness G, Yavno S, Rooke A, Fox MG (2015) To boldly go where no goby has gone before: boldness, dispersal tendency, and metabolism at the invasion front. Behavioral Ecology 26(4): 1083–1090. https://doi.org/10.1093/beheco/arv050
- Nędzarek A, Czerniejewski P, Tórz A (2020) Macroelements and trace elements in invasive signal crayfish (Pacifastacus leniusculus) from the Wieprza River (Southern Baltic): Human health implications. Biological Trace Element Research 197: 304–315. https://doi.org/10.1007/s12011-019-01978-y
- Nogueira JG, Lopes-Lima M, Varandas S, Teixeira A, Sousa R (2021a) Effects of an extreme drought on the endangered pearl mussel Margaritifera margaritifera: A before/after assessment. Hydrobiologia 848: 3003–3013. https://doi.org/10.1007/s10750-019-04103-1
- Nogueira JG, Teixeira A, Lopes-Lima M, Varandas S, Sousa R (2021b) Assessment of terrestrial protected areas for the conservation of freshwater biodiversity. Aquatic Conservation 31: 520–530. https://doi.org/10.1002/aqc.3502
- Olsson K, Stenroth P, Nyström PER, Granéli W (2009) Invasions and niche width: Does niche width of an introduced crayfish differ from a native crayfish? Freshwater Biology 54(8): 1731–1740. https://doi.org/10.1111/j.1365-2427.2009.02221.x
- Pacioglu O, Zubrod JP, Schulz R, Jones JI, Pârvulescu L (2019) Two is better than one: Combining gut content and stable isotope analyses to infer trophic interactions between native and invasive species. Hydrobiologia 839(1): 25–35. https://doi.org/10.1007/s10750-019-03990-8
- Pereira P, Pereira D, Caetano Alves MI (2007) Geomorphosite assessment in Montesinho natural park (Portugal). Geographica Helvetica 62(3): 159–168. https://doi.org/10.5194/gh-62-159-2007
- Phillips BL, Kelehear C, Pizzatto L, Brown GP, Barton D, Shine R (2010) Parasites and pathogens lag behind their host during periods of host range advance. Ecology 91(3): 872–881. https://doi.org/10.1890/09-0530.1
- Picone M, Distefano GG, Corami F, Franzoi P, Bristol SR, Basso M, Panzarin L, Ghirardini AV (2022) Occurrence of rare earth elements in fledgelings of Thalasseus sandvicensis. Environmental Research 204: 112152. https://doi.org/10.1016/j.envres.2021.112152
- Plummer M (2024) rjags: Bayesian Graphical Models using MCMC (Version 4-16). [R package]
- R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
- Raven PJ, Holmes NTH, Dawson FH, Everard M (1998) Quality assessment using river habitat survey data. Aquatic Conservation 8(4): 477–499. https://doi.org/10.1002/(SICI)1099-0755(199807/08)8:4<477::AID-AQC299>3.0.CO;2-K
- Rebrina F, Skejo J, Lucić A, Hudina S (2015) Trait variability of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region reflects potential benefits and trade-offs during dispersal. Aquatic Invasions 10(1): 41–50. https://doi.org/10.3391/ai.2015.10.1.04
- Rosewarne PJ, Mortimer RJG, Dunn AM (2012) Branchiobdellidan infestation on endangered white-clawed crayfish (Austropotamobius pallipes) in the UK. Parasitology 139(6): 774–780. https://doi.org/10.1017/S003118201100240X
- Rowe CL, Hopkins WA, Zehnder C, Congdon JD (2001) Metabolic costs incurred by crayfish (Procambarus acutus) in a trace element-polluted habitat: Further evidence of similar responses among diverse taxonomic groups. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 129(3): 275–283. https://doi.org/10.1016/S1532-0456(01)00204-6
- Saad AA, El-Sikaily A, Kassem H (2014) Essential, non-essential metals and human health. Blue Biotechnology Journal 3(4): 447.
- Sayer CA, Fernando E, Jimenez RR, Macfarlane NB, Rapacciuolo G, Böhm M, Darwall WR (2025) One-quarter of freshwater fauna threatened with extinction. Nature 638: 138–145. https://doi.org/10.1038/s41586-024-08375-z
- Schober P, Boer C, Schwarte LA (2018) Correlation coefficients: appropriate use and interpretation. Anesthesia & Analgesia 126(5): 1763–1768. https://doi.org/10.1213/ANE.0000000000002864
- Simberloff D (2010) Invasive species. In: Sodhi NS, Ehrlich PR (Eds) Conservation Biology for All. Oxford Academic, Oxford, 131–152. https://doi.org/10.1093/acprof:oso/9780199554232.003.0008
- Skelton J, Farrell KJ, Creed RP, Williams BW, Ames C, Helms BS, Brown BL (2013) Servants, scoundrels, and hitchhikers: Current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida). Freshwater Science 32(4): 1345–1357. https://doi.org/10.1899/12-198.1
- Soto I, Le Hen G, Buřič M, Cuthbert RN, Haubrock PJ, Sentis A, Kouba A (2023) Sustained ecological impacts of invasive crayfish following claw injury. Inland Waters 13(4): 534–544. https://doi.org/10.1080/20442041.2024.2321088
- Sousa R, Dias S, Antunes C (2007) Subtidal macrobenthic structure in the lower Lima estuary, NW of Iberian Peninsula. Annales Zoologici Fennici: 303–313.
- Sousa R, Freitas F, Nogueira AJA, Mota M, Antunes C (2013) Invasive dynamics of the crayfish Procambarus clarkii (Girard, 1852) at the international section of the River Minho (NW of the Iberian Peninsula). Aquatic Conservation 23: 656–666. https://doi.org/10.1002/aqc.2323
- Sousa R, Amorim A, Froufe E, Varandas S, Teixeira A, Lopes-Lima M (2015) Conservation status of the freshwater pearl mussel Margaritifera margaritifera in Portugal. Limnologica 50: 4–10. https://doi.org/10.1016/j.limno.2014.07.004
- Sousa R, Ferreira A, Carvalho F, Lopes-Lima M, Varandas S, Teixeira A (2018) Die-offs of the endangered pearl mussel Margaritifera margaritifera during an extreme drought. Aquatic Conservation 28: 1244–1248. https://doi.org/10.1002/aqc.2945
- Sousa R, Nogueira J, Ferreira A, Carvalho F, Lopes-Lima M, Varandas S, Teixeira A (2019) A tale of shells and claws: The signal crayfish as a threat to the pearl mussel Margaritifera margaritifera in Europe. The Science of the Total Environment 665: 329–337. https://doi.org/10.1016/j.scitotenv.2019.02.094
- Sousa R, Ferreira A, Carvalho F, Lopes-Lima M, Varandas S, Teixeira A, Gallardo B (2020) Small hydropower plants as a threat to the endangered pearl mussel Margaritifera margaritifera. The Science of the Total Environment 719: 137361. https://doi.org/10.1016/j.scitotenv.2020.137361
- Sousa R, Nogueira JG, Padilha J (2024) Moving from the species to the population level in biological invasions. Global Change Biology 30(7): e17396. https://doi.org/10.1111/gcb.17396
- Suárez-Serrano A, Alcaraz C, Ibanez C, Trobajo R, Barata C (2010) Procambarus clarkii as a bioindicator of heavy metal pollution sources in the lower Ebro River and Delta. Ecotoxicology and Environmental Safety 73(3): 280–286. https://doi.org/10.1016/j.ecoenv.2009.11.001
- Vedia I (2018) Ecología del cangrejo señal y sus interacciones con la biodiversidad.
- Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Davies P (2010) Global threats to human water security and river biodiversity. Nature 467(7315): 555–561. https://doi.org/10.1038/nature09440
- Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. https://doi.org/10.1007/978-3-319-24277-4_9
- Wickham H, Bryan J (2023) readxl: Read Excel Files (Version 1.4.3). [R package]
- Wickham H, Hester J, Chang W, Bryan J (2022) devtools: Tools to Make Developing R Packages Easier (Version 2.4.5). [R package]
- Wickham H, François R, Henry L, Müller K, Vaughan D (2023) dplyr: A Grammar of Data Manipulation (Version 1.1.4). [R package]
- WWF (2024) Living Planet Report 2024 – A System in Peril. WWF, Gland, Switzerland.
- Yagound B, West AJ, Richardson MF, Selechnik D, Shine R, Rollins LA (2022) Brain transcriptome analysis reveals gene expression differences associated with dispersal behaviour between range‐front and range‐core populations of invasive cane toads in Australia. Molecular Ecology 31(6): 1700–1715. https://doi.org/10.1111/mec.16347
- Zhang L, Song Z, Zhou Y, Zhong S, Yu Y, Liu T, Gao X, Li L, Kong C, Wang X, He L, Gan J (2023) The accumulation of toxic elements (Pb, Hg, Cd, As, and Cu) in red swamp crayfish (Procambarus clarkii) in Qianjiang and the associated risks to human health. Toxics 11(7): 635. https://doi.org/10.3390/toxics11070635
- Zieritz A, Bogan AE, Rahim KAA, Sousa R, Jainih L, Harun S, Lopes-Lima M (2018) Changes and drivers of freshwater mussel diversity and distribution in northern Borneo. Biological Conservation 219: 126–137. https://doi.org/10.1016/j.biocon.2018.01.012
- Zoroddu MA, Aaseth J, Crisponi G, Medici S, Peana M, Nurchi VM (2019) The essential metals for humans: A brief overview. Journal of Inorganic Biochemistry 195: 120–129. https://doi.org/10.1016/j.jinorgbio.2019.03.013