Philippa Kaur

Wernberg, T., Krumhansl, K. A., Filbee-Dexter, K. & Pedersen, M. Status and trends for the world’s kelp forests. In World Seas: An Environmental Evaluation (ed. Sheppard, C.) 57–78 (Elsevier, 2019).Chapter 

Google Scholar 
Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9, 306–312. https://doi.org/10.1038/s41558-019-0412-1 (2019).ADS 
Article 

Google Scholar 
Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172. https://doi.org/10.1126/science.aad8745 (2016).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Coleman, M. A., Minne, A. J. P., Vranken, S. & Wernberg, T. Genetic tropicalisation following a marine heatwave. Sci. Rep. UK 10, 12726. https://doi.org/10.1038/s41598-020-69665-w (2020).ADS 
CAS 
Article 

Google Scholar 
Krumhansl, K. A. et al. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. 113, 13785–13790. https://doi.org/10.1073/pnas.1606102113 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Arafeh-Dalmau, N. et al. Extreme marine heatwaves alter kelp forest community near its equatorward distribution limit. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00499 (2019).Article 

Google Scholar 
Tanaka, K., Taino, S., Haraguchi, H., Prendergast, G. & Hiraoka, M. Warming off southwestern Japan linked to distributional shifts of subtidal canopy-forming seaweeds. Ecol. Evol. 2, 2854–2865. https://doi.org/10.1002/ece3.391 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Wernberg, T. et al. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep. UK 8, 1851. https://doi.org/10.1038/s41598-018-20009-9 (2018).ADS 
CAS 
Article 

Google Scholar 
Graham, M. H., Kinlan, B. P., Druehl, L. D., Garske, L. E. & Banks, S. Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc. Natl. Acad. Sci. 104, 16576. https://doi.org/10.1073/pnas.0704778104 (2007).ADS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Marzinelli, E. M. et al. Large-scale geographic variation in distribution and abundance of Australian deep-water kelp forests. PLoS ONE 10, e0118390. https://doi.org/10.1371/journal.pone.0118390 (2015).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Varela, R., Rodríguez-Díaz, L., de Castro, M. & Gómez-Gesteira, M. Influence of Eastern Upwelling systems on marine heatwaves occurrence. Glob. Planet Change 196, 103379. https://doi.org/10.1016/j.gloplacha.2020.103379 (2021).Article 

Google Scholar 
Assis, J. et al. Deep reefs are climatic refugia for genetic diversity of marine forests. J. Biogeogr. 43, 833–844. https://doi.org/10.1111/jbi.12677 (2016).Article 

Google Scholar 
Lourenço, C. R. et al. Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. J. Biogeogr. 43, 1595–1607. https://doi.org/10.1111/jbi.12744 (2016).Article 

Google Scholar 
Vranken, S. et al. Genotype-environment mismatch of kelp forests under climate change. Mol. Ecol. 30, 3730–3746. https://doi.org/10.1111/mec.15993 (2021).Article 
PubMed 

Google Scholar 
Wood, G. et al. Genomic vulnerability of a dominant seaweed points to future-proofing pathways for Australia’s underwater forests. Glob. Change Biol. 27, 2200–2212. https://doi.org/10.1111/gcb.15534 (2021).ADS 
Article 

Google Scholar 
Wernberg, T. et al. Biology and ecology of the globally significant kelp Ecklonia radiata. Oceanogr. Mar. Biol.: An Annu. Rev. 57, 265–324 (2019).Article 

Google Scholar 
Durrant, H. M. S., Barrett, N. S., Edgar, G. J., Coleman, M. A. & Burridge, C. P. Shallow phylogeographic histories of key species in a biodiversity hotspot. Phycologia 54, 556–565. https://doi.org/10.2216/15-24.1 (2015).Article 

Google Scholar 
Rothman, M. D. et al. A molecular investigation of the genus Ecklonia (Phaeophyceae, Laminariales) with special focus on the southern hemisphere. J. Phycol. 51, 236–246. https://doi.org/10.1111/jpy.12264 (2015).CAS 
Article 
PubMed 

Google Scholar 
Starko, S. et al. A comprehensive kelp phylogeny sheds light on the evolution of an ecosystem. Mol. Phylogenetics Evol. 136, 138–150. https://doi.org/10.1016/j.ympev.2019.04.012 (2019).Article 

Google Scholar 
Shepherd, S. A. & Edgar, G. J. In (eds Shepherd, S. A. & Edgar, G. J.) (CSIRO Publishing, 2013).Guiry, M. D. et al. AlgaeBase: An on-line resource for algae. Cryptogam. Algol. 35, 105–115, 111 (2014).Barratt, L., Ormond, R. F. G. & Wrathall, T. J. Ecological studies of southern Oman kelp communities. Part 1. Ecology and productivity of the sublittoral algae Ecklonia radiata and Sargassopsis zanardinii (Council for the conservation of the environment and water resources, and regional organisation for the protection of the marine environment, Muscat and Kuwait, 1986).Barratt, L. et al. An ecological study of the rocky shores on the south coast of Oman. Report of IUCN to UNEP’s regional seas programme, Vol. 104 (Tropical Marine Research Unit, York, 1984).Klaus, R. & Turner, J. R. The marine biotopes of the Socotra Archipelago. Fauna Arab. 20, 45–116 (2004).
Google Scholar 
Claereboudt, M. R. Oman. In World Seas: An Environmental Evaluation, (ed. Sheppard, C.) 25–47 (Academic Press, 2019).Savidge, G., Lennon, H. J. & Matthews, A. D. A shore based survey of oceanographic variables in the Dhofar region of southern Oman, August–October 1985. In Ecological Studies of Southern Oman Kelp Communities. Summary Report, 4–21. ROPME/GC-6/001 (1988).Hatcher, B. G., Kirkman, H. & Wood, W. F. Growth of the kelp Ecklonia-radiata near the northern limit of its range in Western-Australia. Mar. Biol. 95, 63–73. https://doi.org/10.1007/Bf00447486 (1987).Article 

Google Scholar 
Veenhof, R. et al. Kelp gametophytes in changing oceans. Oceanogr. Mar. Biol. Annu. Rev. 60 (in press).Goes, J. I., Thoppil, P. G., Gomes, H. D. R. & Fasullo, J. T. Warming of the Eurasian landmass is making the Arabian sea more productive. Science 308, 545. https://doi.org/10.1126/science.1106610 (2005).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Roxy, M. K. et al. A reduction in marine primary productivity driven by rapid warming over the tropical Indian Ocean. Geophys. Res. Lett. 43, 826–833. https://doi.org/10.1002/2015GL066979 (2016).ADS 
Article 

Google Scholar 
Watanabe, T. K., Watanabe, T., Yamazaki, A., Pfeiffer, M. & Claereboudt, M. R. Oman coral δ18O seawater record suggests that Western Indian Ocean upwelling uncouples from the Indian Ocean Dipole during the global-warming hiatus. Sci. Rep. UK 9, 1887. https://doi.org/10.1038/s41598-018-38429-y (2019).ADS 
CAS 
Article 

Google Scholar 
Watanabe, T. K. et al. Past summer upwelling events in the Gulf of Oman derived from a coral geochemical record. Sci. Rep. UK 7, 4568. https://doi.org/10.1038/s41598-017-04865-5 (2017).ADS 
CAS 
Article 

Google Scholar 
Edwards, M. & Estes, J. A. Catastrophe, recovery and range limitation in NE Pacific kelp forests: a large-scale perspective. Mar. Ecol. Prog. Ser. 320, 79–87 (2006).ADS 
Article 

Google Scholar 
Glynn, P. W. Monsoonal upwelling and episodic Acanthaster predation as probable controls of coral reef distribution and community structure in Oman, Indian Ocean. Atoll Res. Bull. 379, 1–66 (1993).Article 

Google Scholar 
Hiscock, S., Barratt, L. & Ormond, R. The marine algae of Dhofar, Oman-an upwelling system in the Arabian Sea. Br. Phycol. J. 19, 194 (1984).Article 

Google Scholar 
Kirkman, H. The 1st year in the life-history and the survival of the juvenile marine macrophyte, Ecklonia-radiata (Turn) J Agardh. J. Exp. Mar. Biol. Ecol. 55, 243–254. https://doi.org/10.1016/0022-0981(81)90115-5 (1981).Article 

Google Scholar 
Maeda, T., Kawai, T., Nakaoka, M. & Yotsukura, N. Effective DNA extraction method for fragment analysis using capillary sequencer of the kelp, Saccharina. J. Appl. Phycol. 25, 337–347 (2013).CAS 
Article 

Google Scholar 
Voisin, M., Engel, C. R. & Viard, F. Differential shuffling of native genetic diversity across introduced regions in a brown alga: Aquaculture vs. maritime traffic effects. Proc. Natl. Acad. Sci. USA 102, 5432. https://doi.org/10.1073/pnas.0501754102 (2005).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Lane, C. E., Lindstrom, S. C. & Saunders, G. W. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenetics Evol. 44, 634–648 (2007).CAS 
Article 

Google Scholar 
Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Johnson, M. et al. NCBI BLAST: A better web interface. Nucl. Acids Res. 36, W5–W9 (2008).CAS 
Article 

Google Scholar 
Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucl. Acids Res. 44, W232–W235 (2016).CAS 
Article 

Google Scholar 
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).CAS 
Article 

Google Scholar 
Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008. https://doi.org/10.1093/sysbio/syw037 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).CAS 
Article 

Google Scholar 
Rambaut, A. & Drummond, A. FigTree: Tree Figure Drawing Tool, Version 1.2. 2 (Institute of Evolutionary Biology, University of Edinburgh, 2008).
Google Scholar 
Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302. https://doi.org/10.1093/molbev/msx248 (2017).CAS 
Article 
PubMed 

Google Scholar 
Clement, M., Posada, D. & Crandall, K. A. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x (2000).CAS 
Article 
PubMed 

Google Scholar 
Leigh, J. W. & Bryant, D. popart: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).Article 

Google Scholar 
Team, R. C. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).Vergés, A. et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl. Acad. Sci. 113, 13791–13796. https://doi.org/10.1073/pnas.1610725113 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Wood, G. et al. Using genetics to test provenance effects and to optimise seaweed restoration. J. Appl. Ecol. https://doi.org/10.1111/1365-2664.13707 (2020).Article 

Google Scholar 
Wynne, M. J. A checklist of the benthic marine algae of the Northern Arabian Sea coast of the Sultanate of Oman. Bot. Mar. 61, 481–498. https://doi.org/10.1515/bot-2018-0035 (2018).Richards, G. & Wynne, M. J. 57 (2003).Schils, T. Marine Plant Communities of Upwelling Areas Within the Arabian Sea: A Taxonomic, Ecological ABD Biogeographic Case Study on the Marine Flora of the Socotra Archipelago (Yemen) and Masirah Island (Oman). PhD thesis (2002).Schils, T. & Coppejans, E. Phytogeography of upwelling areas in the Arabian Sea. J. Biogeogr. 30, 1339–1356. https://doi.org/10.1046/j.1365-2699.2003.00933.x (2003).Article 

Google Scholar 
Schils, T. & Wilson, S. C. temperature threshold as a biogeographic barrier in northern Indian Ocean Macroalgae. J. Phycol. 42, 749–756. https://doi.org/10.1111/j.1529-8817.2006.00242.x (2006).Article 

Google Scholar 
Wiggert, J. D., Hood, R. R., Banse, K. & Kindle, J. C. Monsoon-driven biogeochemical processes in the Arabian Sea. Prog. Oceanogr. 65, 176–213. https://doi.org/10.1016/j.pocean.2005.03.008 (2005).ADS 
Article 

Google Scholar 
Serisawa, Y., Imoto, Z., Ishikawa, T. & Ohno, M. Decline of the Ecklonia cava population associated with increased seawater temperatures in Tosa Bay, southern Japan. Fish. Sci. 70, 189–191. https://doi.org/10.1111/j.0919-9268.2004.00788.x (2004).CAS 
Article 

Google Scholar 
Nelson, W., Duffy, C., Trnski, T. & Stewart, R. Mesophotic Ecklonia radiata (Laminariales) at Rangitāhua, Kermadec Islands, New Zealand. Phycologia 57, 534–538. https://doi.org/10.2216/18-9.1 (2018).Article 

Google Scholar 
Richmond, S. & Stevens, T. Classifying benthic biotopes on sub-tropical continental shelf reefs: How useful are abiotic surrogates?. Estuar. Coast. Shelf Sci. 138, 79–89. https://doi.org/10.1016/j.ecss.2013.12.012 (2014).ADS 
Article 

Google Scholar 
Davis, T. R., Champion, C. & Coleman, M. A. Climate refugia for kelp within an ocean warming hotspot revealed by stacked species distribution modelling. Mar. Environ. Res. 166, 105267. https://doi.org/10.1016/j.marenvres.2021.105267 (2021).CAS 
Article 
PubMed 

Google Scholar 
Jooste, C. M., Oliver, J., Emami-Khoyi, A. & Teske, P. R. Is the Wild Coast in eastern South Africa a distinct marine bioregion?. Helgol. Mar. Res. 72, 6. https://doi.org/10.1186/s10152-018-0509-3 (2018).Article 

Google Scholar 
Bolton, J. J. et al. Where is the western limit of the tropical Indian Ocean seaweed flora? An analysis of intertidal seaweed biogeography on the east coast of South Africa. Mar. Biol. 144, 51–59. https://doi.org/10.1007/s00227-003-1182-9 (2004).Article 

Google Scholar 
Bolton, J. J. The biogeography of kelps (Laminariales, Phaeophyceae): A global analysis with new insights from recent advances in molecular phylogenetics. Helgol. Mar. Res. 64, 263–279. https://doi.org/10.1007/s10152-010-0211-6 (2010).ADS 
Article 

Google Scholar 
Bolton JJ, De Clerck O, John DM (2003). Seaweed diversity patterns in Sub-Saharan Africa. In Proceedings of the Marine Biodiversity in Sub-Saharan Africa: The Known and the Unknown. (eds. Decker, C. et al. ) Cape Town, South Africa, pp. 229–241 (2003).Wood, M. et al. Zanzibar and Indian Ocean trade in the first millennium CE: The glass bead evidence. Archaeol. Anthropol. Sci. 9, 879–901. https://doi.org/10.1007/s12520-015-0310-z (2017).Article 

Google Scholar 
Pollard, E., Bates, R., Ichumbaki, E. B. & Bita, C. Shipwreck evidence from Kilwa, Tanzania. Int. J. Naut. Archaeol. 45, 352–369. https://doi.org/10.1111/1095-9270.12185 (2016).Article 

Google Scholar 
Staples, M. In Oman. A Maritime History (eds Al Salimi, A. & Staples, E.) Chap. 4, 81–116 (Georg Olms Verlag, 2017).Assis, J. et al. Past climate changes and strong oceanographic barriers structured low-latitude genetic relics for the golden kelp Laminaria ochroleuca. J. Biogeogr. 45, 2326–2336. https://doi.org/10.1111/jbi.13425 (2018).Article 

Google Scholar 
Wade, R. et al. Macroalgal germplasm banking for conservation, food security, and industry. PLoS Biol. 18, e3000641. https://doi.org/10.1371/journal.pbio.3000641 (2020).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Coleman, M. A. et al. Restore or redefine: Future trajectories for restoration. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00237 (2020).Article 

Google Scholar  More

This is the first study analyzing mandible shape in both mink species and, together with a previous study on their cranial shape38, it has revealed how small morphological differences in highly similar species can lead to substantial biomechanical differences (see breakdown below). As with cranial shape, mandible shape in minks is influenced by the complex interaction of size and sexual dimorphism both at the inter- and intraspecific levels. However, while in cranial shape both species had divergent shape allometries and parallel interspecific sexual allometries, the opposite was true for mandible shape.Differences in mandible shape between European and American mink were summarized by PC1 (Fig. 2, Fig. S1) and can be mainly related to muscle size and jaw biomechanics (i.e., in-levers and out-levers). The relatively taller and slightly wider coronoid process of European minks suggests a relatively larger temporalis muscle, while the anteriorly expanded masseteric fossa of American mink is indicative of a relatively larger masseter complex17,22,25. The relatively enlarged angular process of European mink provides a larger attachment area for the superficial masseter, with both mink species having a distinctive fossa on the lateral side of the angular process where this muscle attaches. This angular fossa is not present in European polecats (Gálvez-López, pers. obs.), part of the sister clade to European mink41.Regarding jaw biomechanics, the particular morphology of the American mink illustrates the compromise between maximizing both bite force efficiency and increased gape. The MAs for all masticatory muscles were higher in European mink due to their relatively longer in-levers (and also shorter out-levers if measured on PC1 configurations), with the exception of the MA of the deep masseter which was considerably higher in American mink (Table S2; Fig. 1D). These findings indicate that American mink exhibit features that allow them to produce larger forces at wide gape, which is particularly useful for holding and killing terrestrial vertebrates22,42. In agreement with this, a short moment arm of the superficial masseter (as observed in American mink) has been associated with increased gape in other mammals43. It is also worth noting that low MAs for the posterior temporalis and superficial masseter have also been associated with fish capture, as they indicate a relatively longer mandible relative to the muscle in-levers, which in turn allows the mouth to close faster when trying to catch elusive prey underwater21. In contrast, the characteristic features of European mink are indicative of stronger bites at the carnassials, which would allow them to cut through relatively tougher tissues and also to crush harder objects (e.g. shells of aquatic prey). Favoring carnassial over anterior bites could also be advantageous to feeding on fish. Mink catch fish underwater by grabbing them by the fins or back with their anterior teeth, and then dragging them to the surface where they are processed using cheek (carnassial) bites (Gálvez-López, pers. obs.).In our previous study on cranial shape in mink38, morphological differences between both species indicated relatively larger muscle volumes overall in the American mink (temporalis: more developed sagittal and nuchal crests, narrower braincase; masseter: longer and more curved zygomatic arches, larger infratemporal fossa), which suggested that bite forces both at the anterior dentition and at the carnassials were larger in this species. However, when combined with the MA results from this study on mandible shape, the relationship between muscle volume and force production becomes less straightforward. In the case of the European mink, the relatively smaller temporalis has a larger attachment site on the mandible (i.e., a broader and taller coronoid) and becomes more efficient (i.e., has higher MAs) due to the relatively longer in-lever. Similarly, in the American mink the effective length of the superficial masseter is increased by the marked curvature of the zygomatic arches, which mitigates the dorsal displacement of the angular process. However, the efficiency of the relatively larger temporalis is diminished by a smaller coronoid (i.e., reduced attachment area and shorter in-levers). The remaining differences in cranial morphology align with differences in mandible shape. Namely, the relatively broader zygomatic arches of the European mink support a strong superficial masseter, while the larger infratemporal fossae of American mink account for their enlarged deep masseter. On a final note, another finding common to both cranial and mandible shape was the relatively larger crushing dentition of American mink.Thus, after combining the results of cranial and mandible shape, it appears that, while the characteristic features of European mink indeed allow stronger carnassial bites, American mink present morphological indicators of both strong killing bites at wide gapes and powerful carnassial bites with a marked crushing component.The allometric effect on mandible size common to both species was represented by PC2 (Fig. 2, Fig. S3), which complements the common allometric trend recovered for both mink species in cranial shape38. The relative expansion of the masseteric fossa and the angular process with increasing size suggests that larger mink present a larger masseter complex. However, most of the allometric shape changes are related to muscle in-levers and out-levers. With increasing size, the length of both the out-lever at the anterior teeth and the in-levers of its related muscles (anterior temporalis, deep masseter) increases (Table S2), but the in-levers scale faster than the out-lever (Table S2). Thus, the mechanical advantages of both muscles at the anterior teeth also increase with size (Table S2), indicating that larger mink have markedly stronger and more efficient killing bites (particularly true for the deep masseter, which also becomes larger with size). This, together with their relatively larger anterior dentition (both in the mandible and the cranium) and taller anterior corpus, can be related to feeding on larger prey as size increases (i.e., stronger bites to perforate tougher skulls and hold onto stronger struggling prey, which would also require more robust teeth and corpora to resist the stresses placed on them). Similar features have been described for felids18, which also kill prey in this way22,32.Note, however, that one of the shape changes along PC2 does not accurately reflect the common allometric pattern: the lever arm of the superficial masseter, which slightly decreases along PC2 (Fig. 2; Table S2) and results in a decrease of the mechanical advantage of the superficial masseter and hence bite force at the carnassials along this axis (Table S2). In contrast, this lever arm significantly increases with size in the original specimens (Table S2), in agreement with the common allometric trend in cranial shape suggesting stronger bites at all teeth with increasing size38. A likely explanation for this phenomenon is that the common allometric trend is being confounded with interspecific shape differences, as American mink have significantly shorter superficial masseter in-levers than European mink (Fig. 1F; Table S2) yet their males are significantly larger than all other specimens (Fig. 1A). As mentioned above, the relative decrease in MA might reflect the trade-off between producing strong bite forces at the anterior teeth and having a wider gape to capture larger prey43, both of which are heavily supported by other morphological features in this common allometric trend.Sexual dimorphism in mandible shape was significant both within each species, and when grouping sexes from both species together. In her study of Palearctic mustelids, Romaniuk28 also found evidence for interspecific sexual dimorphism in mandible shape, but within species it was only significant for the Siberian weasel (Mustela sibirica). The different results for the European mink in that study might be related to its smaller sample. Note, however, that Hernández-Romero et al.40 did not find evidence for sexual dimorphism in mandible shape within Neotropical otters (Lontra longicaudis) even though their sample sizes were equivalent to those in the present study.Overall, the results of the present study reveal that mandible shape differences between males and females are the consequence of a complex interaction between sex and size at both inter- and intraspecific levels. For instance, each sex in each species has a mandible shape significantly different from each other (Table 1), but allometric shape changes within each of them are similar (except maybe female American mink; Fig. S5A). Additionally, while trajectory analysis indicates that the degree of sexual dimorphism in mandible shape is similar within each species, the specific differences between sexes are different in each species (i.e., same magnitude, different orientation; Table 2, Fig. S5B). While at the interspecific level, male and female mandible shapes change differently with increasing size even though the change per unit size is similar in both sexes (Tables 1, 2; Fig. S5C,D), and some of the allometric changes are common to both species and sexes (see section above; PC2 in Fig. 2). Finally, another set of shape changes related to sexual dimorphism and common to both species are those related to sexual dimorphism in mandible size, illustrated by PC3 (Figs. 2, Fig. S4).Shape changes related to sexual dimorphism in size are represented along PC3 and can be related to an overall increase in bite force (i.e., at all teeth), as higher scores on this axis correspond to increased muscle attachment areas and longer in-levers (taller and wider coronoid, anteriorly expanded masseteric fossa, ventrally expanded angular process), shorter out-levers (particularly at the anterior teeth), and a more robust corpus (dorsoventrally and mediolaterally expanded). This interpretation of shape changes along PC3 is supported by the results of the ANOVAs on the lever arms and MAs measured on the PC3 configurations (Table S2). These variables were only related to sex and size, with female mink having longer out-levers and male mink presenting longer in-levers and higher MAs, while out-levers decreased with increasing size and in-levers and MAs increased in both sexes (no significant interaction between sex and size indicates parallel allometric trajectories in both sexes). This trend is consistent with the common sexual allometry described for cranial shape, which suggested that larger males have bigger masticatory muscles than smaller females and thus produce higher bite forces38. Additionally, even though the relative length of the toothrow decreases, the size of the canine markedly increases and there is no change in molar size or the relative proportions in its shearing and crushing regions. Although this might be interpreted as reinforcing the canines to cope with killing larger prey while maintaining an otherwise similar dietary regime20, it is worth noting that larger canines have been long described as a feature of sexual size dimorphism in mustelids19,44,45.In terms of interspecific differences in sexual allometry, with increasing size the following shape changes were observed in females but not in males (Fig. S5C): a dorsoventrally more robust corpus, a ventral expansion of the angular process, longer in-levers for all masticatory muscles, larger incisors, and an increase in the shearing portion of m1 relative to the crushing portion. Most of these shape changes are similar to those described for PC3, which suggests that the female interspecific allometry bridges the bite force gap caused by sexual dimorphism in size. The changes to the female dentition suggest a shift in diet from crushing tough food items (e.g. aquatic invertebrates) towards slicing meat, which makes sense since these changes occur simultaneously with the common allometric trend (related to improved capabilities for killing larger vertebrate prey). However, as noted earlier, the increased shearing component is also advantageous for a piscivorous diet. Shape changes in male mandibles not observed in females seem to emphasize the common allometric trend (i.e., stronger killing bite at larger gapes) (Fig. S5D): a wider coronoid process for more muscle attachment, a dorsally displaced angular process to allow wider gapes, and mediolateral expansion of the corpus to increase its strength. Regarding their dentition, the opposite trend to females was observed (i.e., slightly smaller anterior teeth and a longer crushing molar portion), suggesting a larger durophagous component in the diet of larger males.As expected, variation in mandible shape could be linked to potential dietary differences between European and American mink, and also between sexes. In summary, the results of the present study show that:

American mink are better equipped for preying on terrestrial vertebrates, as they can achieve relatively larger gapes and their mandibles are able to produce larger forces during the killing bite (i.e., at the anterior teeth and with an open mouth).

European mink, on the other hand, can produce relatively stronger bites at the carnassials, suggesting that they rely more on tougher prey and/or fish.

Regardless of species and sex, morphological features in larger mink demonstrate increased capabilities for feeding on larger terrestrial prey (stronger killing bites and more robust anterior teeth and corpora to resist the stresses caused by struggling prey).

Due to their larger size, male mink of both species have stronger bites than females at both the anterior teeth and the carnassials. However, with increasing size, females bridge the gap by developing relatively stronger bites overall while shifting their diet from tougher or harder prey (probably aquatic invertebrates) towards less mechanically demanding food items (e.g. terrestrial vertebrates and/or fish). In contrast, increasing size in males leads to even more specialization towards feeding on larger terrestrial prey while tough items become more relevant in their diets (probably crushing bones of small prey).

These findings confirm our original predictions based on previous results on cranial shape differences, but do they agree with observed dietary preferences in minks? Diet studies in American mink are numerous, and provide a wide picture of seasonal and regional variation8,11 as well as intraspecific dietary competition6,7,12. However, studies on European mink diet are scarcer9,14, particularly those comparing the sexes13. Additionally, a few studies have compared diets of sympatric European and American mink10,15. All these studies can be summarized as: A, male American mink favor medium-sized mammals and birds usually heavier than themselves; B, female American mink favor aquatic prey, but are displaced towards small mammals and birds when seasonal changes in prey availability shift the males’ diet towards aquatic prey; C, European mink favor aquatic prey, particularly fish and crayfish; but D, they are displaced towards amphibians and small mammals when sympatric with American mink. From these, our results on mandible shape variation support A and somewhat B and C, but provide no information on the interspecific competition scenario or on potential seasonal or local dietary differences. Additionally, there is no information on size-related dietary changes in either species that could validate our findings on sexual allometry in mandible shape. Thus, while mandible shape is very useful for identifying broad dietary indicators even between highly similar species, its ability to provide accurate information on their potential prey is limited.As a final note on mink diets, our previous study on cranial shape38, suggested a gradient in muscle force (and potential dietary range) from female European mink to male American mink. Based on those results and studies on social interactions between and within species35,46, we hypothesized that competition between both mink species could be displacing female European mink towards narrower and poorer diets, which could affect their survivability and ability to successfully reproduce. Fortunately, the results of the present study not only propose that there might be less overlap in diets between species and sexes than suggested by dietary studies7,10,13,15, but also indicate that dietary competition seems to be higher for small terrestrial vertebrates, not aquatic prey (on which female European mink are particularly well equipped to feed). More

Barton, N. Evolutionary biology. The geometry of adaptation. Nature 395, 751–752. https://doi.org/10.1038/27338 (1998).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Otto, S. P. & Lenormand, T. Resolving the paradox of sex and recombination. Nat. Rev. Genet. 3, 252–261. https://doi.org/10.1038/nrg761 (2002).CAS 
Article 
PubMed 

Google Scholar 
Becks, L. & Agrawal, A. F. Higher rates of sex evolve in spatially heterogeneous environments. Nature 468, 89–92. https://doi.org/10.1038/nature09449 (2010).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83. https://doi.org/10.1126/science.aan8048 (2018).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Thompson, D. M. & van Woesik, R. Corals escape bleaching in regions that recently and historically experienced frequent thermal stress. Proc. Biol. Sci. 276, 2893–2901. https://doi.org/10.1098/rspb.2009.0591 (2009).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422. https://doi.org/10.1126/science.1204794 (2011).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264. https://doi.org/10.1038/s41467-019-09238-2 (2019).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Yund, P. O. How severe is sperm limitation in natural populations of marine free-spawners?. Trends Ecol. Evol. 15, 10–13 (2000).CAS 
Article 

Google Scholar 
Levitan, D. R. & Petersen, C. Sperm limitation in the sea. Trend Ecol. Evol. 10, 228–231 (1995).CAS 
Article 

Google Scholar 
Baird, A., Guest, J. & Willis, B. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu. Rev. Ecol. Evol. Syst. 40, 551–571. https://doi.org/10.1146/Annurev.Ecolsys.110308.120220 (2009).Article 

Google Scholar 
Wei, N. V. et al. Reproductive isolation among Acropora species (Scleractinia: Acroporidae) in a marginal coral assemblage. Zool. Stud. 51, 85–92 (2012).
Google Scholar 
Kitanobo, S., Isomura, N., Fukami, H., Iwao, K. & Morita, M. The reef-building coral Acropora conditionally hybridize under sperm limitation. Biol. Lett. 12, 20160511. https://doi.org/10.1098/rsbl.2016.0511 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Mercier, A. & Hamel, J.-F. Synchronized breeding events in sympatric marine invertebrates: Role of behavior and fine temporal windows in maintaining reproductive isolation. Behav. Ecol. Sociobiol. 64, 1749–1765 (2010).Article 

Google Scholar 
Levitan, D. R. et al. Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58, 308–323 (2004).Article 

Google Scholar 
Willis, B. L., Babcock, R. C., Harrison, P. L. & Wallace, C. C. Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16, S53–S65 (1997).Article 

Google Scholar 
Nozawa, Y., Isomura, N. & Fukami, H. Influence of sperm dilution and gamete contact time on the fertilization rate of scleractinian corals. Coral Reefs 34, 1199–1206. https://doi.org/10.1007/s00338-015-1338-3 (2015).ADS 
Article 

Google Scholar 
Oliver, J. & Babcock, R. Aspects of the fertilization ecology of broadcast spawning corals: Sperm dilution effects and in situ measurements of fertilization. Biol. Bull. 183, 409–417. https://doi.org/10.2307/1542017 (1992).CAS 
Article 
PubMed 

Google Scholar 
Coma, R. & Lasker, H. R. Small-scale heterogeneity of fertilization success in a broadcast spawning octocoral. J. Exp. Mar. Biol. Ecol. 214, 107–120. https://doi.org/10.1016/S0022-0981(97)00017-8 (1997).Article 

Google Scholar 
Teo, A. & Todd, P. A. Simulating the effects of colony density and intercolonial distance on fertilisation success in broadcast spawning scleractinian corals. Coral Reefs 37, 891–900. https://doi.org/10.1007/s00338-018-1715-9 (2018).ADS 
Article 

Google Scholar 
Marshall, D. J. In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate. Mar. Ecol. Prog. Ser. 236, 113–119 (2002).ADS 
Article 

Google Scholar 
Babcock, R. C., Mundy, C. N. & Whitehead, D. Sperm diffusion-models and in-situ confirmation of long-distance fertilization in the free-spawning asteroid Acanthaster planci. Biol. Bull. 186, 17–28 (1994).CAS 
Article 

Google Scholar 
Omori, M., Fukami, H., Kobinata, H. & Hatta, M. Significant drop of fertilization of Acropora corals in 1999. An after-effect of heavy coral bleaching?. Limnol. Oceanogr. 46, 704–706. https://doi.org/10.4319/lo.2001.46.3.0704 (2001).ADS 
Article 

Google Scholar 
Levitan, D. R., Fogarty, N. D., Jara, J., Lotterhos, K. E. & Knowlton, N. Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65, 1254–1270. https://doi.org/10.1111/j.1558-5646.2011.01235.x (2011).Article 
PubMed 

Google Scholar 
Fukami, H., Omori, M., Shimoike, K., Hayashibara, T. & Hatta, M. Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals. Mar. Biol. 142, 679–684. https://doi.org/10.1007/S00227-002-1001-8 (2003).Article 

Google Scholar 
Morita, M. et al. Reproductive strategies in the intercrossing corals Acropora donei and A. tenuis to prevent hybridization. Coral Reefs 38, 1211–1223. https://doi.org/10.1007/s00338-019-01839-z (2019).ADS 
Article 

Google Scholar 
Shinzato, C. et al. Development of novel, cross-species microsatellite markers for Acropora corals using next-generation sequencing technology. Front. Mar. Sci. 1, 11 (2014).Article 

Google Scholar 
R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020).Albright, R. & Mason, B. Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLoS One 8, e56468. https://doi.org/10.1371/journal.pone.0056468 (2013).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Iguchi, A., Morita, M., Nakajima, Y., Nishikawa, A. & Miller, D. In vitro fertilization efficiency in coral Acropora digitifera. Zygote 17, 225–227. https://doi.org/10.1017/S096719940900519X (2009).Article 
PubMed 

Google Scholar 
Morita, M. et al. Eggs regulate sperm flagellar motility initiation, chemotaxis and inhibition in the coral Acropora digitifera, A. gemmifera and A. tenuis. J. Exp. Biol. 209, 4574–4579. https://doi.org/10.1242/jeb.02500 (2006).CAS 
Article 
PubMed 

Google Scholar 
Chan, W. Y., Hoffmann, A. A. & van Oppen, M. J. H. Hybridization as a conservation management tool. Conserv. Lett. https://doi.org/10.1111/conl.12652 (2019).Article 

Google Scholar  More

Lees, A. C., Attwood, S., Barlow, J. & Phalan, B. Biodiversity scientists must fight the creeping rise of extinction denial. Nat. Ecol. Evol. 4, 1440–1443 (2020).PubMed 

Google Scholar 
Díaz, S. et al. Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366, eaax3100 (2019).
Google Scholar 
Driscoll, D. A. et al. A biodiversity-crisis hierarchy to evaluate and refine conservation indicators. Nat. Ecol. Evol. 2, 775–781 (2018).PubMed 

Google Scholar 
Jackson, J. B. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).CAS 
PubMed 

Google Scholar 
McCauley, D. J. et al. Marine defaunation: Animal loss in the global ocean. Science 347, 6219 (2015).
Google Scholar 
Sala, E. & Knowlton, N. Global marine biodiversity trends. Annu. Rev. Environ. Resour. 31, 93–122 (2006).
Google Scholar 
Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Beaumont, N. et al. Identification, definition and quantification of goods and services provided by marine biodiversity: Implications for the ecosystem approach. Mar. Pollut. Bull. 54, 253–265 (2007).CAS 
PubMed 

Google Scholar 
Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).
Google Scholar 
Turpie, J. K. The existence value of biodiversity in South Africa: How interest, experience, knowledge, income and perceived level of threat influence local willingness to pay. Ecol. Econ. 46, 199–216 (2003).
Google Scholar 
Ruiz-Frau, A., Hinz, H., Edwards-Jones, G. & Kaiser, M. Spatially explicit economic assessment of cultural ecosystem services: Non-extractive recreational uses of the coastal environment related to marine biodiversity. Mar. Policy 38, 90–98 (2013).
Google Scholar 
Thrush, S. F., Gray, J. S., Hewitt, J. E. & Ugland, K. I. Predicting the effects of habitat homogenization on marine biodiversity. Ecol. Appl. 16, 1636–1642 (2006).PubMed 

Google Scholar 
Gillies, C. L. et al. Australian shellfish ecosystems: Past distribution, current status and future direction. PLoS ONE 13, e0190914 (2018).PubMed 
PubMed Central 

Google Scholar 
Commito, J. A., Como, S., Grupe, B. M. & Dow, W. E. Species diversity in the soft-bottom intertidal zone: Biogenic structure, sediment, and macrofauna across mussel bed spatial scales. J. Exp. Mar. Biol. Ecol. 366, 70–81 (2008).
Google Scholar 
Tokeshi, M. Species Coexistence: Ecological and Evolutionary Perspectives (Wiley, Hoboken, 2009).
Google Scholar 
Paul, L. J. A history of the Firth of Thames dredge fishrey for mussels: Use and abuse of a coastal resource. Report No. 94, (Wellington, New Zealand, 2012).Enderlein, P. & Wahl, M. Dominance of blue mussels versus consumer-mediated enhancement of benthic diversity. J. Sea Res. 51, 145–155 (2004).ADS 

Google Scholar 
Lejart, M. & Hily, C. Differential response of benthic macrofauna to the formation of novel oyster reefs (Crassostrea gigas, Thunberg) on soft and rocky substrate in the intertidal of the Bay of Brest, France. J. Sea Res. 65, 84–93 (2011).ADS 

Google Scholar 
Norling, P. & Kautsky, N. Patches of the mussel Mytilus sp. are islands of high biodiversity in subtidal sediment habitats in the Baltic Sea. Aquat. Biol. 4, 75–87 (2008).
Google Scholar 
Norling, P., Lindegarth, M., Lindegarth, S. & Strand, Å. Effects of live and post-mortem shell structures of invasive Pacific oysters and native blue mussels on macrofauna and fish. Mar. Ecol. Prog. Ser. 518, 123–138 (2015).ADS 

Google Scholar 
McLeod, I., Parsons, D., Morrison, M., Van Dijken, S. & Taylor, R. Mussel reefs on soft sediments: A severely reduced but important habitat for macroinvertebrates and fishes in New Zealand. N. Z. J. Mar. Freshw. Res. 48, 48–59 (2014).CAS 

Google Scholar 
Seitz, R. D., Wennhage, H., Bergström, U., Lipcius, R. N. & Ysebaert, T. Ecological value of coastal habitats for commercially and ecologically important species. ICES J. Mar. Sci. 71, 648–665 (2014).
Google Scholar 
zu Ermgassen, P. S., Grabowski, J. H., Gair, J. R. & Powers, S. P. Quantifying fish and mobile invertebrate production from a threatened nursery habitat. J. Appl. Ecol. 53, 596–606 (2016).
Google Scholar 
Grabowski, J. H. The influence of trophic interactions, habitat complexity, and landscape setting on community dynamics and restoration of oyster reefs. Ph.D., The University of North Carolina at Chapel Hill (2002).Harding, J. M., Allen, D. M., Haffey, E. R. & Hoffman, K. M. Site fidelity of oyster reef blennies and gobies in saltmarsh tidal creeks. Estuaries Coasts 43, 409–423 (2020).CAS 

Google Scholar 
Parsons, D. et al. Snapper (Chrysophrys auratus): A review of life history and key vulnerabilities in New Zealand. N. Z. J. Mar. Freshw. Res. 48, 256–283 (2014).
Google Scholar 
Callier, M. D., Richard, M., McKindsey, C. W., Archambault, P. & Desrosiers, G. Responses of benthic macrofauna and biogeochemical fluxes to various levels of mussel biodeposition: An in situ “benthocosm” experiment. Mar. Pollut. Bull. 58, 1544–1553. https://doi.org/10.1016/j.marpolbul.2009.05.010 (2009).CAS 
Article 
PubMed 

Google Scholar 
Ysebaert, T., Hart, M. & Herman, P. M. Impacts of bottom and suspended cultures of mussels Mytilus spp. on the surrounding sedimentary environment and macrobenthic biodiversity. Helgol. Mar. Res. 63, 59–74 (2009).ADS 

Google Scholar 
Sea, M. A., Thrush, S. F. & Hillman, J. R. Environmental predictors of sediment denitrification rates within restored green-lipped mussel (Perna canaliculus) beds. Mar. Ecol. Prog. Ser. 667, 1–13 (2021).ADS 
CAS 

Google Scholar 
Hillman, J. R., O’Meara, T. A., Lohrer, A. M., & Thrush, S. F. Influence of restored mussel reefs on denitrification in
marine sediments. J. Sea Res. 175, 102099 (2021).
Google Scholar 
Bacheler, N. M. et al. Comparison of trap and underwater video gears for indexing reef fish presence and abundance in the southeast United States. Fish. Res. 143, 81–88 (2013).
Google Scholar 
Wells, R. D., Boswell, K. M., Cowan, J. H. Jr. & Patterson, W. F. III. Size selectivity of sampling gears targeting red snapper in the northern Gulf of Mexico. Fish. Res. 89, 294–299 (2008).
Google Scholar 
Emslie, M. J., Cheal, A. J., MacNeil, M. A., Miller, I. R. & Sweatman, H. P. Reef fish communities are spooked by scuba surveys and may take hours to recover. PeerJ 6, e4886 (2018).PubMed 
PubMed Central 

Google Scholar 
Piggott, C. V., Depczynski, M., Gagliano, M. & Langlois, T. J. Remote video methods for studying juvenile fish populations in challenging environments. J. Exp. Mar. Biol. Ecol. 532, 151454 (2020).
Google Scholar 
Dean, W. E. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: Comparison with other methods. J. Sediment. Res. 44, 242–248 (1974).CAS 

Google Scholar 
Lorenzen, C. J. Determination of chlorophyll and pheo-pigments: Spectrophotometric equations. Limnol. Oceanogr. 12, 343–346 (1967).ADS 
CAS 

Google Scholar 
Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
Google Scholar 
McArdle, B. H. & Anderson, M. J. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82, 290–297 (2001).
Google Scholar 
Clarke, K. R. & Gorley, R. N. PRIMER v7: User Manual/Tutorial (2015).Anderson, M. J., Gorley, R. N. & Clarke, K. R. PERMANOVA+ for PRIMER: Guide to software and statistical methods (2008).R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2021).Saier, B. Subtidal and intertidal mussel beds (Mytilus edulis L.) in the Wadden Sea: Diversity differences of associated epifauna. Helgol. Mar. Res. 56, 44–50 (2002).ADS 

Google Scholar 
Peterson, C. H., Grabowski, J. H. & Powers, S. P. Estimated enhancement of fish production resulting from restoring oyster reef habitat: Quantitative valuation. Mar. Ecol. Prog. Ser. 264, 249–264 (2003).ADS 

Google Scholar 
Gutiérrez, J. L., Jones, C. G., Strayer, D. L. & Iribarne, O. O. Mollusks as ecosystem engineers: The role of shell production in aquatic habitats. Oikos 101, 79–90 (2003).
Google Scholar 
Norkko, A., Hewitt, J. E., Thrush, S. F. & Funnell, T. Benthic-pelagic coupling and suspension-feeding bivalves: Linking site-specific sediment flux and biodeposition to benthic community structure. Limnol. Oceanogr. 46, 2067–2072 (2001).ADS 

Google Scholar 
Russell, B. The food and feeding habits of rocky reef fish of north-eastern New Zealand. N. Z. J. Mar. Freshw. Res. 17, 121–145 (1983).
Google Scholar 
Gillies, C., Creighton, C. & McLeod, I. Shellfish reef habitats: A synopsis to underpin the repair and conservation of Australia’s environmentally, socially and economically important bays and estuaries. Report to the National Environmental Science Programme, Marine Biodiversity Hub, Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER) Publication, James Cook University, Townsville, Qld, Australia (2015).Lenihan, H. S. et al. Cascading of habitat degradation: Oyster reefs invaded by refugee fishes escaping stress. Ecol. Appl. 11, 764–782 (2001).
Google Scholar 
Connell, S. & Jones, G. The influence of habitat complexity on postrecruitment processes in a temperate reef fish population. J. Exp. Mar. Biol. Ecol. 151, 271–294 (1991).
Google Scholar 
Usmar, N. Ontogeny and Ecology of Snapper (Pagrus auratus) in an estuary, the Mahurangi Harbour (University of Auckland, 2009).
Google Scholar 
Willis, T. J. & Anderson, M. J. Structure of cryptic reef fish assemblages: Relationships with habitat characteristics and predator density. Mar. Ecol. Prog. Ser. 257, 209–221 (2003).ADS 

Google Scholar 
Thompson, S. Homing in a territorial reef fish. Copeia 1983, 832–834 (1983).
Google Scholar 
Thrush, S. F., Schultz, D., Hewitt, J. E. & Talley, D. Habitat structure in soft-sediment environments and abundance of juvenile snapper Pagrus auratus. Mar. Ecol. Prog. Ser. 245, 273–280 (2002).ADS 

Google Scholar 
Pickering, H. & Whitmarsh, D. Artificial reefs and fisheries exploitation: A review of the ‘attraction versus production’debate, the influence of design and its significance for policy. Fish. Res. 31, 39–59 (1997).
Google Scholar 
Karp, M. A., Seitz, R. D. & Fabrizio, M. C. Faunal communities on restored oyster reefs: Effects of habitat complexity and environmental conditions. Mar. Ecol. Prog. Ser. 590, 35–51 (2018).ADS 

Google Scholar 
Hanke, M. H., Posey, M. H. & Alphin, T. D. The effects of intertidal oyster reef habitat characteristics on faunal utilization. Mar. Ecol. Prog. Ser. 581, 57–70 (2017).ADS 

Google Scholar 
Cranfield, H., Rowden, A., Smith, D., Gordon, D. & Michael, K. Macrofaunal assemblages of benthic habitat of different complexity and the proposition of a model of biogenic reef habitat regeneration in Foveaux Strait, New Zealand. J. Sea Res. 52, 109–125 (2004).ADS 

Google Scholar 
Norling, P. & Kautsky, N. Structural and functional effects of Mytilus edulis on diversity of associated species and ecosystem functioning. Mar. Ecol. Prog. Ser. 351, 163–175 (2007).ADS 

Google Scholar 
Jaunatre, R. et al. New synthetic indicators to assess community resilience and restoration success. Ecol. Indicators 29, 468–477 (2013).
Google Scholar 
O’Meara, T. A., Hewitt, J. E., Thrush, S. F., Douglas, E. J. & Lohrer, A. M. Denitrification and the role of macrofauna across estuarine gradients in nutrient and sediment loading. Estuaries Coasts 43, 1394–1405. https://doi.org/10.1007/s12237-020-00728-x (2020).CAS 
Article 

Google Scholar 
McCann, L. D. Oligochaete influence on settlement, growth and reproduction in a surface-deposit-feeding polychaete. J. Exp. Mar. Biol. Ecol. 131, 233–253 (1989).
Google Scholar 
Hope, J. A., Paterson, D. M. & Thrush, S. F. The role of microphytobenthos in soft-sediment ecological networks and their contribution to the delivery of multiple ecosystem services. J. Ecol. 108, 815–830 (2020).
Google Scholar 
Christianen, M. J. et al. Benthic primary producers are key to sustain the Wadden Sea food web: Stable carbon isotope analysis at landscape scale. Ecology 98, 1498–1512 (2017).CAS 
PubMed 

Google Scholar 
Commito, J. A. & Dankers, N. M. Dynamics of spatial and temporal complexity in European and North American soft-bottom mussel beds. In Ecological Comparisons of Sedimentary Shores, 39–59 (Springer, Berlin, 2001).Arribas, L. P., Donnarumma, L., Palomo, M. G. & Scrosati, R. A. Intertidal mussels as ecosystem engineers: Their associated invertebrate biodiversity under contrasting wave exposures. Mar. Biodivers. 44, 203–211 (2014).
Google Scholar 
Walles, B., Salvador de Paiva, J., van Prooijen, B. C., Ysebaert, T. & Smaal, A. C. The ecosystem engineer Crassostrea gigas affects tidal flat morphology beyond the boundary of their reef structures. Estuaries Coasts 38, 941–950 (2015).
Google Scholar 
Tsuchiya, M. & Nishihira, M. Islands of Mytilus edulis as a habitat for small intertidal animals: Effect of Mytilus age structure on the species composition of the associated fauna and community organization. Mar. Ecol. Prog. Ser. 31, 171–178 (1986).ADS 

Google Scholar 
Craeymeersch, J. A. & Jansen, H. M. Bivalve assemblages as hotspots for biodiversity. In Goods and Services of Marine Bivalves, 275–294 (Springer, Cham, 2019).Buschbaum, C. et al. Mytilid mussels: Global habitat engineers in coastal sediments. Helgol. Mar. Res. 63, 47–58 (2009).ADS 

Google Scholar  More

Alerstam, T., Hedenström, A. & Åkesson, S. Long‐distance migration: evolution and determinants. Oikos 103, 247–260 (2003).Article 

Google Scholar 
Newton, I. The migration ecology of birds (Elsevier, London, 2008).Putman, N. F. et al. An inherited magnetic map guides ocean navigation in juvenile Pacific salmon. Curr. Biol. 24, 446–450 (2014).CAS 
Article 

Google Scholar 
Jesmer, B. R. et al. Is ungulate migration culturally transmitted? Evidence of social learning from translocated animals. Science 361, 1023–1025 (2018).ADS 
CAS 
Article 

Google Scholar 
Milner-Gulland, E. J., Fryxell, J. M. & Sinclair, A. R. (Eds.) Animal migration: a synthesis (Oxford University Press, New York, 2011).Conradt, L. & Roper, T. J. Consensus decision making in animals. Trends Ecol. Evol. 20, 449–456 (2005).Article 

Google Scholar 
Couzin, I. D., Krause, J., Franks, N. R. & Levin, S. A. Effective leadership and decision-making in animal groups on the move. Nature 433, 513–516 (2005).ADS 
CAS 
Article 

Google Scholar 
Vansteelant, W. M. G., Kekkonen, J. & Byholm, P. Wind conditions and geography shape the first outbound migration of juvenile honey buzzards and their distribution across sub-Saharan Africa. Proc. R. Soc. B 284, 20170387 (2017).Article 

Google Scholar 
Flack, A., Nagy, M., Fiedler, W., Couzin, I. D. & Wikelski, M. From local collective behavior to global migratory patterns in white storks. Science 360, 911–914 (2018).ADS 
CAS 
Article 

Google Scholar 
Chernetsov, N., Berthold, P. & Querner, U. Migratory orientation of first-year white storks (Ciconia ciconia): inherited information and social interactions. J. Exp. Biol. 207, 937–943 (2004).Article 

Google Scholar 
Mueller, T., O’Hara, R. B., Converse, S. J., Urbanek, R. P. & Fagan, W. F. Social learning of migratory performance. Science 341, 999–1002 (2013).ADS 
CAS 
Article 

Google Scholar 
Whiten, A. Cultural evolution in animals. Annu. Rev. Ecol. Evol. Syst. 50, 27–48 (2019).Article 

Google Scholar 
Whitehead, H. & Rendell, L. The Cultural Lives of Whales and Dolphins (Chicago University Press, Chicago, 2015).Franks, N. R. & Richardson, T. Teaching in tandem-running ants. Nature 439, 153–153 (2006).ADS 
CAS 
Article 

Google Scholar 
Thornton, A. & McAuliffe, K. Teaching in wild meerkats. Science 313, 227–229 (2006).ADS 
CAS 
Article 

Google Scholar 
Cramp, S. (Ed.) The birds of the Western Palearctic. Vol. IV. Terns to woodpeckers (Oxford University Press, New York, 1985).Méndez, V. et al. Paternal effects in the initiation of migratory behaviour in birds. Sci. Rep. 11, 2782 (2021).ADS 
Article 

Google Scholar 
Olson, V. A., Liker, A., Freckleton, R. P. & Székely, T. Parental conflict in birds: comparative analyses of offspring development, ecology and mating opportunities. Proc. R. Soc. B 275, 301–307 (2008).CAS 
Article 

Google Scholar 
Ledwoń, M. & Neubauer, G. Offspring desertion and parental care in the Whiskered Tern Chlidonias hybrida. Ibis 159, 860–872 (2017).Article 

Google Scholar 
Arnqvist, G. & Rowe, L. Sexual conflict (Princeton University Press, New York, 2005).Goodenough, K. S. & Patton, R. T. Satellite telemetry reveals strong fidelity to migration routes and wintering grounds for the gull-billed tern (Gelochelidon nilotica). Waterbirds 42, 400–410 (2019).Article 

Google Scholar 
Gu, Z. et al. Climate-driven flyway changes and memory-based long-distance migration. Nature 591, 259–264 (2021).ADS 
CAS 
Article 

Google Scholar 
Baert, J. M. et al. Resource predictability drives interannual variation in migratory behavior in a long-lived bird. Behav. Ecol. arab132, https://doi.org/10.1093/beheco/arab132 (2021).Papageorgiou, D. & Farine, D. R. Group size and composition influence collective movement in a highly social terrestrial bird. eLife 9, e59902 (2020).CAS 
Article 

Google Scholar 
Caro, T. M. & Hauser, M. D. Is there teaching in nonhuman animals? Q. Rev. Biol. 67, 151–174 (1992).CAS 
Article 

Google Scholar 
Thornton, A. & Raihani, N. J. The evolution of teaching. Anim. Behav. 75, 1823–1836 (2008).Article 

Google Scholar 
Riedman, M. L. The evolution of alloparental care and adoption in mammals and birds. Q. Rev. Biol. 57, 405–435 (1982).Article 

Google Scholar 
Sheppard, C. E. et al. Decoupling of genetic and cultural inheritance in a wild mammal. Curr. Biol. 28, 1846–1850 (2018).CAS 
Article 

Google Scholar 
Åkesson, S. & Helm, B. Endogenous programs and flexibility in bird migration. Front. Ecol. Evol. 8, 1–20 (2020).Article 

Google Scholar 
Sasaki, T. & Biro, D. Cumulative culture can emerge from collective intelligence in animal groups. Nat. Commun. 8, 1–6 (2017).ADS 
Article 

Google Scholar 
Whiten, A., Ayala, F. J., Feldman, M. W. & Laland, K. N. The extension of biology through culture. Proc. Natl Acad. Sci. USA 114, 7775–7781 (2017).CAS 
Article 

Google Scholar 
Aplin, L. M. Culture and cultural evolution in birds: a review of the evidence. Anim. Behav. 147, 179–187 (2019).Article 

Google Scholar 
Laland, K. N., Toyokawa, W. & Oudman, T. Animal learning as a source of developmental bias. Evol. Dev. 22, 126–142 (2020).Article 

Google Scholar 
Sergio, F. et al. Individual improvements and selective mortality shape lifelong migratory performance. Nature 515, 410–413 (2014).ADS 
CAS 
Article 

Google Scholar 
Guttal, V. & Couzin, I. D. Social interactions, information use, and the evolution of collective migration. Proc. Natl Acad. Sci. USA 107, 16172–16177 (2010).ADS 
CAS 
Article 

Google Scholar 
Oudman, T. et al. Young birds switch but old birds lead: how barnacle geese adjust migratory habits to environmental change. Front. Ecol. Evol. 7, 106–120 (2020).Article 

Google Scholar 
Pearson, R. G. et al. Life history and spatial traits predict extinction risk due to climate change. Nat. Clim. Chang 4, 217–221 (2014).ADS 
Article 

Google Scholar 
Vickery, J. A. The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis 156, 1–22 (2014).Article 

Google Scholar 
Thaxter, C. B. et al. A trial of three harness attachment methods and their suitability for long-term use on Lesser Black-backed Gulls and Great Skuas. Ringing Migr. 29, 65–76 (2014).Article 

Google Scholar 
Byholm, P., Beal, M., Isaksson, N., Lötberg, U. & Åkesson, S. Data from: paternal transmission of migration knowledge in a long-distance bird migrant. Movebank Data Repos. https://doi.org/10.5441/001/1.352qf1cv (2022).Article 

Google Scholar 
R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, 2020). https://www.R-project.org/. More

Abell RA, Olsen DM, Dinerstein E, Hurley PT (2000) Freshwater ecoregions of North America: a conservation assessment. Island Press, Washington, DC
Google Scholar 
Adams NE, Inoue K, Seidel RA, Lang BK, Berg DJ (2018) Isolation drives increased diversification rates in freshwater amphipods. Mol Phylogenet Evol 127:746–757
Google Scholar 
Allendorf FW, Luikart GH, Aitken SN (2012) Conservation and the genetics of populations. John Wiley and Sons, West Sussex, UK
Google Scholar 
Ansah KN, Inoue K, Lang BK, Berg DJ (2014) Identification and characterization of 12 microsatellite loci for Physa in the Chihuahuan Desert. Conserv Genet Resour 6:769–771
Google Scholar 
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522
Google Scholar 
Bohonak A (1999) Dispersal, gene flow and population structure. Q Rev Biol 74:21–45CAS 

Google Scholar 
Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796
Google Scholar 
Bousfield EL (1958) Fresh-water amphipod crustaceans of glaciated North America. Can Field-Natural 72:55–113
Google Scholar 
Bousset L, Pointier JP, David P, Jarne P (2014) Neither variation loss, nor change in selfing rate is associated with worldwide invasion of Physa acuta from its native North America. Biol Invasions 16:1769–1783
Google Scholar 
Brune G (1981) Springs of Texas. Texas A and M University Press, Fort Worth, TX
Google Scholar 
Burridge CP, Craw D, Jack CD, King TM, Waters JM (2008) Does fish ecology predict dispersal across a river drainage divide? Evolution 62:1484–1499
Google Scholar 
Callens T, Galbusera P, Matthysen E, Durand EY, Githiru M, Huyghe JR, Lens L (2011) Genetic signature of population fragmentation varies with mobility in seven bird species of a fragmented Kenyan cloud forest. Mol Ecol 20:1829–1844
Google Scholar 
Cayuela H, Rougemont Q, Prunier JG, Moore J-S, Clobert J, Besnard A, Bernatchez L (2018) Demographic and genetic approaches to study dispersal in wild animal populations: a methodological review. Mol Ecol 27:3976–4010
Google Scholar 
Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol Ecol 12:2907–2918CAS 

Google Scholar 
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Biol Evol 24:621–631CAS 

Google Scholar 
Benton TG, Bowler DE (2012) Dispersal in invertebrates: influences on individual decisions. In: Clobert J, Baguette M, Benton TG, Bullock JM eds. Dispersal ecology and evolution. Oxford University PressCole GA (1981) Gammarus desperatus, a new species from New Mexico (Crustacea: Amphipoda). Hydrobiologia 76:27–32
Google Scholar 
Collas FPL, Koopman KR, Hendriks AJ, van der Velde G, Verbrugge LNH, Leuven RSEW (2014) Effects of desiccation on native and non-native molluscs in rivers. Freshw Biol 59:41–55
Google Scholar 
Dillon RT, Wethington AR, Rhett JM, Smith TP (2002) Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebr Biol 121:226–234
Google Scholar 
Diniz-Filho JAF, Soares TN, Lima JS, Dobrovolski R, Landeiro VL, Telles MPDC, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485PubMed Central 

Google Scholar 
Douglas ME, Douglas MR, Schuett GW, Porras LW (2006) Evolution of rattlesnakes (Viperidae: Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and Quaternary climate change. Mol Ecol 15:3353–3374CAS 

Google Scholar 
Duncan CJ (1975) Reproduction. In: Fretter V, Peake J eds. Pulmonates, vol. 1. Academic Press, New York, NYFaircloth BC (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8:92–94CAS 

Google Scholar 
Frankham R (2003) Genetics and conservation biology. Comptes Rendus Biol 326:S22–S29
Google Scholar 
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Google Scholar 
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Google Scholar 
Gervasio V, Berg DJ, Allan NL, Guttman SI (2004) Genetic diversity in the Gammarus pecos species complex: implications for conservation and regional biogeography in the Chihuahuan Desert. Limnol Oceanogr 49:520–531
Google Scholar 
Gómez-Rodriguez C, Miller KE, Castillejo J, Iglesias-Piñeiro, JI and Baselga A (2020) Disparate dispersal limitation in Geomalacus slugs unveiled by the shape and slope of the genetic-spatial distance relationship. Ecography: 43:1229–1240Gomez-Uchida D, Knight TW, Ruzzante DE (2009) Interaction of landscape and life history attributes on genetic diversity, neutral divergence, and gene flow in a pristine community of salmonids. Mol Ecol 18:4854–4869
Google Scholar 
Goudet J (1995) A computer program to calculate F-statistics. J Heredity 86:485–486
Google Scholar 
Guillot G, Rousset F (2013) Dismantling the Mantel tests. Methods Ecol Evol 4:336–344
Google Scholar 
Guzik MT, Cooper SJB, Humphreys WF, Austin AD (2009) Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in western Australia. Mol Ecol 18:3683–3698CAS 

Google Scholar 
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond Ser B: Biol Sci 351:1291–1298
Google Scholar 
Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2002) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482
Google Scholar 
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Google Scholar 
Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967CAS 
PubMed Central 

Google Scholar 
Harris PM, Roosa BR, Norment L (2002) Underground dispersal by amphipods (Crangonyx pseudogracilis) between temporary ponds. J Freshw Ecol 17:589–594
Google Scholar 
Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251
Google Scholar 
Hershler R (1994) A review of the North American freshwater snail genus Pyrgulopsis (Hydrobiidae). Smithson Contrib Zool 555:1–115Hershler R (1998) A systematic review of the hydrobiid snails (Gastropoda: Rissooidea) of the Great Basin, western United States. Part I. Genus Pyrgulopsis. Veliger 41:1–132Hershler R, Liu HP (2008) Ancient vicariance and recent dispersal of springsnails (Hydrobiidae: Pyrgulopsis) in the Death Valley System, California-Nevada. In: Hershler R, et al., eds. Late Cenozoic drainage history of the Southwestern Great Basin and Lower Colorado river region: geological and biotic perspectives. Geological Society of America Special Paper 439, Colorado, p 91–102Hickerson M, Cunningham CW (2005) Contrasting quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution 59:344–360
Google Scholar 
Holste DR, Inoue K, Lang BK, Berg DJ (2016) Identification of microsatellite loci and examination of endangered springsnails Juturnia kosteri and Pyrgulopsis roswellensis in the Chihuahuan Desert. Aquat Conserv: Mar Freshw Ecosyst 26:715–723
Google Scholar 
Hughes JM (2007) Constraints on recovery: using molecular methods to study connectivity of aquatic biota in rivers and streams. Freshw Biol 52:616–631
Google Scholar 
Huxel GR, Hastings A (1999) Habitat loss, fragmentation, and restoration. Restor Ecol 7:309–314
Google Scholar 
Jarne P, Charlesworth D (1993) The evolution of the selfing rate in functionally hermaphroditic plants and animals. Annu Rev Ecol Syst 24:441–466
Google Scholar 
Johnson WP, Butler MJ, Sanchez JI, Wadlington BE (2019) Development of monitoring techniques for endangered spring endemic invertebrates: an assessment of abundance. Nat Areas J 39:150–168
Google Scholar 
Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543CAS 

Google Scholar 
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Google Scholar 
Kodric-Brown A, Brown JH (2007) Native fishes, exotic mammals, and the conservation of desert springs. Front Ecol Environ 5:549–553
Google Scholar 
Land L (2005) Evaluation of groundwater residence time in a karstic aquifer using environmental tracers: Roswell Artesian Basin, New Mexico. In: Proceedings of the tenth multidisciplinary conference on sinkholes and the engineering and environmental impacts of Karst, San Antonio, Texas 2005. ASCE Geotechnical Special Publication, 144, 432–440.Land L, Newton BT (2007) Seasonal and long-term variations in hydraulic head in a karstic aquifer: Roswell Artesian Basin, New Mexico. New Mexico Bureau of Geology and Mineral Resources Open-File Report no. 503. New Mexico Bureau of Geology and Mineral Resources, Socorro
Google Scholar 
Land L, Newton BT (2008) Seasonal and long-term variations in hydraulic head in a karstic aquifer: Roswell Artesian Basin, New Mexico. J Am Water Resour Assoc 44:175–191
Google Scholar 
Lang BK (1998) Macroinvertebrate Population Monitoring at Bitter Lake National Wildlife Refuge, June 1995 to June 1998. New Mexico Department of Game and Fish. E-20-6 Performance Report.Lang BK (2005) Longitudinal distribution and abundance of the Alamosa springsnail, Pseudotryonia alamosae, in the Alamosa Creek drainage, Socorro County, New Mexico. Final report to the U.S. Fish and Wildlife Service. New Mexico Department of Game and Fish, Albuquerque, New Mexico. (Available from: New Mexico Department of Game and Fish, One Wildlife Way, Santa Fe, New Mexico 87507 USA.)Lefébure T, Douady CJ, Malard F, Gilbert J (2007) Testing dispersal and cryptic diversity in a widely distributed groundwater amphipod (Niphargus rhenorhodanensis). Mol Phylogenet Evol 42:676–686
Google Scholar 
Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844
Google Scholar 
Legendre P, Fortin M-J, Borcard D (2015) Should the Mantel test be used in spatial analysis? Methods Ecol Evolution 6:1239–1247
Google Scholar 
Lemer S, Planes S (2014) Effects of habitat fragmentation on the genetic structure and connectivity of the black-lipped pearl oyster Pinctada margaritifera populations in French Polynesia. Mar Biol 161:2035–2049
Google Scholar 
Lewis CA, Lester NP, Bradshaw AD, Fitzgibbon JE, Fuller K, Hakanson L, Richards C (1996) Considerations of scale in habitat conservation and restoration. Can J Fish Aquat Sci 53:440–445
Google Scholar 
Liu HP, Hershler R, Clift K (2003) Mitochondrial DNA sequences reveal extensive cryptic diversity within a western American springsnail. Mol Ecol 12:2771–2782CAS 

Google Scholar 
Lydeard C, Campbell D, Golz M (2016) Physa acuta Draparnaud, 1805 should be treated as a native of North America, not Europe. Malacologia 59:347–350
Google Scholar 
Marten A, Brändle M, Brandl R (2006) Habitat type predicts genetic population differentiation in freshwater invertebrates. Mol Ecol 15:2643–2651CAS 

Google Scholar 
Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983CAS 

Google Scholar 
Metcalf AL, Smartt RA (1997) Land snails of New Mexico. N Mex Mus Nat Hist Sci Bull 10:1–145
Google Scholar 
Mims MC, Phillipsen IC, Lytle DA, Hartfield-Kirk EE, Olden JD (2015) Ecological strategies predict associations between aquatic and genetic connectivity for dryland amphibians. Ecology 96:1371–1382
Google Scholar 
Monsutti A, Perrin N (1999) Dinucleotide microsatellite loci reveal a high selfing rate in the freshwater snail Physa acuta. Mol Ecol 8:1075–1092
Google Scholar 
Morningstar CR, Inoue K, Sei M, Lang BK, Berg DJ (2014) Quantifying morphological and genetic variation of sympatric populations to guide conservation of endangered micro-endemic springsnails. Aquat Conserv: Mar Freshw Ecosyst 24:536–545
Google Scholar 
Murphy NP, Adams M, Austin AD (2009) Independent colonization and extensive cryptic speciation of freshwater amphipods in the isolated groundwater springs of Australia’s Great Artesian Basin. Mol Ecol 18:109–122CAS 

Google Scholar 
Murphy NP, Guzik MT, Worthington-Wilmer J (2010) The influence of landscape on population structure of four invertebrates in groundwater springs. Freshw Biol 55:2499–2509
Google Scholar 
Murphy NP, Adams M, Guzik MT, Austin AD (2013) Extraordinary micro-endemism in Australian desert spring amphipods. Mol Phylogenet Evol 66:645–653CAS 

Google Scholar 
Murphy NP, King RA, Delean S (2015) Species, ESUs or populations? Delimiting and describing morphologically cryptic diversity in Australian desert spring amphipods. Invertebr Syst 29:457–467
Google Scholar 
Noel MS (1954) Animal ecology of a New Mexico springbrook. Hydrobiologia 6:120–135
Google Scholar 
Ochoa-Ochoa LM, Bezaury-Creel JE, Vazquez L-B, Flores-Villela O (2011) Choosing the survivors? A GIS-based triage support tool for micro-endemics: application to data for Mexican amphibians. Biol Conserv 144:2710–2718
Google Scholar 
Olson DM, Dinerstein E (1998) The Global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv Biol 12:502–515
Google Scholar 
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Google Scholar 
Phillipsen IC, Kirk EH, Bogan MT, Mims MC, Olden JD, Lytle DA (2015) Dispersal ability and habitat requirements determine landscape-level genetic patterns in desert aquatic insects. Mol Ecol 24:54–69
Google Scholar 
Phillipsen IC, Lytle DA (2012) Aquatic insects in a sea of desert: population genetic structure is shaped by limited dispersal in a naturally fragmented landscape. Ecography 36:731–743
Google Scholar 
Ponder WF, Colgan DJ (2002) What makes a narrow-range taxon? Insights from Australian freshwater snails. Invertebr Syst 16:571–82
Google Scholar 
Ponder WF, Colgan DJ, Clark SA, Miller AC, Terzis T (1994) Microgeographic, genetic and morphological differentiation of freshwater snails—the Hydrobiidae of Wilson’s Promontory, Victoria, South-eastern Australia. Aust J Zool 42:557–678
Google Scholar 
Ponder WF, Eggler P, Colgan DJ (1995) Genetic differentiation of aquatic snails (Gastropoda: Hydrobiidae) from artesian springs in arid Australia. Biol J Linn Soc 56:553–596
Google Scholar 
Ponder WF, Hershler R, Jenkins B (1989) An endemic radiation of hydrobiid snails from artesian springs in northern South Australia: their taxonomy, physiology, distribution and anatomy. Malacologia 31:1–140
Google Scholar 
Puechmaille SJ, Gouilh MA, Piyapan P, Yokubol M, Mie Mie K, Bates PJ, Satasook C, Nwe T, Hla Bu SS, Mackie IJ, Petit EJ, Teeling EC (2011) The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nat Commun 2:573
Google Scholar 
Rachalewski M, Banha F, Grabowski M, Anastácio PM (2013) Ectozoochory as a possible vector enhancing the spread of an alien amphipod Crangonyx pseudogracilis. Hydrobiologia 717:109–117
Google Scholar 
Ribera I, Vogler AP (2000) Habitat type as a determinant of species range sizes: the example of lotic-lentic differences in aquatic Coleoptera. Biol J Linn Soc 71:33–52
Google Scholar 
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Google Scholar 
Rice KJ, Emery NC (2003) Managing microevolution: restoration in the face of global change. Front Ecol Environ 1:469–478
Google Scholar 
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Google Scholar 
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S eds. Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, p 365–386Sada DW, Vinyard GL (2002) Anthropogenic changes in biogeography of Great Basin aquatic biota. Smithson Contrib Earth Sci 33:277–293
Google Scholar 
Seidel RA, Lang BK, Berg DJ (2009) Phylogeographic analysis reveals multiple cryptic species of amphipods (Crustacea: Amphipoda) in Chihuahuan Desert springs. Biol Conserv 142:2303–2313
Google Scholar 
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CAS 

Google Scholar 
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264CAS 
PubMed Central 

Google Scholar 
Stanislawczyk K, Walters AD, Haan TJ, Sei M, Lang BK, Berg DJ (2018) Variation among macroinvertebrate communities suggests the importance of conserving desert springs. Aquat Conserv: Mar Freshw Ecosyst 28:944–953
Google Scholar 
Taylor DW (1987) Fresh-water molluscs from New Mexico and vicinity. N Mex Bur Mines Miner Resour Bull 116:1–50Toro MA, Caballero A (2005) Characterization and conservation of genetic diversity in subdivided populations. Philos Trans R Soc B: Biol Sci 360:1367–1378CAS 

Google Scholar 
U.S. Fish and Wildlife Service (1998) Final comprehensive conservation plan and environmental assessment. Bitter Lake National Wildlife Refuge, U.S. Fish and Wildlife Service, Southwest Region, Albuquerque, New Mexico
Google Scholar 
U.S. Fish and Wildlife Service (2005) Endangered and threatened wildlife and plants; listing Roswell springsnail, Koster’s springsnail, Noel’s amphipod, and Pecos assiminea as endangered with critical habitat; final rule. Fed Register 70:46304–46333
Google Scholar 
U.S. Fish and Wildlife Service (2019) Recovery plan for four invertebrate species of the Pecos River valley: Noel’s amphipod (Gammarus desperatus), Koster’s springsnail (Juturnia kosteri), Roswell springsnail (Pyrgulopsis roswellensis), and Pecos assiminea (Assiminea pecos). Southwest Region, Albuquerque, New Mexicovan Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Google Scholar 
Walters AD, Cannizzaro AG, Trujillo DA, Berg DJ (2021) Addressing the Linnean shortfall in a cryptic species complex. Zool J Linn Soc 192:277–305Walters AD, Schwartz MK (2020) Population genomics and management of wild vertebrate populations. In: Hohenlohe P, Rajora OP eds. Population genomics: wildlife. Springer International Publishing, SwitzerlandWaples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Heredity 89:438–450
Google Scholar 
Wethington AR, Lydeard C (2007) A molecular phylogeny of Physidae (Gastropoda: Basommatophora) based on mitochondrial DNA sequences. J Mollusca Stud 73:241–257
Google Scholar 
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMed Central 

Google Scholar 
Witt JDS, Threloff DL, Hebert PDN (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Mol Ecol 15:3073–3082CAS 

Google Scholar 
Witt JDS, Threloff DL, Hebert PDN (2008) Genetic zoogeography of the Hyalella azteca species complex in the Great Basin: rapid rates of molecular diversification in desert springs. In: Hershler R, et al., eds. Late Cenozoic drainage history of the southwestern Great Basin and Lower Colorado River region: geologic and biotic perspectives. Geological Society of America Special Paper 439, Colorado, p 103–114Worthington-Wilmer JL, Murray L, Elkin C, Wilcox C, Niejalke D, Possingham H (2011) Catastrophic floods may pave the way for increased genetic diversity in endemic spring snail populations. PLoS One 6:e28645PubMed Central 

Google Scholar 
Zickovich JM, Bohonak AJ (2007) Dispersal ability and genetic structure in aquatic invertebrates: a comparative study in southern California streams and reservoirs. Freshw Biol 52:1982–1996CAS 

Google Scholar  More

Siver et al.19 identified three categories of fossil Mallomonas species uncovered in the extensive Giraffe Pipe locality. One group of species had scales with morphological characteristics similar to, and difficult to separate from, modern congeners. Based on a morphological species concept, these could be viewed as representing the same species. A second group had morphologically different scales, but ones that could be linked to one or more modern species. The third group possessed scales that could not be directly linked to any modern species. The majority of the species contained in the latter group lacked a V-rib and well developed dome, and were considered as stem organisms within the broad section Planae. Siver et al.19 further reported that the mean size of scales in the group containing the extinct stem taxa was larger than those fossil taxa grouped with modern congeners.The current study adds additional modern and fossil species to the database used by Siver et al.19, including the oldest known taxon from the Cretaceous Wombat locality, and provides the first attempt to reconstruct cell size for fossil Mallomonas species. Based on the expanded database, several trends with respect to the evolution of scale and cell size of Mallomonas taxa can be made. First, there is a strong relationship between scale width and scale length that was similar for both fossil and modern forms. Second, as a group, fossil taxa had scales that are significantly larger than those produced by modern species, especially with respect to surface area. The five species with the largest scales belong to extinct fossil species, four of which belong to the group of stem taxa within section Planae. These scales are massive compared with modern forms, and support the concept of scale gigantism for early members of the Mallomonas clade containing species with scales that lack a V-rib and dome (Fig. 1; subclade A2). Third, assuming the model relating scale and cell size can be applied to the geologic record, fossil species produced significantly larger cells than modern forms.Because the models relating scale length to scale width were similar for modern and fossil species, the assumption is that the models developed relating scale size to cell size are appropriate for fossil taxa. In addition, the precise overlapping pattern of scales comprising the cell covering on modern species has recently been documented for Eocene fossil species22, indicating that this architectural design was well evolved by at least the early Eocene. Thus, making the assumption that other fossil taxa had similarly constructed cell coverings is reasonable, and further supports the application of the models relating scale and cell size to these fossil forms.Based on the model estimates, the mean cell size of the fossil species is approximately twice as large as the average cell produced by modern organisms. This doubling of cell size was also observed for the smallest species. The mean size of the five smallest modern species (M. canina, M. mangofera, M. dickii, M. madagascariensis, and M. gutata) was 9.3 × 5 µm, compared to the mean cell size estimated for the five smallest fossil taxa (M. pseudohamata, M. preisigii, M. dispar, M. bakeri and M. GP4) of 18 × 8.7 µm. The cell size discrepancy is even greater for fossil species that lack modern congeners, and especially for the extinct stem species within section Planae that possessed an average cell size of 69.2 × 20.8 µm, with a maximum cell size of 81.7 × 22.7 µm for M. GP13. The scales produced by these large fossil cells were not only massive in size, but also robust and heavily silicified. It is likely that these large cells covered with large, heavy and cumbersome scales would have been slow swimmers that expended significantly more energy to maintain their position in the water column than modern species. Perhaps these cells were also more prone to predation by larger zooplankton, and a combination of decreased motility and greater predation provided the evolutionary pressure for smaller and faster cells with less dense siliceous components, and ultimately caused the demise of the large-celled fossil species. In contrast, it is also possible that the stimulus initially resulting in the evolution of the larger species was the fact that they were too big to be preyed upon by smaller invertebrates.Several points regarding the models used to estimate cell size are warranted. First, it is important to note that because the scale sizes used to estimate cell sizes for the larger fossil taxa are at the end of the range used to produce the model, caution needs to be exercised. The assumption is being made that the linear relationship of the model holds for the larger scales, and that the linear relationship does not begin to flatten and reach a maximum cell size. However, there is no indication that the relationship is reaching an asymptote, nor reason to assume that the model would not hold for organisms that produce larger siliceous components. Second, the scale and cell size data used to produce the models consisted of the midpoint values of the ranges given in the literature. Thus, the cell sizes inferred from the models represent a midpoint estimate of the range for each species, and not an upper size limit. Third, there is more data available in the literature documenting scale size than there is for cell size for most modern Mallomonas species. Additional data on cell size, especially inclusion of mean values, may help to further fine-tune the models. Lastly, the formula of an ellipse was used to estimate scale surface area for the few species with “square-shaped” scales. Although this may slightly underestimate the surface area, using a formula for a square or rectangle would have resulted in an overestimation. Because the few species with square-shaped scales were primarily the extinct fossil taxa lacking modern congeners, their cell size may actually have been slightly larger than estimated in this study.Interestingly, fossil scales that have morphologically similar (identical) modern counterparts were not significantly different in size from each other, implying that their corresponding cells were also of similar size. These taxa have significantly smaller scales compared to those species with gigantic scales, and closer to the mean of modern species. Perhaps, this is why the lineages of these morphologically-identical species have survived for tens of millions of years. Despite maintaining virtually identical scale types, the degree of genetic difference from a physiological or reproductive perspective between taxa with virtually identical siliceous components remains unknown19,23.The extinct scale types are not only significantly larger than those of species with modern congeners, but some have a tendency of being more rectangular to square-shaped. In contrast, fossil scale types that can be linked to modern species, along with their contemporary counterparts, tend to have elliptical-shaped scales. This is especially true of body scales15,16,19. Although a few smaller species of Mallomonas form spherical cells, the vast majority of species produce ellipsoidal-shaped cells, and this is especially true of species forming larger cells15,16. Smaller elliptical-shaped scales would be more efficient in covering a curving ellipsoidal cell surface than larger and square-shaped scales, and allow for a closer fitting cell covering. Jadrná et al.26 recently reported that scales of the closely related synurophyte genus, Synura, have also become smaller and more elongate over geologic time, complementing the observations for Mallomonas. Taken together, these findings support the idea that the evolutionary trend for synurophyte organisms has been towards smaller, elliptical scales.Cyanobacteria, a prokaryotic group of organisms estimated to have evolved by 3.5–3.4 Ga, represent one of the earliest known and smallest life forms on Earth27. Since the evolution of these early prokaryotes, Smith et al.28 estimated that the maximum body size of subsequent life forms has increased approximately 18-fold, with large jumps occurring with the evolution of eukaryote cells, and another concurrent with the advent of multicellularity. In contrast, shifts in the sizes of siliceous scales and corresponding cells of Mallomonas species are small in comparison, within an order of magnitude, and similar to changes observed for prokaryote organisms and other unicellular protists over the Geozoic28,29.Despite the overall lack of historical information on cell size for the majority of unicellular eukaryote lineages, there are data for some organisms that build resistant cell walls or coverings that are taxonomically diagnostic and become incorporated into the fossil record. Diatoms produce a siliceous cell wall known as the frustule, a structure composed of top and bottom pieces called valves that are held together with additional structures called girdle bands. Frustules, or their valve components, can be uncovered from the fossil record and used to provide a direct measure of cell size. Using this technique, Finkel et al.29 reported that the size of planktic marine diatoms declined over the Cenozoic, and correlated the shift with abiotic forcing factors, including a rise in sea surface temperature and water column stratification. Foraminifera are heterotrophic marine protists that build shells out of calcium carbonate, the latter of which can also become part of the fossil record. Changes in the size of foraminifera shells over the Cenozoic have also been correlated with shifts in the intensity of water column stratification30. At this time, it is not known if the decline in cell size for Mallomonas species in the section Planae lineage recorded in the current study was the result of abiotic variables (e.g. energy expenditure or temperature), biotic factors (e.g. predation), or a combination of forcing variables.The current study has provided a means to link scale size to cell size for Mallomonas that, in turn, can be used to trace shifts in cell size over geologic time. As additional scales of Mallomonas species are uncovered from the fossil record, the scale-to-cell size model will be a valuable tool for continuing to unravel the evolutionary history of cell size for this important photosynthetic organism. Other groups of unicellular protists, including euglyphids, heliozoids and rotosphaerids, are similar to synurophytes in that they build cell coverings using numerous overlapping siliceous scales or plates that can become fossilize. Perhaps the same technique of relating scale size to cell size could be used to develop models for these protist organisms, and similarly applied to the fossil record.It is interesting to note that most modern Mallomonas species with large body scales are found in warm tropical regions, including M. bronchartiana Compère, M. pseudobronchartiana Gusev, Siver & Shin, M. velari Gusev, Siver & Shin31, M. vietnamica Gusev, Kezlya & Trans32, M. gusakovii33 and several varieties of M. matvienkoae16. In addition, the modern tropical taxa M. neoampla Gusev & Siver and M. vietnamica share several rare features of their scales and bristles with fossil species recorded from the Giraffe locality, suggesting a possible link between the modern tropical and fossil floras. During the early to middle Eocene, the Earth experienced warm greenhouse conditions and lacked a cryosphere34. The Giraffe locality, positioned near the Arctic Circle, had an estimated mean annual temperature 17 °C warmer, and a mean annual precipitation over four times higher, than present conditions35. In fact, the assemblage of plants and animals in the Eocene Arctic has been described as analogous to those found today in eastern Asia36. Perhaps tropical regions, especially in southeastern Asia, offered refugia for some of the ancient Mallomonas lineages.In summary, multiple extinct fossil species of the diverse and common synurophyte genus, Mallomonas, are reported here to have possessed gigantic scales that are significantly larger than those found on modern species. Based on a model relating scale to cell size, cells of fossil Mallomonas species were estimated to be, on average, twice as large as modern species. A combination of larger cells with heavy siliceous scales that fit less effectively around the cell may have resulted in slower cells more prone to predation, heavier cells requiring more energy resources to maintain their position in the water column, and ultimately their demise. Additional fossil species, especially representing other localities and time periods, will ultimately strengthen our understanding of the evolution of scale and cell size in synurophyte algae. More

.readcube-buybox { display: none !important;}

Ancient trees thrive where humans don’t: on the remote, rocky slopes of high mountains. So shows an analysis of tens of thousands of trees1.

Access options

Access through your institution

Change institution

Buy or subscribe

/* style specs start */
style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0% 0%;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50% 0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:”;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
/* style specs end */Subscribe to Nature+Get immediate online access to the entire Nature family of 50+ journals$29.99monthlySubscribeSubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueSubscribeAll prices are NET prices. VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00BuyAll prices are NET prices.

Additional access options:

Log in

Learn about institutional subscriptions

doi: https://doi.org/10.1038/d41586-022-00832-x

ReferencesLiu, J. et al. Conserv. Biol. https://doi.org/10.1111/cobi.13907 (2022).Article 

Google Scholar 
Download references

Subjects

Conservation biology

Jobs

Research Associate in Joint Sensing and Communications for Next Generation Wireless Networks

Interdisciplinary Centre for Security, Reliability and Trust (SnT), University of Luxembourg
Luxembourg, Luxembourg

Research Associate / PhD Position (m/f/x)

Technische Universität Dresden (TU Dresden)
01069 Dresden, Germany

Research Associate / PhD Student (m/f/x)

Technische Universität Dresden (TU Dresden)
01069 Dresden, Germany

Research Technician

Oklahoma Medical Research Foundation (OMRF)
Oklahoma City, United States More