Ecology

Alves, J. A. et al. Costs, benefits, and fitness consequences of different migratory strategies. Ecology 94(1), 11–17 (2013).PubMed 

Google Scholar 
Alexander, R. M. When is migration worthwhile for animals that walk, swim or fly?. J. Avian Biol. 29(4), 387–394 (1998).
Google Scholar 
Wikelski, M. et al. Costs of migration in free-flying songbirds. Nature 423, 704 (2003).ADS 
CAS 
PubMed 

Google Scholar 
Alerstam, T., Hedenström, A. & Åkesson, S. Long-distance migration: evolution and determinants. Oikos 103(2), 247–260 (2003).
Google Scholar 
Alerstam, T. Optimal bird migration revisited. J. Ornithol. 152, 5–23 (2011).
Google Scholar 
Hedenstrom, A. & Alerstam, T. Optimum fuel loads in migratory birds: Distinguishing between time and energy minimization. J. Theor. Biol. 189, 227–234 (1997).ADS 
CAS 
PubMed 

Google Scholar 
Åkesson, S. & Helm, B. Endogenous programs and flexibility in bird migration. Front. Ecol. Evol. 8, 78 (2020).
Google Scholar 
Jiguet, F. et al. Desert crossing strategies of migrant songbirds vary between and within species. Sci. Rep. 9(1), 20248 (2019).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Senner, N. R., Morbey, Y. E. & Sandercock, B. K. Editorial: Flexibility in the migration strategies of animals. Front. Ecol. Evol. 8, 111 (2020).
Google Scholar 
Mellone, U., López-López, P., Limiñana, R., Piasevoli, G. & Urios, V. The trans-equatorial loop migration system of Eleonora’s falcon: Differences in migration patterns between age classes, regions and seasons. J. Avian Biol. 44, 417–426 (2013).
Google Scholar 
Chevallier, D. et al. Influence of weather conditions on the flight of migrating black storks. Proc. Biol. Sci. 277(1695), 2755–2764 (2010).CAS 
PubMed 
PubMed Central 

Google Scholar 
Verhelst, B., Jansen, J. & Vansteelant, W. South West Georgia: An important bottleneck for raptor migration during autumn. Ardea 99, 137–146 (2011).
Google Scholar 
Klaassen, R. H. G., Strandberg, R., Hake, M. & Alerstam, T. Flexibility in daily travel routines causes regional variation in bird migration speed. Behav. Ecol. Sociobiol. 62(9), 1427–1432 (2008).
Google Scholar 
Alerstam, T. Detours in bird migration. J. Theor. Biol. 209(3), 319–331 (2001).ADS 
CAS 
PubMed 

Google Scholar 
Alerstam, T. & Hedenström, A. The development of bird migration theory. J. Avian Biol. 29(4), 343–369 (1998).
Google Scholar 
Liechti, F., Klaassen, M. & Bruderer, B. Predicting migratory flight altitudes by physiological migration models. Auk 117, 205–214 (2000).
Google Scholar 
Senner, N. R. et al. High-altitude shorebird migration in the absence of topographical barriers: Avoiding high air temperatures and searching for profitable winds. Proc. Biol. Sci. 2018, 285 (1881).
Google Scholar 
Norevik, G., Akesson, S., Andersson, A., Backman, J. & Hedenstrom, A. Flight altitude dynamics of migrating European nightjars across regions and seasons. J. Exp. Biol. 224(20), jeb242836 (2021).PubMed 
PubMed Central 

Google Scholar 
Hadjikyriakou, T. G., Nwankwo, E. C., Virani, M. Z. & Kirschel, A. N. G. Habitat availability influences migration speed, refueling patterns and seasonal flyways of a fly-and-forage migrant. Mov. Ecol. 8, 10 (2020).PubMed 
PubMed Central 

Google Scholar 
Strandberg, R., Klaassen, R. H. G., Olofsson, P. & Alerstam, T. Daily travel schedules of adult Eurasian Hobbies Falco subbuteo—Variability in flight hours and migration speed along the route. Ardea 97(3), 287–295 (2009).
Google Scholar 
Strandberg, R. & Alerstam, T. The strategy of fly-and-forage migration, illustrated for the osprey (Pandion haliaetus). Behav. Ecol. Sociobiol. 61(12), 1865–1875 (2007).
Google Scholar 
McKinnon, E. A. & Love, O. P. Ten years tracking the migrations of small landbirds: Lessons learned in the golden age of bio-logging. Auk 135(4), 834–856 (2018).
Google Scholar 
Backman, J. et al. Actogram analysis of free-flying migratory birds: New perspectives based on acceleration logging. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 203(6–7), 543–564 (2017).PubMed 
PubMed Central 

Google Scholar 
Evens, R., Beenaerts, N., Witters, N. & Artois, T. Study on the foraging behaviour of the European nightjar Caprimulgus europaeus reveals the need for a change in conservation strategy in Belgium. J. Avian Biol. 48(9), 1238–1245 (2017).
Google Scholar 
Evens, R. et al. Lunar synchronization of daily activity patterns in a crepuscular avian insectivore. Ecol. Evol. 10(14), 7106–7116 (2020).PubMed 
PubMed Central 

Google Scholar 
Liechti, F. et al. Miniaturized multi-sensor loggers provide new insight into year-round flight behaviour of small trans-Sahara avian migrants. Mov. Ecol. 6, 19 (2018).PubMed 
PubMed Central 

Google Scholar 
Liechti, F., Witvliet, W., Weber, R. & Bachler, E. First evidence of a 200-day non-stop flight in a bird. Nat. Commun. 4, 2554 (2013).ADS 
PubMed 

Google Scholar 
Dhanjal-Adams, K. L. PAMLr: Suite of functions for manipulating pressure, activity, magnetism and light data in R. (2020).Lisovski, S. et al. Light-level geolocator analyses: A user’s guide. J. Anim. Ecol. 89(1), 221–236 (2020).PubMed 

Google Scholar 
Lisovski, S. et al. Geolocation by light: Accuracy and precision affected by environmental factors. Methods Ecol. Evol. 3(3), 603–612 (2012).
Google Scholar 
Wotherspoon, S., Sumner, M., Lisovski, S. SGAT-Package: Solar/Satellite Geolocation for Animal Tracking. (2021). R package version 0.1.3. GitHub Repository.Bauer, R. RchivalTag: Analyzing Archival Tagging Data. R package version 0.1.2. (2020).Sjöberg, S. et al. Barometer logging reveals new dimensions of individual songbird migration. J. Avian Biol. 49(9), e01821 (2018).
Google Scholar 
Evens, R. et al. Migratory pathways, stopover zones and wintering destinations of Western European Nightjars Caprimulgus europaeus. Ibis 159(3), 680–686 (2017).
Google Scholar 
Becker, J. J. et al. Global bathymetry and elevation data at 30 arc seconds resolution: SRTM30_PLUS. Mar. Geodesy 32(4), 355–371 (2009).
Google Scholar 
Ricketts, T. H. Terrestrial Ecoregions of North America: A Conservation Assessment (Island Press, 1999).
Google Scholar 
Olson, D. M. et al. Terrestrial ecoregions of the world: A new map of life on earth. Bioscience 51(11), 933–938 (2001).
Google Scholar 
QGIS-Development-Team: QGIS Geographic Information System. Open Source Geospatial Foundation (2021).Vansteelant, W. M. G., Gangoso, L., Bouten, W., Viana, D. S. & Figuerola, J. Adaptive drift and barrier-avoidance by a fly-forage migrant along a climate-driven flyway. Mov. Ecol. 9(1), 37 (2021).PubMed 
PubMed Central 

Google Scholar 
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9(2), 378–400 (2017).
Google Scholar 
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical Multi-Level/Mixed) Regression Models. R package version 0.3.3.0. (2020).Lenth, R. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.1. (2020).Akesson, S., Bianco, G. & Hedenstrom, A. Negotiating an ecological barrier: Crossing the Sahara in relation to winds by common swifts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371(1704), 20150393 (2016).PubMed 
PubMed Central 

Google Scholar 
Strandberg, R., Klaassen, R. H. G., Hake, M., Olofsson, P. & Alerstam, T. Converging migration routes of Eurasian Hobbies Falco subbuteo crossing the African equatorial rain forest. Proc. R. Soc. B 276, 727–733 (2009).PubMed 

Google Scholar 
Rodriguez-Ruiz, J. et al. Disentangling migratory routes and wintering grounds of Iberian near-threatened European Rollers Coracias garrulus. PLoS ONE 9(12), e115615 (2014).ADS 
PubMed 
PubMed Central 

Google Scholar 
Vickery, J. A. et al. The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis 156, 1–22 (2014).
Google Scholar 
Evens, R. et al. Proximity of breeding and foraging areas affects foraging effort of a crepuscular, insectivorous bird. Sci. Rep. 8(1), 3008 (2018).ADS 
PubMed 
PubMed Central 

Google Scholar 
Conring, C. M., Brautigam, K., Grisham, B. A., Collins, D. P. & Conway, W. C. Identifying the migratory strategy of the Lower Colorado River Valley population of Greater Sandhill Cranes. Avian Conserv. Ecol. 14(1), 11 (2019).
Google Scholar 
Imlay, T. L., Saldanha, S. & Taylor, P. D. The fall migratory movements of Bank Swallows, Riparia riparia: Fly-and-forage migration?. Avian Conserv. Ecol. 15(1), 2 (2020).
Google Scholar 
Piersma, T. Hop, skip, or jump? Constraints on migration of arctic waders by feeding, fattening, and flight speed. Limosa 60, 185–194 (1987).
Google Scholar 
Warnock, N. Stopping vs. staging: The difference between a hop and a jump. J. Avian Biol. 41(6), 621–626 (2010).
Google Scholar 
Gomez, C. et al. Fuel loads acquired at a stopover site influence the pace of intercontinental migration in a boreal songbird. Sci. Rep. 7(1), 3405 (2017).ADS 
PubMed 
PubMed Central 

Google Scholar 
Tottrup, A. P. et al. The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proc. Biol. Sci. 279(1730), 1008–1016 (2012).PubMed 

Google Scholar 
Lisovski, S. et al. Inherent limits of light-level geolocation may lead to over-interpretation. Curr. Biol. 28(3), R99–R100 (2018).CAS 
PubMed 

Google Scholar 
Buler, J. J., Moore, F. R. & Woltmann, S. A multi-scale examination of stopover habitat use by birds. Ecology 88(7), 1789–1802 (2007).PubMed 

Google Scholar 
Loon, A. V. et al. Migratory stopover timing is predicted by breeding latitude, not habitat quality, in a long-distance migratory songbird. J. Ornithol. 158(3), 745–752 (2017).
Google Scholar 
Norevik, G. et al. Wind-associated detours promote seasonal migratory connectivity in a flapping flying long-distance avian migrant. J. Anim. Ecol. 89(2), 635–646 (2020).PubMed 

Google Scholar 
Norevik, G., Åkesson, S. & Hedenström, A. Migration strategies and annual space-use in an Afro-Palaearctic aerial insectivore—The European nightjar Caprimulgus europaeus. J. Avian Biol. 48(5), 738–747 (2017).
Google Scholar 
Cresswell, B. & Edwards, D. Geolocators reveal wintering areas of European Nightjar (Caprimulgus europaeus). Bird Study 60(1), 77–86 (2013).
Google Scholar 
Jacobsen, L. B. et al. Annual spatiotemporal migration schedules in three larger insectivorous birds: European nightjar, common swift and common cuckoo. Anim. Biotelem. 5(1), 1–11 (2017).
Google Scholar 
Liechti, F. & Bruderer, B. The relevance of wind for optimal migration theory. J. Avian Biol. 29(4), 561–568 (1998).
Google Scholar 
Schmaljohann, H., Bruderer, B. & Liechti, F. Sustained bird flights occur at temperatures far beyond expected limits. Anim. Behav. 76(4), 1133–1138 (2008).
Google Scholar 
Schmaljohann, H., Liechti, F. & Bruderer, B. Trans-Sahara migrants select flight altitudes to minimize energy costs rather than water loss. Behav. Ecol. Sociobiol. 63(11), 1609–1619 (2009).
Google Scholar 
Sjöberg, S. et al. Extreme altitudes during diurnal flights in a nocturnal songbird migrant. Science 372, 646–648 (2021).ADS 
PubMed 

Google Scholar 
Bruderer, B., Peter, D. & Korner-Nievergelt, F. Vertical distribution of bird migration between the Baltic Sea and the Sahara. J. Ornithol. 159(2), 315–336 (2018).
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

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

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

Kelley, N. P. & Pyenson, N. D. Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene. Science 348, aaa3716 (2015).PubMed 

Google Scholar 
Gutarra, S. & Rahman, I. A. The locomotion of extinct secondarily aquatic tetrapods. Biol. Rev. 97, 67–98 (2022).PubMed 

Google Scholar 
Owen, R. A description of a portion of the skeleton of the Cetiosaurus, a gigantic extinct saurian reptile occurring in the oolitic formations of different portions of England. Proc. Geol. Soc. Lond. 3, 457–462 (1841).
Google Scholar 
Cope, E. On the characters of the skull in the Hadrosauridae. Proc. Natl Acad. Nat. Sci. USA 35, 97–107 (1883).
Google Scholar 
Bidar, A., Demay, L. & Thomel, G. Compsognathus corallestris, une nouvelle espèce de dinosaurien théropode du Portlandien de Canjuers (Sud-Est de la France). Annales Muséum d’Histoire Naturelle de Nice 1, 9–40 (1972).
Google Scholar 
Norell, M. A., Makovicky, P. J. & Currie, P. J. The beaks of ostrich dinosaurs. Nature 412, 873–874 (2001).ADS 
CAS 
PubMed 

Google Scholar 
Tereschenko, V. S. Adaptive features of protoceratopoids (Ornithischia: Neoceratopsia). Paleontol. J. 42, 273–286 (2008).
Google Scholar 
Lee, Y. N. et al. Resolving the long-standing enigmas of a giant ornithomimosaur Deinocheirus mirificus. Nature 515, 257–260 (2014).ADS 
CAS 
PubMed 

Google Scholar 
Ibrahim, N. et al. Semiaquatic adaptations in a giant predatory dinosaur. Science 345, 1613–1616 (2014).ADS 
CAS 
PubMed 

Google Scholar 
Cau, A. et al. Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs. Nature 552, 395–399 (2017).ADS 
CAS 
PubMed 

Google Scholar 
Ibrahim, N. et al. Tail-propelled aquatic locomotion in a theropod dinosaur. Nature 581, 67–70 (2020).ADS 
CAS 
PubMed 

Google Scholar 
Henderson, D. M. A buoyancy, balance and stability challenge to the hypothesis of a semi-aquatic Spinosaurus Stromer, 1915 (Dinosauria: Theropoda). PeerJ 6, e5409 (2018).PubMed 
PubMed Central 

Google Scholar 
Hone, D. W. E. & Holtz, T. R. Jr Evaluating the ecology of Spinosaurus: shoreline generalist or aquatic pursuit specialist? Palaeontol. Electronica 24, a03 (2021).
Google Scholar 
Thewissen, J. G., Cooper, L. N., Clementz, M. T., Bajpai, S. & Tiwari, B. N. Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450, 1190–1194 (2007).ADS 
CAS 
PubMed 

Google Scholar 
Houssaye, A. Bone histology of aquatic reptiles: what does it tell us about secondary adaptation to an aquatic life? Biol. J. Linn. Soc. 108, 3–21 (2013).
Google Scholar 
Motani, R. et al. A basal ichthyosauriform with a short snout from the Lower Triassic of China. Nature 517, 485–488 (2015).ADS 
CAS 
PubMed 

Google Scholar 
Rauhut, O. W. & Pol, D. Probable basal allosauroid from the early Middle Jurassic Cañadón Asfalto Formation of Argentina highlights phylogenetic uncertainty in tetanuran theropod dinosaurs. Sci. Rep. 9, 1–9 (2019).
Google Scholar 
You, H. L. et al. A nearly modern amphibious bird from the Early Cretaceous of northwestern China. Science 312, 1640–1643 (2006).ADS 
CAS 
PubMed 

Google Scholar 
Wilson, L. E. & Chin, K. Comparative osteohistology of Hesperornis with reference to pygoscelid penguins: the effects of climate and behaviour on avian bone microstructure. R. Soc. Open Sci. 1, 140245 (2014).ADS 
PubMed 
PubMed Central 

Google Scholar 
Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996).PubMed 

Google Scholar 
Amiot, R. et al. Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology 38, 139–142 (2010).ADS 
CAS 

Google Scholar 
Hassler, A. et al. Calcium isotopes offer clues on resource partitioning among Cretaceous predatory dinosaurs. Proc. R. Soc. B 285, 20180197 (2018).PubMed 
PubMed Central 

Google Scholar 
Larramendi, A., Paul, G. S. & Hsu, S. Y. A review and reappraisal of the specific gravities of present and past multicellular organisms, with an emphasis on tetrapods. Anat. Rec. 304, 1833–1888 (2021).
Google Scholar 
Charig, A. J. & Milner, A. C. Baryonyx, a remarkable new theropod dinosaur. Nature 324, 359–361 (1986).ADS 
CAS 
PubMed 

Google Scholar 
Schoener, T. W. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331, 426–429 (2011).ADS 
CAS 
PubMed 

Google Scholar 
Houssaye, A. “Pachyostosis” in aquatic amniotes: a review. Integr. Zool. 4, 325–340 (2009).PubMed 

Google Scholar 
Houssaye, A., Sander, M. P. & Klein, N. Adaptive patterns in aquatic amniote bone microanatomy—more complex than previously thought. Integr. Comp. Biol. 56, 1349–1369 (2016).PubMed 

Google Scholar 
Quemeneur, S., De Buffrenil, V. & Laurin, M. Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol. J. Linn. Soc. 109, 644–655 (2013).
Google Scholar 
Canoville, A., de Buffrénil, V. & Laurin, M. Microanatomical diversity of amniote ribs: an exploratory quantitative study. Biol. J. Linn. Soc. 118, 706–733 (2016).
Google Scholar 
Amson, E., de Muizon, C., Laurin, M., Argot, C. & de Buffrénil, V. Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proc. R. Soc. B 281, 20140192 (2014).PubMed 
PubMed Central 

Google Scholar 
Grafen, A. The phylogenetic regression. Philos. Trans. R. Soc. B 326, 119–157 (1989).ADS 
CAS 

Google Scholar 
Liem, K. F. Adaptive significance of intra-and interspecific differences in the feeding repertoires of cichlid fishes. Am. Zool. 20, 295–314 (1980).
Google Scholar 
Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M. & Norell, M. A. A basal dromaeosaurid and size evolution preceding avian flight. Science 317, 1378–1381 (2007).ADS 
CAS 
PubMed 

Google Scholar 
Voeten, D. F. et al. Wing bone geometry reveals active flight in Archaeopteryx. Nat. Commun. 9, 1319 (2018).
Google Scholar 
Houssaye, A., Martin, F., Boisserie, J. R. & Lihoreau, F. Paleoecological inferences from long bone microanatomical specializations in Hippopotamoidea (Mammalia, Artiodactyla). J. Mamm. Evol. 28, 847–870 (2021).
Google Scholar 
Amson, E. & Bibi, F. Differing effects of size and lifestyle on bone structure in mammals. BMC Biol. 19, 87 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Malafaia, E. et al. A new spinosaurid theropod (Dinosauria: Megalosauroidea) from the upper Barremian of Vallibona, Spain: Implications for spinosaurid diversity in the Early Cretaceous of the Iberian Peninsula. Cret. Res. 106, 104221 (2020).
Google Scholar 
Sereno, P. C. et al. A long-snouted predatory dinosaur from Africa and the evolution of spinosaurids. Science 282, 1298–1302 (1998).ADS 
CAS 
PubMed 

Google Scholar 
Aureliano, T. et al. Semi-aquatic adaptations in a spinosaur from the Lower Cretaceous of Brazil. Cret. Res. 90, 283–295 (2018).
Google Scholar 
Barker, C. T. et al. New spinosaurids from the Wessex Formation (Early Cretaceous, UK) and the European origins of Spinosauridae. Sci. Rep. 11, 19340 (2021).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Taquet, P. Géologie et Paléontologie du Gisement de Gadoufaoua (Aptien du Niger) (Éditions du Centre national de la Recherche Scientifique, 1976).Rayfield, E. J., Milner, A. C., Xuan, V. B. & Young, P. G. Functional morphology of spinosaur ‘crocodile-mimic’ dinosaurs. J. Vertebr. Paleontol. 27, 892–901 (2007).
Google Scholar 
Benson, R. B., Butler, R. J., Carrano, M. T. & O’Connor, P. M. Air‐filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition. Biol. Rev. 87, 168–193 (2012).PubMed 

Google Scholar 
Reid, R. E. H. Zonal “growth rings” in dinosaurs. Mod. Geol. 15, 19–48 (1990).
Google Scholar 
Chinsamy, A. & Raath, M. A. Preparation of fossil bone for histological examination. Palaeont. Afr. 29, 39–44 (1992).
Google Scholar 
Griffin, C. T. et al. Assessing ontogenetic maturity in extinct saurian reptiles. Biol. Rev. 96, 470–525 (2021).
Google Scholar 
Carrano, M. T., Benson, R. B. & Sampson, S. D. The phylogeny of Tetanurae (Dinosauria: Theropoda). J. Syst. Palaeontol. 10, 211–300 (2012).
Google Scholar 
Ibrahim, N. et al. Geology and paleontology of the Upper Cretaceous Kem Kem Group of eastern Morocco. ZooKeys 928, 1–216 (2020).PubMed 
PubMed Central 

Google Scholar 
Smyth, R. S., Ibrahim, N. & Martill, D. M. Sigilmassasaurus is Spinosaurus: a reappraisal of African spinosaurines. Cret. Res. 114, 104520 (2020).
Google Scholar 
Goloboff, P. A., Farris, J. S. & Nixon, K. C. TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786 (2008).
Google Scholar 
Erickson, G. M. Assessing dinosaur growth patterns: a microscopic revolution. Trends Ecol. Evol. 20, 677–684 (2005).PubMed 

Google Scholar 
Hayashi, S. et al. Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS ONE 8, e59146 (2013).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Straehl, F. R., Scheyer, T. M., Forasiepi, A. M., MacPhee, R. D. E. & Sánchez-Villagra, M. R. Evolutionary patterns of bone histology and bone compactness in xenarthran mammal long bones. PLoS ONE 8, e69275 (2013).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Houssaye, A., Tafforeau, P., de Muizon, C. & Gingerich, P. D. Transition of Eocene whales from land to sea: evidence from bone microstructure. PLoS ONE 10, e0118409 (2015).PubMed 
PubMed Central 

Google Scholar 
Girondot, M. & Laurin, M. Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J. Vertebr. Paleontol. 23, 458–461 (2003).
Google Scholar 
De Ricqlès, A. J., Padian, K., Horner, J. R., Lamm, E. T. & Myhrvold, N. Osteohistology of Confuciusornis sanctus (Theropoda: Aves). Journ. Vertebr. Paleontol. 23, 373–386 (2003).
Google Scholar 
Maddison, W. P. Mesquite: a modular system for evolutionary analysis. Evolution 62, 1103–1118 (2008).
Google Scholar 
Upham, N. S., Esselstyn, J. A. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 17, e3000494 (2019).CAS 
PubMed 
PubMed Central 

Google Scholar 
Simoes, T. R. et al. The origin of squamates revealed by a Middle Triassic lizard from the Italian Alps. Nature 557, 706–709 (2018).ADS 
CAS 
PubMed 

Google Scholar 
Nesbitt, S. J. et al. The earliest bird-line archosaurs and the assembly of the dinosaur body plan. Nature 544, 484–487 (2017).ADS 
CAS 
PubMed 

Google Scholar 
Langer, M. C. et al. Untangling the dinosaur family tree. Nature 551, E1–E3 (2017).PubMed 

Google Scholar 
Brusatte, S. L., Lloyd, G. T., Wang, S. C. & Norell, M. A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition. Curr. Biol. 24, 2386–2392 (2014).CAS 
PubMed 

Google Scholar 
Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).ADS 
CAS 
PubMed 

Google Scholar 
Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).
Google Scholar 
Schmitz, L. & Motani, R. Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science 332, 705–708 (2011).ADS 
CAS 
PubMed 

Google Scholar 
Motani, R. & Schmitz, L. Phylogenetic versus functional signals in the evolution of form–function relationships in terrestrial vision. Evolution 65, 2245–2257 (2011).PubMed 

Google Scholar  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

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

The Willmott similarity indices, over the first 4 months, for outside and inside temperatures, in sunny and shaded environments, with values close to 1, confirm that A. sexdens colonies were exposed to significantly different temperatures. The lowest values of this index for irradiance, differing between the sunny and shaded environments for internal temperature (in the initial chamber), indicates variation in this parameter between environments. Irradiance values close to 0 between environments represent differences between sunny and shaded areas, but the temperature of the initial chamber did not vary. The selection pressure from irradiance and, consequently, temperature, defines the ideal depth of the initial chamber for the founding queens16 to keep this parameter at values adequate for the fungus garden and the offspring8 in the field. The similar temperature, in the nests in the shaded environment, agrees with that reported for this leaf-cutting ant, of 24°C3, but this varies between species of these insects, being 25–28 °C for A. sexdens17, 27.5 °C for A. vollenweideri18 and 27 °C for A. heyeri19. This adaptation of an ideal depth to construct the initial chamber allows A. sexdens to adapt to different habitats in full sun and shade. The nesting process, habits and foraging strategies differ between A. bisphaerica and A. sexdens, with the former normally establishing their nests in full sun in areas with predominantly grass forages and the latter in shaded areas where it cuts dicot leaves14. Furthermore, differences in nest depth between these species may be related to soil temperature, which is lower in shaded areas7. For this reason, fungal chambers in exposed nests in pastures are deeper than in shaded areas in forests, as soil temperature is negatively correlated with depth7. Soil humidity and temperature act simultaneously due to the thermo preference of workers, resulting in the construction of shallower nests in cold soils and deeper nests in warmer ones7. Soil moisture also varies according to depth, affecting the nest-digging behavior of leaf-cutting ants7,15.The temperature in the shaded environment was higher than that reported for A. sexdens rubropilosa, from 24.82 ± 3.14 to 24.11 ± 1.30 °C at a depth of 5–25 cm underground, for optimal offspring development and, consequently, reduction in the lipid content of queens at high temperatures, without affecting their survival20. This is because the depth of the initial chamber excavated by the queen is adequate for colony success8,16.The different habitats occupied by the ant A. sexdens21, from dense forests to cerrado and caatinga may explain the greater depth and volume of the initial chamber of the nests in shaded than in sunny environments. However, the depth of the initial nests varies between Atta species with 7.5–12 cm, 6.5–13 cm, 15–25 cm, 10–30 cm, 10–15 cm, 11–34 cm, and 9–15 cm for A. colombica, A. cephalotes, A. texana, A. sexdens rubropilosa, A bisphaerica, A capiguara, and A. insulares, respectively1,13,15,22,23,24. The initial chamber volume is within the expected range for A. sexdens1,13 in both environments, with a chamber volume of 24.88 cm3 in a shaded area with eucalyptus plantation13. Different excavation efforts with the removal of small soil particles by the founding queen using her jaws in repeated biting motions25, subsequently discarded outside the nest8,16,26 may explain the greater volume of the initial chamber in the shaded area. The greater solar irradiation in sunny areas increases the temperature, with the higher soil temperature generating greater excavation effort and oxidative damage27,28, in addition to water loss, as described for seed-collecting ants29,30. Further, humid soils are easier to dig, which explains the greater volume of the initial chamber in the shaded area as found for the excavation behavior by Atta spp. in soils with different densities and moistures15,16,31.The higher mass of A. sexdens queens in the first month of the claustral phase than in the fourth, in both sunny and shaded environments, stems from a reduction in their body mass, due to the metabolism of the lipid content during the first 6 months following the flight, but with recovery in the subsequent months1. The mass loss is due to the use of body reserves by the queens to prepare and maintain the colony in the claustral phase, as stored lipids are important in the evolutionary history of the Attini tribe, from semi-claustral to claustral foundation32. The queen, with a claustral foundation, does not feed, remaining enclosed in the nest and rearing her initial offspring by metabolizing her own body reserves33, as reported for this ant species1. The selection pressure on the evolution of claustral foundation tends to minimize risk during foraging33 with a more viable adaptation being the storing of reserves in the body, as observed in our study. The greater biomass of the fungus garden in the fourth month is due to growth, but its values were lower than those reported for 4-month-old A. sexdens nests, from 2000 to 3000 mg1.The lower number of A. sexdens eggs in the first than in the third month is similar to that observed in laboratory colonies of this ant8. The irregularity in the egg production by the queen is due to hormone fluctuations regulated by the endocrine system, and is correlated with the activity cycle of the corpora allata during the 3 or 4 months of colony life34. This gland synthesizes the juvenile hormone, which acts in the oviposition of founding queens, as verified for females that underwent alatectomy34. This hormone acts in the fat body, initiating the synthesis of vitellogenin (glycolipophosphoproteins, with lipids and carbohydrates in its composition) to be deposited in the oocyte35. Thus, the production of offspring depends on body reserves (fatty body lipids and muscle mass protein), as the queen does not feed during the foundation period (claustral foundation). The lower production of small and medium workers in the first month than in the second, third or fourth months, agrees with that reported in A. sexdens nests1. The similar number of larvae over the 4 months is due to the duration of the larval period of A. sexdens, of around 25 days8, with new immature individuals produced monthly with overlapping generations, common in social insects. This overlap begins with larvae in the first month of nests and pupae, usually in the second month of ant nests in the laboratory8.The lower values of fungus biomass and number of eggs, larvae, pupae and small and medium workers of A. sexdens in nests in the sunny environment may be due to a higher incidence of solar irradiance increasing the variation in the internal temperature of the initial chamber. This agrees with reports that a lower incidence of solar irradiance improved the stability of the internal temperature of the initial chamber, favoring A. sexdens with narrow thermal tolerance range as it is a thermally protected underground species11. However, frequent heat peaks, with habitat-specific physiological consequences for subterranean ectothermic animals, are common in sunny areas11. The queen’s body mass, similar between environments, indicates a similar reduction of this parameter between them and their tolerance to temperature variations in this type of foundation. A reduction in the mass of A. sexdens queens is expected from the nuptial flight to the end of the claustral phase. The energy expenditure of A. sexdens queens, in carbohydrates and body lipids for the nuptial flight and nest excavation, was estimated at 0.58 J36 and during the claustral phase, they metabolize body lipids and proteins to survive and form the initial colony26,37.The higher mortality of A. sexdens nests in the sunny environment, during the claustral foundation, is due to a higher incidence of solar irradiance, increasing the variation in the internal temperature of the initial chamber and, consequently, the excavation effort and oxidative damage to the founding queens27,28, in addition to water losses as reported for seed-collecting ants29,30. This mortality may also be related to entomopathogens, unsuccessful symbiotic fungus regurgitation, excavation effort, density and soil moisture1,9,38,39.Atta sexdens founder queens were exposed to sunny and shaded environments with greater solar irradiance and, consequently, a greater variation range in the internal temperature of the initial chamber in the first environment. The shaded environment, with lower incidence of solar irradiance and greater stability of the internal temperature of the initial chamber, was more favorable for colony development, as confirmed by the biological parameters and greater survival of A. sexdens queens.
Atta sexdens female collection methods- after the nuptial flightAtta sexdens queens were collected at the Experimental Farm Lageado in Botucatu, Brazil in 2019 (22°50′37.3″S 48°25′38.3″W) on sunny days after heavy rains from late October to early November. Two hundred queens were collected using tweezers. They were stored separately in 250 ml pots with 1 cm wet plaster for 60 min prior to use. We had permission to collect Atta sexdens queen specimens.Experimental areasThe A. sexdens queens were individualized in two experimental areas: sunny—an open area exposed to Global Horizontal Irradiation with exclusive coverage of Paspalum notatum Flügge grass (N = 100) and shaded – an area exposed to Diffuse Horizontal Irradiation (50% shade screen—1.50 × 50 MT), in a plowed environment (N = 100). The soil is a superficial horizon of oxisols.The founding A. sexdens queens were individualized in the center of a square of land (50 × 50 cm) covered with a transparent bottle measuring 20 cm in diameter by 12 cm in height, delimiting the space to be drilled in the soil by the ant queens per experimental area of 25 m2 (Fig. S1).Development of early nests during the claustral phaseAtta sexdens queens were evaluated over 4 months following nest foundation, to monitor its development. A total of 25% of the successfully established nests were excavated per month by removing the colony with a gardening shovel. The number of eggs, larvae, pupae and adults was counted and the mass of the queen and the biomass of the fungus garden determined. The depth, width, length, and height of each nest were measured with the aid of a caliper. The estimated volume of each fungus chamber was based on a cylinder. A correction factor was used to calculate the volume of the chamber because they are rounded: V = πr2 (ch + r0.67), in which ‘r’ is the chamber base radius and ‘ch’ the cylinder height, measured by subtracting the maximum height of the chamber from its radius, ch = h − r40. Queen mortality was evaluated during the excavation of their nests.Temperature and radiation measurementThe temperatures of the external and internal environments (15 cm deep), in each area, were measured for 4 months, with Data loggers (Testo), after the foundation of the nest by the leaf-cutting ant. Global Horizontal Irradiation (GHI) was measured using an Eppley PSP Pyranometer and Diffuse Horizontal Irradiation by a Kipp & Zonen CM3 Pyranometer (Table 3). Solar measurements were obtained over a five-minute time scale (mean of 60 readings with scanning time every five seconds) in W/m2 by a CR300041 model data logger and stored in an ASCII file.Table 3 Instruments used to measure solar irradiance in nests of Atta sexdens (Hymenoptera: Formicidae) in sunny and shaded environments.Full size tableThe measurements were submitted to a quality control procedure to verify if their values were in accordance with pre-defined solar irradiance thresholds. This procedure consists of a series of checks on physically possible limits per component measured (Table 4). These checks were carried out according to the process created by the International Commission on Illumination (CIE) discarding erroneous measures to avoid compromising the processes of numerical integration or data processing.Table 4 Physically possible minimum and maximum values for each measurement of solar irradiance.Full size tableMeasures accepted as possible were those above 0 W/m2 and lower than the maximum stipulated limit, per component, according to the extraterrestrial solar irradiance (IE) (Eq. 1). This represents the maximum value reaching the top of the atmosphere, without attenuation by atmospheric elements (clouds, particles, among others). Values measured at the earth’s surface are lower than those at the top of the atmosphere. However, the phenomenon of multireflection when scattered clouds near the apparent location of the sun reflect part of the solar irradiance onto the sensor, increase the value measured even higher than the extraterrestrial irradiance over short periods45. For this reason, the global irradiance value can be up to 20% higher than that of the extraterrestrial one.The 1361 of Eq. (1), to calculate the extraterrestrial irradiance, represents the solar constant in W/m246, R the relation of the average dimensionless distance between the Earth and the Sun (Eq. 2) and Z the zenithal angle of the Sun (Eq. 3) in degrees47.$${text{I}}_{{text{E}}} = {1361}left( {text{1/R}} right) ,{{cos}}, left( {text{Z}} right)$$
(1)
$$begin{aligned} {text{R}} & = {1} – 0.000{9467};{text{sen}} left( {text{F}} right) – 0.0{1671};{text{cos}},left( {text{F}} right) – 0.000{1489}left( {{text{2F}}} right) \ & quad – 0.0000{2917};{text{sen}}left( {{text{3F}}} right) – 0.000{3438};{text{cos}},left( {{text{4F}}} right) \ end{aligned}$$
(2)
$${text{Z}} = {text{sen}} ,left(updelta right);{text{sen}}left(upphi right) + cos left(updelta right);cos left(upphi right);cos left(upomega right)$$
(3)
F, in Eq. (4), is the angular fraction of the date of interest in degrees, δ, at 5, the solar declination in degrees, Φ, at 6, the geographic latitude of the location in degrees (22.85) and ω, at 6, the clockwise angle in degrees.$${mathbf{F}} = {36}0^circ ;{text{D/365}}$$
(4)
$$begin{aligned} {{varvec{updelta}}} & = 0.{3964} + {3}.{631};{text{sen}}left( {text{F}} right) – {22}.{97};{text{cos}}left( {text{F}} right) + 0.0{3838};{text{sen}}left( {{text{2F}}} right) – 0.{3885};{text{cos}};left( {{text{2F}}} right) \ & quad + 0.0{7659};{text{sen}};left( {{text{3F}}} right) – 0.{1587};{text{cos}}left( {{text{3F}}} right) – 0.0{1}0{21};{text{cos}}left( {{text{4F}}} right) \ end{aligned}$$
(5)
$${{varvec{upomega}}} = left( {{12} – {text{Hd}}} right){15}$$
(6)
The d, in the previous expression, represents the day of the year, from 1 to 365 and the Hd, the hour and the tenth of an hour in degrees of the moment of interest.The values were numerically integrated, after applying the measurement quality control procedure, obtaining a solar irradiation value for the day in MJ/m2 representing the total energy received daily, on a horizontal surface of 1 m2.Statistical analysisThe null hypothesis that the mortality proportions (probabilities of success) of the founding queens of both groups are the same was submitted to the test of equal proportions.The null hypothesis that a data sample came from a normally distributed population was submitted to the Shapiro–Wilk test.Data structure fitting the ANOVA (completely randomized factorial scheme) assumptions were submitted to this analysis and to Tukey’s test for multiple comparisons of means. The Scheirer Ray Hare test is a nonparametric test used for a two-way completely randomized factorial design49. This procedure is an extension of the Kruskal–Wallis rank test allowing for calculation of the interaction effects and linear contrasts and were used for data structure that did not fit the ANOVA assumptions. Dunn’s test50 of multiple median comparisons was performed with a correction (the false discovery rate method) to control the experiment-wise error rate.The Willmott’s Index of Similarity (d) is a standardized measure of the degree of similarity between two data series ranging from 0.0 to 1.0 with the value 1.0 indicating a perfect match (two identical data sets), and 0 no agreement at all51. As an example, in the sunny environment, the indoor and outdoor temperature data were identical, which results in 1.0. The more identical, close, and concordant two data sets are, the closer to 1.0 they will be. The calculation of the index is presented with A and B representing two data sets whose agreement is to be evaluated.$$begin{aligned} A^{prime}_{i} & = A_{i} – overline{B} \ B^{prime}_{i} & = B_{i} – overline{B} \ d & = 1 – frac{{sumnolimits_{i = 1}^{N} {left( {A_{i} – B_{i} } right)^{2} } }}{{sumnolimits_{i = 1}^{N} {left[ {left| {A_{i} } right| – left| {B_{i} } right|} right]^{2} } }} \ end{aligned}$$The R companion package, ggplot252, FSA53, tidyverse54, and hydroGOF55 used is a free software environment for statistical computing and graphics R version 4.0.456. More