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    Long-distance, synchronized and directional fall movements suggest migration in Arctic hares on Ellesmere Island (Canada)

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    Measuring protected-area effectiveness using vertebrate distributions from leech iDNA

    This section provides an overview of methods. The Supplementary Information provides additional detailed descriptions of the leech collections, laboratory processing, bioinformatics pipeline, and site-occupancy modelling. Code for our bioinformatics pipeline is available at Ji72 and Yu73. Code for our site-occupancy modelling and analysis is available at Baker et al.74.Leech collectionsSamples were collected during the rainy season, from July to September 2016, by park rangers from the Ailaoshan Forestry Bureau. The nature reserve is divided into 172 non-overlapping patrol areas defined by the Yunnan Forestry Survey and Planning Institute. These areas range in size from 0.5 to 12.5 km2 (mean 3.9 ± sd 2.5 km2), in part reflecting accessibility (smaller areas tend to be more rugged). These patrol areas pre-existed our study, and are used in the administration of the reserve. The reserve is divided into six parts, which are managed by six cities or autonomous counties (NanHua, ChuXiong, JingDong, ZhenYuan, ShuangBai, XinPing) which assign patrol areas to the villages within their jurisdiction based on proximity. The villages establish working groups to carry out work within the patrol areas. Thus, individual park rangers might change every year, but the patrol areas and the villages responsible for them are fixed.Each ranger was supplied with several small bags containing tubes filled with RNAlater preservative. Rangers were asked to place any leeches they could collect opportunistically during their patrols (e.g. from the ground or clothing) into the tubes, in exchange for a one-off payment of RMB 300 ( ~USD 45) for participation, plus RMB 100 if they caught one or more leeches. Multiple leeches could be placed into each tube, but the small tube sizes generally required the rangers to use multiple tubes for their collections.A total of 30,468 leeches were collected in 3 months by 163 rangers across all 172 patrol areas. When a bag of tubes contained  More

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    Mandible shape variation and feeding biomechanics in minks

    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

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    Rush or relax: migration tactics of a nocturnal insectivore in response to ecological barriers

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