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Home , African striped weasel, Galictis, Greater grison, Musteloidea, Patagonian weasel

chapter 3 Form and function of the musteloids

Andrew C. Kitchener, Carlo Meloro, and Terrie M. Williams

Fisher skull © Neil McLean, National Museums Scotland

Introduction with short legs. This common body plan is adapted to three main functional types: terrestrial/fossorial With a fossil history dating back 30–32 million years (e.g. , , ; see Chapters 10 and 15, ago (late Eocene and early ), the Muste- this volume), scansorial/arboreal (e.g. ; see loidea are now the most successful superfamily of Chapter 12, this volume), and aquatic/semi-aquatic the , as shown by an abundance of species (e.g. and ; see Chapters 16, 17, 22, and with a global distribution (Agnarsson et al. 2010; 23, this volume), although many species are not Sato et al. 2012). Ranging in size from tiny weasels restricted to one of these functional types, for ex- (Mustela nivalis, which may weigh 30 g or less) to ample, martens (Martes spp.) may be terrestrial. Ex- huge specialized sea otters (Enhydra lutris, >30 kg), ceptions to this rule, the -like (Gulo they may not have evolved to be as physically large gulo, see Chapter 18, this volume) and (see as members of other carnivoran families, but the ra- Chapters 13, 19, and 21, this volume), have shorter, tio of the smallest to largest is the ­greatest—a mas- robust bodies and relatively longer legs compared sive 1000:1 in body masses (Table 3.1). With around with those of other mustelids. However, mustelids 90 species, the Musteloidea is the most speciose are not equally successful globally. ­Although about superfamily (c.30% of carnivorans) and the Mus- 43% of smaller carnivoran species in the Americas telidae (>60 species; c.20% of carnivorans) the most and the Oriental region are mustelids, they com- speciose family of the Carnivora (Wilson and Mit- prise a mere 12% of smaller carnivoran species in termeier 2009; Hunter 2011; see Chapters 1 and 2, (Figure 3.1). Despite colonizing Africa from this volume). the Miocene alongside viverrids and herpestids The mustelids are mostly specialized predators (Hunt 1996), the only mustelids, apart from ot- that generally have a thin, elongated body plan ters, south of the Sahara all have black-and-white

Kitchener, A. C., Meloro, C., and Williams, T. M., Form and function of the musteloids. In: Biology and Conservation of Musteloids. Edited by David W. Macdonald, Christopher Newman, and Lauren A. Harrington: Oxford University Press (2017). © Oxford University Press. DOI 10.1093/oso/9780198759805.003.0003

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aposematic coloration (e.g. honey ­[Mellivora three to four species, differentiated by size and diet capensis], African striped [­ spp.], (usually fish versus crustaceans), per biogeograph- and African striped weasels [Poecilogale albinucha]), ical region (see Chapter 1, this volume). backed up by anal sacs producing noxious secre- The other musteloid families, (Mephiti- tions—perhaps the mustelids arrived a little later dae; see Chapters 24 and 25, this volume), , and only those mustelids packed with chemical , (; see Chapters 26, 27 weapons could muscle their way in. In contrast, and 28, this volume), and red pandas (; in the Palaearctic all small carnivorans are mus- see Chapter 29, this volume), are rather more eclec- telids with the possible exceptions of one or two tic and comprise fewer species, although procyo- marginal herpestids and viverrids, which may re- nids show greater diversity of form than mustelids, sult from human introductions. Otters are almost if they do indeed form a monophyletic family unique among carnivorans (the only exceptions be- (Koepfli et al. 2007; Koepfli et al., Chapter 2, this ing [Cynogale bennetti], and aquatic gen- volume). In contrast to the other families, red pan- ets ­[Genetta piscivora], among viverrids) in being das (Ailurus fulgens) have evolved as largely spe- adapted to aquatic environments; there are usually cialized vegetarians that show many evolutionary

Table 3.1 Body size of smallest and largest members of each musteloid family.

Family

Mustelidae Procyonidae Ailuridae

Number of species >60 11 14 1

Largest species Enhydra lutris Conepatus leuconotus lotor Ailurus (f.) styani Body mass (g) 45,000 4500 28,000 7500 HB (mm) 1200 510 620 730

Smallest species Mustela nivalis Spilogale pygmaea astutus Ailurus (f.) fulgens Body mass (g) 25 130 800 4500 HB (mm) 114 190 305 510

Ratio body masses 1800 34.6 35 1.7

Ratio HBs 10.5 2.7 2 1.4

100% 90% 80% 70% 60% 50% Non-mustelids 40% Mustelids 30% 20% 10% Figure 3.1 Proportion of small 0% carnivorans that are mustelids in different Nearctic Neotropical Oriental African Palaearctic biogeographical regions.

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parallels to the unrelated ( (Isaac 2005; Lindenfors et al. 2007). Sexual size di- melanoleuca). Procyonids and mephitids dominate morphism may be a consequence of sexual selection the Americas, but tend to be less carnivorous and in polygynous species for larger males that compete more omnivorous than sympatric mustelids. for access to oestrous females. Females may also In this chapter we review the form and func- be smaller than males so that their total energy re- tion of the musteloid carnivorans to discover the quirements are less than for males and so they can key adaptations that have helped the musteloids invest more energy in the development of young. in general and the mustelids in particular achieve Sexual dimorphism may also allow for a degree global success in terms of numbers of species and of niche separation between the sexes so that each geographical spread (see Macdonald et al., Chap- sex can prey on of different sizes, thereby ter 1, this volume). We begin with a discussion of minimizing competition. Clearly there is interplay primarily terrestrial and arboreal species, followed between these factors and considerations of popu- by specific adaptations for those species that live lation density, social behaviour, home-range size, partially or fully in aquatic environments. length of oestrus and energy use (Ferguson and Larivière 2004). There is not space here to discuss Sexual dimorphism further the causes and consequences of differential sexual dimorphism in musteloids but the theme is It is very apparent from external appearances that developed further in Macdonald et al., Chapter 6, there is a wide degree of sexual dimorphism in this volume, and in Noonan et al. (2016). musteloids. Although much has been written about Working from the outside in, let us take a closer the causes of sexual dimorphism in musteloids look at the adaptations of musteloids. (especially mustelids), there has been little inves- tigation as to the degree of sexual dimorphism in Hiding in plain sight—pelage coloration different musteloid groups. and markings Therefore, based on data in the literature, we es- timated sexual dimorphism in mean condylobasal Pelage has two main functions. First, pelage colora- skull lengths and mean body weights of the Melinae tion and markings enable many musteloids to re- (badgers), (polecats, weasels, and mar- main hidden from predators and prey. For example, tens), Lutrinae (otters), Mephitidae (skunks) and weasels and stoats (Mustela spp.) at high latitudes Procyonidae (raccoons and coatis) (Figure 3.2). The moult into white winter to match the snow in degree of sexual dimorphism in condylobasal skull contrast to the brown summer pelage. However, length (CBL) is less than that in body weight. This some markings may function in communication is not surprising since the former is a linear measure within and between species (see Buesching and whereas the latter is a cubic measure. However, even Stankowich, Chapter 5, this volume). Second, the so the pattern is consistent with both measures. The pelage ensures that musteloids are insulated to Mustelinae show a much higher mean sexual di- avoid excessive heat loss to (or gain from) the sur- morphism (1.71 body weight, 1.10 CBL) than other rounding environment. This is especially important musteloid groups, which tend to display similar de- for weasels and stoats in colder northern latitudes, grees of sexual dimorphism (1.3–1.38 body weight; and also otters living in the sea and exposed to cold 1.06–1.07 CBL) with the melines showing the least water for prolonged periods, owing to the high sur- sexual dimorphism (1.22 body weight, 1.05 CBL). face area to volume ratios of their elongated bodies What is striking from this preliminary analysis is (Kruuk 2006; King and Powell 2007). that the most carnivorous terrestrial musteloids, Most musteloids have a uniform coloration either the mustelines, show the highest degree of sexual all over or dorsally, with typically paler coloration dimorphism. ventrally, providing counter-shading to remain Causes of sexual dimorphism among carnivorans hidden in a wide variety of habitats. Although are often discussed and centre around the follow- most are brownish and dark, some, for example, ing themes, which may not be mutually exclusive Siberian (Mustela sibirica), Malay weasel

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(a) 1.12 1.11 1.1 1.09 1.08 1.07 1.06 1.05 1.04 1.03 condylobasal skull lengths Ratio of male to female mean 1.02 1.01 Melinae Mustelinae Lutrinae Mephitidae Procyonidae

(b) 1.8

1.6

1.4

1.2

1

0.8

body weights 0.6

0.4

Ratio of male to female mea n 0.2

0 Melinae Mustelinae Lutrinae Mephitidae Procyonidae

Figure 3.2 Sexual dimorphism in musteloids. a. Ratios of male:female body weights. b. Ratios of male: female condylobasal skull lengths. References: Abramov and Puzachenko 2005; Abramov and Tumanov 2003; Balharry et al. 2008; Begg et al. 2013; Birks and Kitchener 2008; d’Inzilla Carranza and Rowe-Rowe 2013; Copeland and Whitman 2003; Delahay et al. 2008; Dragoo and Sheffield 2009; Dunstone and Macdonald 2008; Elbroch 2006; Gittleman and Van Valkenburgh 1997; Gompper 1995; Gompper and Decker 1998; Heptner and Naumov 2002; Hwang and Larivière 2001, 2003, 2005; Jefferies and Woodroffe 2008; King and Powell 2007; Kinlaw 1995; Kitchener and Birks 2008; Larivière 1999c, 2001a, b, and c, 2002a and b, 2003a; Larivière and Walton 1998; Lindzey 2003; Lotze and Anderson 1979; Lynch and O’Sullivan 1993; McDonald 2013; McDonald and King 2008a and b; Meiri et al. 2005; Mendelssohn and Yom-Tov 1999; Monakhov 2011; Ohdachi et al. 2009; Pasitschniak-Arts and Larivière 1995; Redford and Eisenberg 1992; Reyes-Küppers 2007; Roberts and Gittleman 1984; Rosatte and Larivière 2003; Rozhnov and Abramov 2006; Somers and Nel 2013; Storz and Wozencraft 1999; Stuart and Stuart 2013; Van Gelder 1968; Vanderhaar and Hwang 2003; Verts et al. 2001; de Villa-Meza et al. 2011; Weckerley 1998; Wilson and Ruff 1999; Wisely et al. 2002; Youngman 1990.

(Mustela nudipes), Japanese (Martes melam- badgers ( spp., Arctonyx spp., Melogale spp., pus), Siberian­ or steppe (Mustela eversma- and Taxidea taxus), skunks ( spp., Conepatus nii), and black-footed (Mustela nigripes), are spp., and Spilogale spp.), marbled polecats (Vormela quite pale. Several have contrasting throat patches, peregusna), honey badgers, African striped polecats including martens, some (Eira barbara) and , and grisons ( ­individuals, and giant otters (Pteronura brasiliensis; spp.), which have mostly contrasting black-and- see Groenendijk et al., Chapter 22, this volume). white pelages, comprised usually of white spots ­Others have striking pelage patterns. These include and stripes, with the dorsum often paler than the

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ventrum. Procyonids often have banded tails and predators, or perhaps giving the impression of dark facial masks surrounding the eyes, as do red larger, more threatening eyes. However, they con- pandas, and polecats and ferrets (Mustela spp.). cluded that because facial masks are found mostly This contrasting coloration is generally interpreted in mesopredators that risk predation from larger as aposematic (Newman et al. 2005; Caro 2009; carnivorans, their facial masks probably have an Stankowich et al. 2011; Buesching and Stankowich, aposematic role to deter predators, being particu- Chapter 5, this volume). larly effective in low-light nocturnal conditions. Aposematic or warning coloration, coupled with Contrasting facial stripes in badgers, dark fa- anal sacs that deliver a powerful, noxious olfactory cial masks in procyonids and ailurids, and throat deterrent, has evolved six times within the muste- patches in martens may have a primarily social loids, demonstrating their value in effective deter- function in species recognition and/or to warn rence of potential predators of these mostly small predators or conspecifics of strong bites and sharp carnivorans. The highly contrasting black-and- claws, but their specific functions for each species white coloration of the skunks is well known, but is remain to be investigated. For example, the Euro- seen also in related stink badgers (Mydaus spp.), and pean badgers’ facial stripes have also been inter- among unrelated mustelids (e.g. preted as glare reducers, but other badger species [Lyncodon patagonicus], grisons, honey badgers, Af- (Meles spp.), may have less contrasting facial stripes rican striped polecats, polecats, ferrets, and mar- or even lack them, so further investigation of why bled polecats, Caro 2009; Stankowich et al. 2011). badgers have facial stripes is required. Banded tails Although visual displays of contrasting pelage in procyonids and ailurids probably function in patterns mostly warn potential predators of chemi- signalling aggression and other social behaviours, cal weapons, other mustelids, for example Old depending on their positioning, but in ringtails World badgers (Meles spp.), hog badgers (Arctonyx and (Bassariscus spp.), they have an ap- spp.), and American badgers (Taxidea taxus), have parently aposematic role, warning of noxious anal contrasting black-and-white head stripes that ap- gland secretions (Caro 2009). Black tail tips in stoats parently warn of ferocious retaliatory behaviour, if (Mustela erminea), and long-tailed weasels (Mustela attacked (Caro 2009). The mostly black-and-white frenata), appear to divert the attention of attacking honey badgers also combine ferocity with nox- birds of prey, causing them to miss and result in ious anal gland secretions. Although wolverines lower predation risk (Powell 1982; see also Buesch- are brown, they have contrasting pelage patterns ing and Stankowich, Chapter 5, this volume). and face masks that may signal that they are also fierce protagonists. Several species are sym- patric in parts of the Americas and it is likely that Keeping warm—pelage insulative similar aposematic coloration coupled with anal properties sacs, producing noxious secretions, is an example of Müllerian mimicry (Caro 2009). A similar pattern Although musteloids moult once or twice per year, is observed in Africa, where all known terrestrial depending on latitude (and the need for extra win- mustelids south of the Sahara (African striped pole- ter insulation), stoats, long-tailed weasels, and least , African striped weasel, and honey badgers) weasels may also undergo dramatic changes in col- show aposematic warning coloration and chemical oration from brown in summer to white in winter deterrents. (King and Powell 2007). The mechanism for seasonal Dark facial masks are common among procyon- moulting in higher latitudes is similar whether the ids (raccoons [Procyon spp.], coatis [ spp. and pelage changes coloration or not (Figure 3.3). Speed spp.]), red pandas, some mustelids (e.g. of pelage transition is affected by rate of day-length polecats and ferrets), and skunks. Newman et al. change, occurring in a few days in the Arctic and (2005) reviewed the possible functions of facial up to six weeks at lower latitudes. There are tran- masks in carnivorans, including as anti-glare de- sition zones between animals that turn white in vices, disruption of the face and hiding eyes from winter and those that do not, resulting in animals

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summer fur grows in brown

no inhibition decreasing light of MSH

increased melatonin induction of release from the spring molt pineal gland SUMMER

increased inhibition of prolactin prolactin levels release from the anterior AUTUMN pituitary release of inhibition on SPRING prolactin induction of winter molt

inhibition of melanocyte WINTER decreasing stimulating melatonin hormone (MSH) release from anterior pituitary

increasing no production daylength of melanin winter fur grows in white

Figure 3.3 Seasonal moult cycle of stoats and weasels. Reproduced from King and Powell (2007).

of variable pelage coloration. In stoats this occurs dense pelages (see Adaptations for aquatic living). between 52 and 56°N, in long-tailed weasels at Table 3.2 shows the seasonal differences in fur length 40°N in a 350 km-wide zone, and in least weasels at and density for contour hairs, guard hairs, and un- 59–60°N. King and Powell (2007) hypothesized that derfur of mustelids and ­Figure 3.4 shows length of mustelines that partially change coloration in transi- fur of various carnivorans. Autumn moult results tion zones are effectively hybrids between northern in pelages with much higher densities of underfur, populations with white winter pelage adapted to so that winter pelages may appear lighter than in snowier, colder winters and southern populations summer, for example in polecats, but this is differ- with brown winter pelage adapted to milder, less ent to changes in fur coloration shown by stoats snowy winters. and weasels, which involves the replacement of the Owing to their small size and elongated bodies, external guard hairs too. Wolverines’ guard hairs most mustelids at colder, high latitudes require thick resist hoar frost settling on them, so their fur does insulating pelages, and because of this high quality not become clogged with ice, while their underfur fur, have long been the target of the fur trade and fur stays dry (Ewer 1973; Quick 1952). Chappell (1980) farming (Harrington et al., Chapter 7, this volume). measured the insulation, radiation, and convection Otters, and especially sea otters, have exceptionally of small Arctic using models covered in

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Table 3.2 Pelage lengths, hair diameters, and hair densities of mustelids.

Summer Winter

Species Contour Contour Guard Guard Underfur Underfur Ratio Fur Locality Contour Contour Guard Guard Underfur Underfur Ratio Fur Locality Ref. hair hair hair hair hair hair G:U density hair hair hair hair hair hair G:U density length diameter length diameter length diameter (cm−2) length diameter length diameter length diameter (cm−2) (mm) (μ) (mm) (μ) (mm) (μ) (mm) (μ) (mm) (μ) (mm) (μ) (G) (U) (G) (U) Martes 19.3 105 11.4– 30–100 11.4 18 Moscow, 42–56 85.1– 29–50 25.9– 25–38 11.1–22.2 1:55.6 19,988 Buryatia 2 zibellina 16.6 Russia 114.7 114.7 Martes 23–27 100–150 11–12 15–16 1:4–5 36–38 75–90 22–22.5 14–15 2 martes Martes 25.1 112 13.2– 48–154 9.7 22 Caucasus 2 foina 19.9 Mustela 9.5 70 7.6–9 27–55 6 17 Pskov 9.8 84 8.8– 62–82 5.7 14 1:23 24,000 Vyborg, 2 nivalis and 9.4 Russia Gellenor, Russia; Turkmenia Mustela 13.9 102 9.9– 50–97 8.1 18 1:36.5 14,544 Moscow, 15.75 96 11.5– 55–98 9.1 14 1:27.1 19,232 Moscow, 2 erminea 12.1 Russia 13.7 Russia Mustela 30–35 50 117 43 112 26 20 1:19– 8500– 1,2 putorius 20 9000 Mustela 11.6 85 7.2– 50–67 6.8 18 Aska- 16.8 110 11.6– 82–111 8.8 13 Zaisan 2 evers- 9.8 nia Nova 14.1 manni Mustela 20.3 91 13.5 31 9.7 18 1:39.3 27,000 Tatar 2 lutreola Mustela 16.2 122 9.1– 35–94 10.2 19 1:20.6 29,000 Shangan- 35.0 106 25.2 86 18.0 14 1:14 8614 Sverd- 2 sibirica 15.3 da River lovsk Mustela 18–21 1:2– 3476– Sikhote- 27–31 1:3– 9866– Sikhote- 2 sibirica 25.9 4224 Alin, 34.7 13,696 Alin, Russian Russian Far East Far East Neovison 1:52.1 10,090 27 133 18.5– 47–123 15.1 15 1:54.8 9266 Saltyk- 2 vison 24.5 ovo 31/05/17 7:03 PM 2 2 2 2 2 3 2 3 2 3, 4 U rals Sakhalin W. Siberia 14,712 34,972 34,972 16,325 1:155 1:63.6 8 12 11 15.3 13.3 16.0 12.2 15.8 14.6 14.6 22.5 187 47.4 123.9 21.9 21.5 18.4 18.4 27.7 204 101 170 100.9 27.9 26.0 25.3 24.4 24.2 24.2 Azerbai - jan O xford 550 6660 70,000 80,000 41,332 164,662 58,000– 60,000– 26,413– + 1:80 1:9.1 1:100 1:10.3 . Williams et al. 1992 . 13 10 7.6–11.9 7.6 11.6 4.6–15.8 50–65 3.9–7.7 44–106 25 11.1 26.9 9.8– 8.2– 12.1– 75 149 11.9 19.5

Neovison vison Vormela - pere gusna Meles meles lutra Lutra lutra Lutra lutra Lutra lutra Lutra lutra canaden - sis E nhydra lutris D 4—T. et al. 2010; 3—Kuhn 1982; 2- Sokolov 1— H eptner and Naumov 2001; R eferences:

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1200 Terrestrial Semi-aquatic Marine

1000 ) 2 800 m

600

400 Fur density (hair s/m

200

0

Mink Figure 3.4 Fur density of mustelids Red Ermine Fur seals Sea River otter and other carnivorans. From Liwanag Phocid seals Mountain et al. (2012).

fur. He found that insulation is correlated with fur by allowing more scattering of light, the whiteness thickness and density, so that weasels and stoats are of the unpigmented hair may be enhanced, and sec- actually relatively poorly insulated compared with ondly, by trapping more air, the insulative proper- lemmings (Dicrostonyx torquatus and Lemmus sibiri- ties of the hairs may be increased. Interestingly, the cus, that have longer fur, 6.5–10.5 mm), and shrews lower shaft decreased in diameter in winter stoats, (Sorex spp., that have short, but unusually dense which Russell and Tumlison (1997) suggested could fur). However, insulation loss was more rapid with allow hairs to bend more easily in the wind to avoid increasing wind velocity in longer furred lemmings disruption of the fur and also to allow a greater den- (35% loss from 1 to 6m per s) compared with shorter sity of hairs for increased insulation. furred mustelids (25%), which may be partly due to Fur density is also correlated with buoyancy, be- fur layer compaction by wind pressure (Chappell­ cause the pelage traps air when animals dive un- 1980). Unlike other high-latitude mustelines, wea- der water (Fish et al. 2002). For example, sea otters sels and stoats cannot moult into long fur in the (Estes et al., Chapter 23, this volume) have the high- winter, because that would impede their locomo- est fur density of the aquatic/semi-aquatic muste- tion in burrows or under the snow, so their loids (1,188.8 per mm2), with a buoyancy force of high surface area:volume ratio means that to main- 0.94 N compared with a fur density of 803.12 per tain a body temperature of 39–40°C at rest in sum- mm2 and a buoyancy of 0.82 N for the North Ameri- mer, a requires twice as much energy can river otter, while the ’s fur den- at three times the cost as a lemming of similar size, sity of 338.45 per mm2 generates a buoyancy force and that in winter in Alaska it may have to generate of 0.41 N (Fish et al. 2002). six times the resting basal metabolic rate to main- tain body temperature (King and Powell 2007). Russell and Tumlison (1997) compared the sum- Musteloid sense organs and senses mer and winter guard hairs of Arctic mammals. They Eyes and vision found that in stoats and weasels in the upper shaft of the guard hairs the medulla width and number Mustelids have generally forward-facing eyes, but of air cells within the medulla increased from sum- not to the same degree as in felids. For example, do- mer to winter. This could have two effects; firstly, mestic ferrets (Mustela furo) have a binocular visual

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field of 80° and orbital convergence of 35.3° Com- high densities of photoreceptors in their retinae and pared with 120° and 65.4° For domestic cats ( adjacent ganglion cells (King and Powell 2007; Hef- catus) (Heesy 2004). Forward-facing eyes are advan- fner and Heffner 1992, below). tageous for judging distances, which is essential for A major problem for aquatic and semi-aquatic predators trying to catch prey or for arboreal spe- species is how to adjust to seeing in air and under cies when leaping. Conversely, laterally-facing eyes water, when the cornea cannot refract light enter- are better at detecting potential predators, so that ing the eyes. In otters and American mink (Neovison perhaps the smallest mustelids have an eye orien- vison) the iris sphincter muscles are well developed tation and degree of binocular vision that balances to squeeze the anterior lens, which forms a pro- the need to be effective predators as well as avoid- tuberance, to increase its curvature and increase ing predation themselves. light refraction when submerged (Dunstone 1993; Sunlight is 100 billion times brighter than over- Figure 3.5). cast moonless nights (Kirk 2006), so eye structure As in many other carnivorans, mustelids have and function varies considerably depending on three visual pigments in the photoreceptor cells preferred timing of daily activity. Nocturnal spe- of their retinae. For domestic ferrets these include

cies, for example, badgers, raccoons, ringtails, and a rod opsin, with maximum absorbance (λmax) of red pandas, have relatively larger and more curved 505 nm, a short (S) wavelength cone opsin with

eyeballs for collecting maximum light for the bright- λmax of c.430 nm and a medium-long (M/L) wave-

est retinal images, higher ratios of photoreceptors length cone opsin with λmax of 558 nm (Calderone to ganglion cells (i.e. summation), and increased and Jacobs 2003). The ferret’s retina contains about ratios of light-sensitive rods to cones than diurnal 1.3 million cones, but M/L cones outnumber S species. In contrast diurnal species, for example cones by 14:1. Sea otters have similar visual pig-

yellow-throated martens (Martes flavigula), have ments, but with slightly different λmaxs: rod op- increased visual acuity to resolve fine spatial de- sin 501 nm, S cone opsin 441 nm, and M/L cone tails through reduced retinal summation, reduced 545 nm (Levenson et al. 2006). Even though they eyeball size and curvature for larger retinal images, have cone opsins, musteloids are not trichromatic and increased cone:rod ratios. Cathemeral species, like humans and probably do not see colours as for example weasels, , otters, and such, but rely on cones to see in daylight when rod stink badgers, have intermediate eyeballs (Kirk visual pigments are bleached. Among procyonids, 2006). European polecats and Asian small-clawed (Potos flavus) and raccoons have mono- otters ( cinereus) have similar visual acuities chromatic cone vision (long wavelength [L] cones to each other both in and out of water, but humans (out of water) have visual acuities ten times greater than those of otters (Ewer 1973). Cornea Like many other carnivorans, musteloid eyes have a tapetum lucidum, a reflective layer of cells be- Iris sphincter muscle hind the retina, which reflects back any light that (contracted) misses the photoreceptors onto the retina, thereby enhancing sensitivity of nocturnal vision. American Ciliary muscle Lens ’ eyes have only a few layers of tapetal cells, (contracted) which contain little, haphazardly arranged reflect- ive material, suggesting a nonfunctional tapetum lucidum (Braekevelt 1989), but the domestic ferret does have a functional tapetum lucidium (Ollivier et al. 2004). Little has been recorded about pupil Vision in air Vision underwater (muscles relaxed) (muscles contracted) shape in musteloids, although weasels’ and stoats’ pupils close to horizontal slits (King 1989), which Figure 3.5 Cross-section through otter’s eye showing mechanism probably matches the horizontal visual streak of for accommodation under water. From Dunstone 1993.

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only) (Jacobs and Deegan 1992), consistent with ferret badgers (Melogale spp.), tayra, grisons, Afri- their nocturnal lifestyles, but diurnal coatis have can striped polecats, and smallest in fossorial and/ S and L cones. or social forms, for example badgers, where large Examining ganglion cell distributions in mam- ear flaps would be susceptible to injury under- mal retinae reveals how their eyes are adapted ground or in intraspecific agonistic encounters, and to being most sensitive to detecting predators or aquatic forms, for example otters, Lutrinae (Pocock prey in diverse environments. Weasels have a hor- 1920a, b, 1921b, c, 1926), where they could affect izontal visual streak with a maximum ganglion swimming and diving efficiency. Sea otters’ ears cell density of 17,895 cells per mm2, which is more open as slits, presumably lacking flaps that would than three times greater than that of domestic fer- affect streamlining and may risk thermal injury rets (that have ganglion cell densities up to 5,200 and excessive heat loss in cold high-latitude seas. cells per mm2, Henderson 1985). Thus weasels’ Honey badgers and stink badgers have ear flaps re- eyes have a low visual acuity (ability to resolve duced to thickened ridges of skin (Pocock 1920a), detail) of 2.2 cycles/degree and are most sensi- presumably to protect them against insect stings tive to detecting prey horizontally against the ho- and/or injury when digging. Fossorial species can rizon (Heffner and Heffner 1992, Figure 3.6). Sea close up their ears to prevent soil ingress while dig- otters also have a naso-temporal (i.e. horizontal) ging, and otters’ ears have valves to prevent water visual streak with an area of high ganglion cell ingress while swimming and diving. density of 4,000 cells per mm2 corresponding to There have been few investigations detailing the a much higher visual acuity, compared to that upper limits to hearing frequencies in musteloids of weasels, of 50–60 cycles per degree (Mass and (Table 3.3). The upper range for humans (c.20 kHz) Supin 2007; Figure 3.6). Humans have a similar is much lower than those recorded for musteloids. visual acuity of 67 cycles per degree (Heffner and As suggested for other predatory carnivorans (Ewer Heffner, 1992). 1973), the ability to hear high-frequency sounds al- lows musteloids to hear the high-pitched commu- nication of and other small mammals, and Ears and hearing thus detect their presence. For example, American Ear flap structure in mustelids appears correlated mink respond to ultrasound up to 40 kHz, which is with preferred habitat and behaviour. Ear flaps within rodents’ vocal range of frequencies (Powell are larger in the arboreal martens, smaller in ter- and Zielinski 1989). However, weasels can hear at restrial species, including mustelines, wolverines, even greater frequencies, presumably reflecting the

(a) (b) S D

90 Cells/mm2 60 3750 25% 75% 30 3000 50% T T N 2250 OD 1500 750 0

I 1 mm V

Figure 3.6 visual streaks of a. weasel and b. sea otter, showing horizontal area of high density of ganglion cells. Reproduced from Mass and Supin (2007) and Heffner and Heffner (1992).

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Table 3.3 Upper limits of hearing (kHz) in musteloids and humans. unknown in . The surface area of the VNO’s Sources: Gunn 1988; Kelly et al. 1986; Heffner and Heffner 1985; olfactory epithelium is very small (c.1.6 cm2), but Ghoul and Reichmuth 2014; Voigt et al. 2013; Wollack 1965. impulses from the VNO’s olfactory receptors are Species Upper limit Maximum sensitivity Octaves processed in a small discrete accessory olfactory bulb (0.15% of olfactory bulb volume), which is (kHz) (kHz) caudal and on the medial surface of the main ol- 38 1–16 7.1 factory bulbs of the anterior brain. The function Weasel 60.5 2 (range 1–16) of the ferret’s and badger’s VNOs is unknown, Ferret 44 8–12 5.3 but in other carnivorans it usually detects the Eurasian otter 30 4 reproductive status of individuals from scent se- cretions by detection of non-volatile ingredients River otter 35 16 in scent (either very long-chained fatty acids or Sea otter1 38 2–26 3.7 proteins, i.e. MUPs). 2 Sea otter 38 1.2–27 4.5 Van Valkenburgh et al. (2011) used CT scanning Human 20 1–4 8.5 to look at volumes and surface areas of turbinate 1underwater, 2aerial bones in carnivorans. The maxilloturbinates within noses warm and moisten inhaled air, while the ethmoturbinates bear most of the olfactory recep- higher-pitched vocalizations of their even smaller tors. Terrestrial musteloids have greater ratios of prey (Table 3.3). ethmoturbinate to maxilloturbinate surface areas Lower limits to hearing range from 200–300 Hz, (c.2–3), with wolverines having the largest ratio which is ten times higher than that of humans (c.0.2 (4–5), probably owing to their scavenging behav- kHz). Overall hearing ranges are not vastly differ- iour and need to detect carcasses. Interestingly, ent from those of humans, but are shifted higher aquatic and semi-aquatic musteloids evolved in- in musteloids. For example, human hearing ranges dependently much lower respiratory to olfactory over c.8.5 octaves compared with seven octaves or turbinate surface area ratios (c.0.5–0.8), suggesting less in musteloids (Table 3.3), which is less than for less reliance on olfaction, but this may also reflect some felids and viverrids and more than in canids the need for relatively larger maxilloturbinates to and ursids. prevent thermal loss from exhaled air by acting as counter-current heat exchangers. In water, aquatic mustelids lose body heat rapidly so preventing heat Smell and taste—detecting chemicals loss in this way may be an important adaptation Musteloids have a good sense of smell for detect- (we discuss adaptations to an aquatic lifestyle fur- ing prey and communicating using scent marks. ther towards the end of this chapter). Musteloids typically use the olfactory epithelium The mammalian sense of taste is through G on the turbinate bones of their noses, but some ­protein-coupled receptors (GPCRs) (Jiang et al. 2012). species, for example domestic ferrets and Euro- Sweet foods are detected by heteromers (combina- pean badgers, also have a vomeronasal organ tions of two different receptor subunits) of two type 1 (VNO), with an opening into the roof of the mouth GPCR taste receptors, i.e. Tas1r2/Tas1r3, and umami (Kelliher et al. 2001; Buesching and Stankowich, (savoury) flavours are mediated through Tas1r1/ Chapter 5, this volume). This is a paired olfactory Tas1r3. Bitter tastes are detected by type 2 GPCR re- organ, positioned in a cartilaginous capsule at ceptors, Tas2rs (Jiang et al. 2012). Cats cannot taste the base of the nasal septum, whose occurrence sweetness, because of pseudogenized (hence non- has been little investigated in musteloids. For functional) Tas1r2 genes that affect the Tas1r2 taste example, tayras exhibit flehmen (a characteris- receptors’ ability to respond to sweet foods. Among tic open-mouthed response to intraspecific scent mustelids functional Tas1r2 genes occur in domestic secretions, Ewer 1973), which usually involves ferrets and North American river otters, but non- the VNO in other carnivorans, but this is so far functional genes occur in Asian small-clawed otters

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(Jiang et al. 2012). Raccoons and red pandas also (on the cheeks), and unpaired interramals (on the have intact and active Tas1r2 genes, presumably re- throat) are important in preventing accidental in- lated to their omnivorous diets, but it is unclear why jury, especially to eyes, and allowing unimpaired carnivorous ferrets and North American river otters locomotion at night or in burrows. For example, the (Lontra canadensis) can taste sweetness. mainly terrestrial coatis have stouter vibrissae than arboreal kinkajous, which have only a single genal tuft (Pocock 1921a). Vibrissae are longer and more Touch abundant in predators, for example martens, mus- The most important tactile sensory organs in mus- telines, and striped polecats, compared with those teloids are their well-developed vibrissae (whisk- of fossorial Old World badgers, honey badgers, and ers). Musteloids mostly have the typical carnivoran striped skunks (Mephitis mephitis), which may dam- arrangement of vibrissae, with subtle variations re- age vibrissae while digging (Pocock 1920a, b, 1921c). lated to ecological niches (Figure 3.7; Pocock 1920a, Ferret badgers have many long whiskers, with the b, 1921a–c, 1926, 1928). Snouts are usually well submentals being unusually well developed, per- endowed with mystacial (muzzle) and submental haps for terrestrial foraging (Pocock 1921c). Vibris- (under the chin) whiskers, which are important sae are very well developed, abundant, and stiff in in foraging, especially when catching prey. Super- otters (Lutrinae, Pocock 1921b), for detecting prey ciliaries (above the eyes), lower and upper genals movements under water, but Congo clawless otters

(i) (a) (b)

(k)

(j)

(c) (d) (l)

(m) (n)

(e) (f)

(o)

(g) (h) (p) (q)

Figure 3.7 vibrissae of musteloids. a. Lyncodon patagonicus, b. Martes flavigula, c. Grison furax, d. Eira barbara, e. Ictonyx striatus, f. Melogale personata, g. Amblonyx cinerea, h. Hydrictis maculicollis, i. Taxidea taxus, j. Meles meles, k. Gulo gulo, l. Potos flavus, m. Mellivora capensis, n. Bassariscus astutus, o. Nasua nasua, p. Procyon lotor, q. Ailurus fulgens. From Pocock, 1920a, b, 1921a, b, c, 1926, 1928.

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(Aonyx congicus) apparently lack superciliary and forefeet are quite dexterous (see Paws and claws) upper genal tufts, presumably because their diet and well-endowed with touch receptors compared is richer in invertebrates (Harris 1968). European with those of coatis (Welker et al. 1964, Figure 3.9). badgers may lack upper genal tufts, although why Raccoons and humans have very similar abilities to tayras lack interramal whiskers is unclear. discriminate (by touch) between spheres differing Many musteloids have laterally projecting car- in diameter by only 0.53% (Welker et al. 1964). pal (wrist) vibrissae that appear to be important in prey capture (Figure 3.8). They are recorded in coa- tis, kinkajous, ringtails, olingos ( spp.), raccoons (poorly developed), red pandas (poorly developed), ferret badgers, European badgers, Pa- tagonian weasels, African striped polecats, mustel- ines, grisons, martens, and tayras (Pocock 1921a–c, D 1926, Figure 3.8). Carpal vibrissae are well devel- oped in predators, but (similar to facial vibrissae) 1 much less so in fossorial forms, which instead have 2 a swelling where the vibrissal nerve ends, for exam- 3 ple, honey badgers and American badgers, because 5 4 carpal vibrissae would be broken off while digging underground. The skin of mammals is usually well-endowed with touch receptors for sensing their environments, Figure 3.9 relative degree of enlargement of body subdivisions in the ventro-basal nuclear complex (Vb) of the dorsal thalamus of the but these have been hardly investigated in muste- brain of the raccoon, showing the importance of the manual tactile loids. Raccoons are renowned for apparently ‘wash- sense, which accounts for almost 50% of the Vb volume. From Welker ing’ their food or foraging in shallow water. Their and Johnson 1965.

(a) (b) (i) (j) (p) (q)

(c) (d) (k) (r) (s) (l) (e) (f) (m)

(o) (t) (u) (g) (h) (n)

Figure 3.8 The undersides of hind (left) and front (right) paws of musteloids. a. Eira barbara, b. Martes flavigula, c. Mustela putorius, d. Ictonyx striatus, e. Lyncodon patagonicus, f. Spilogale putorius, g. Mephitis mephitis, h. Mydaus javanensis, i. Hydrictis maculicollis, j. Aonyx capensis, k. Enhydra lutris, l. Meles meles, m. Taxidea taxus, n. Mellivora capensis, o. Gulo gulo, p. Nasua nasua, q. Procyon lotor, r. Potos flavus, s. Bassaricyon sp., t. Bassariscus astutus, u. Ailurus fulgens From Pocock 1920a, b, 1921a, b, c, 1926, 1928.

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Communication—scent glands American ­badgers’ anal sacs open into a protuber- ant anus and ­produce a sweet-smelling secretion. Musteloids communicate using visual displays (see Anal sacs are enlarged­ in honey badgers, grisons, Pelage coloration and markings) and vocalizations, ­African striped polecats, polecats, ferrets, Patago- but the most important channel of communication nian striped weasels,­ skunks, and stink badgers, is through scent marks from specialized cutane- and ­produce ­foul-smelling secretions, which are ous glands, although they frequently make use of squirted at ­potential attackers­ to deter them. Heidt urine and faeces that are free as waste products and Morgans­ (1982) examined anal sac histology in (see also Buesching and Stankowich, Chapter 5, five species of skunks, including Mephitis ­mephitis, this volume). Musteloids have a variety of scent M. macroura, Conepatus mesoleucus, Spilogale putorius, glands that produce secretions for marking home and S. ­pygmaea, and concluded that they are highly ranges and territories, but also for communicating enlarged and modified apocrine sweat glands. The other information, for example, individual, age, sex, walls of the anal sacs are made up of a keratinized aggression/territoriality, and reproductive state mucosal epithelium and layers of striated muscles, (Macdonald 1985). The principal scent glands of which are encapsulated by a thick fibrous layer of musteloids are anal sacs (often called anal glands), connective tissue. The papilla connecting the sac foot glands on foot pads and in interdigital cavi- to the anus has a similar histology and its lumen ties, ventral glands which open onto the abdomen closes up into a u-shape, presumably to prevent in front of or behind the genitals, and subcaudal inadvertent leakage of secretions. The mucosal glands that open ventrally at the root of the tail. layer of the anal sac and papilla are heavily kerati- Musteloids, especially mustelids and mephitids nized to withstand high pressures produced when (but with some exceptions), have well-developed anal sac secretions are forced out. Within anal sacs, anal sacs, which are paired glands that open via glandular tissue occurs in two to three lobes, some- ducts into the rectum either side of the anal ori- times subdivided into lobules (in some species) on fice (Macdonald 1985; Pocock 1920a, b, 1921a–c, one side. The noxious anal sac secretion is squirted 1926, Figure 3.10). Anal sacs are not enlarged vigorously via papillae at great pressure, either as in martens, wolverines, tayras, otters, badgers, a highly atomized mist, or mostly like rain drops, and stoats and weasels (except polecats and fer- and spread through an arc of 30–45°. rets), and, not ­surprisingly, are completely ab- Anal sac secretion is apocrine (secretions released sent in the aquatic sea otters. Old World badgers in membrane-bound vesicles from the surface of also have typical (non-enlarged) anal sacs, but secretory cells) and sebaceous (secretion (sebum) produced by the rupture of secretory cells) in ori- gin in most musteloids (Macdonald 1985). The sac comprises an inner sebaceous layer that produces waxy monoesters and an inner apocrine layer that produces an immiscible aqueous solution—both secretions are rich in sulphur-containing hydrocar- bons, for example thietanes and dithiolanes (dithi- acyclopentanes) in stoats, weasels, polecats, and American mink (although derived from a differ- ent biochemical pathway in mink). Different com- pounds are produced by the anal sacs of Eurasian otters (Lutra lutra), badgers, and martens. The apo- crine secretion is modified by anaerobic bacteria in the anal sac prior to use. For example, 2-piperidone is produced by anaerobic bacteria in the American mink, which also produces two sulphur-rich com- Figure 3.10 The anal sacs of the Patagonian striped weasel. From pounds that are common to eight other mustelid Pocock 1926. species (Sokolov et al. 1980).

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Some musteloids have unusual glands. Badgers the most extreme morphological constraints on (Meles spp.) and hog badgers (Arctonyx spp.) have ­musteloid skulls, while carnivory and omnivory subcaudal glands inside subcaudal pouches (Mac- favour some morphological overlap between some donald 1985; Buesching et al. 2002). Honey badg- ­members of different families (e.g. small predatory ers have a muscular and eversible anal pouch, and mustelines and mephitids). when everted it dribbles a suffocating anal sac se- Mustelids have the most distinctive and peculiar cretion (Pocock 1908, 1920a; Kingdon 1977). Mac- skull shapes of any carnivoran group (Ewer 1973; donald (1985) noted a bristle in the ratel’s anal sac Radinsky 1981), which include generally a short from Pocock (1920a), but this was added by the au- rostrum, elongated braincase with sagittal crest, thor to indicate a connection between sac and rec- short lateral profile with small orbits, and enlarged tum and is not an anatomical feature of this species. carnassials (P4/m1). Mephitids have similar skulls, American badgers have an abdominal or ventral although modified to their generally insectivorous gland, as do wolverines and martens, for marking diet (enlarged M1, well-developed crushing mo- branches and other objects. Tayras may possess a lars), while most procyonids have a longer rostrum, gland in a depression above the anus (Macdonald no sagittal crest, and a higher lateral skull profile. 1985). Some mustelines probably have chin or fa- Major skull modifications between and within these cial glands, which they rub on objects or each other, clades are closely linked to arrangements of masti- for example (Martes zibellina), fishers (Pekania catory muscles and diet. The temporalis, masseter, pennanti, after eating, drinking, or playing), Ameri- and pterygoideus muscles represent the main mas- can martens, long-tailed weasels, stoats, and ferrets ticatory complex for closing the jaws, while the di- (Macdonald 1985). Fishers and other martens have gastric muscle is involved in jaw opening (Turnbull plantar glands within whorls of hair on their hind- 1970). Where the temporalis and masseter muscles feet (Buskirk et al. 1986). are similar in size, this generally reflects a preda- Procyonids also have anal sacs and ventral tory lifestyle (i.e. small mustelines); otters have an glands (Macdonald 1985). Anal sacs are small in enlarged digastric. raccoons and cacomistles (Bassariscus sumichrasti), Predatory musteloids generally have a relatively but they are similar to those of , whereas coatis powerful bite force and there is an evolutionary ten- have anal sacs that open as a series of four to five dency for higher bite forces among mustelids; high parallel slits formed by folds of the anal epithelium bite force quotients (BFQs) characterize species that (Pocock 1921a). Otherwise scent glands are poorly kill prey larger than themselves (Christiansen and known among procyonids. Kaufmann (1962) noted Wroe 2007). Mephitids have the lowest BFQs, owing penile dragging in Nasua narica and A.C.K. has seen to insectivorous diets, while omnivorous procyonids this behaviour in N. nasua. This appears to be a form have BFQs similar to those of mustelids. So, how are of scent marking, which uses the males’ preputial powerful bite forces achieved by musteloids? Their glands (Shannon et al. 1995). Kinkajous lack anal skull architecture and dentition are very different sacs, but have abdominal, sternal, and mandibular to those of more specialized killers, the felids (Ewer glands on the lower lips and jaws, which they use 1973). The very thin zygomatic arches of the most for scent marking in trees (Pocock 1921a; Macdon- predatory—and smallest—mustelines­ ( and ald, 1985; see Brooks and Kays, Chapter 26, this vol- weasels) indicate very small attachment areas for ume). The has typical anal sacs, but the the masseter muscle complex, but this is counter- anal skin is also glandular and indented, similar to balanced by an elongated braincase, providing at- the anal pouches of (Pocock 1921a). tachment for anterior and well-­developed posterior temporalis muscles. The posterior temporalis mus- cle fibres produce maximum forces horizontally, Skulls, jaws and teeth—processing food when jaws are nearly closed. This system, with long, Skull architecture in musteloids varies in relation to straight upper canines, is very efficient for crushing diet and body size, although members of the same the necks and skulls of small rodents (Ewer 1973). clade tend to share similar cranial ­morphology The upper and lower canines of stoats and ­(Figure 3.11). Herbivory and piscivory impose weasels are frequently fractured, owing to high

03-Macdonald-Chap03.indd 113 31/05/17 7:03 PM 114 Biology and Conservation of Musteloids , r. , r.

Melogale , h.

Nasua narica , q. Meles meles (f) (l ) , g.

G ulo gulo , f. , f.

Procyon cancrivorus , p.

ira barbara E ira , e. (e) (k) Ailurus fulgens , o.

Pekania penannti Pekania , d.

G alitcitis vittata , n.

Conepatus chinga. , w. , w. (d) (j ) Martes americana

nhydra lutris E nhydra , c. , m.

Spilogale putorius , v. , v. Neovison vison , b.

Pteronura brasiliensis Pteronura , l. (i) (c)

Mephitis macroura

Mustela erminea , u.

Lontra canadensis Lontra

Potos flavus Potos , k. , t. (h) (b)

Mellivora capensis Mellivora , j.

Bassariscus sumichrasti , s.

Taxidea taxus Taxidea , i. (g) (a)

Figure 3.11 a. views of musteloid skulls. d orsal and lateral moschata Bassaricyon gabbii

03-Macdonald-Chap03.indd 114 31/05/17 7:03 PM Form and function of the musteloids 115 (r) (w) (q) (v) (p) (o) (u) (n) (t)

Continued (m) (s) Figure 3.11

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mechanical stresses in their canines (Van Valken- specializing on crustaceans or molluscs, where the burgh 2009; Meloro 2012). Robust glenoid fossae masseter muscle is more important for crushing (articulations on the skull for the lower jaw) prevent shelled prey (e.g. Aonyx, Enhydra) (Ewer 1973; Riley lateral mandibular (jaw) movements and may be 1985). Among procyonids, raccoons have a tempo- so tight that mandibles cannot disarticulate, as in, ralis with a higher weight relative to the masseter for example, European badgers. The mustelid jaw (60% vs. 15%, Gorniack 1986). The arrangement mechanism dissipates high stresses at the cranio- of the lines of action of jaw muscles suggests very mandibular articulation due to torque exerted by similar jaw movements of musteloids to those of masticatory muscles. The low, narrow skull profile typical carnivorans, with large vertical components of small predatory mustelids is difficult to interpret, and limited lateral movements (Turnbull 1970). Co- although Ewer (1973) suggested this is an adapta- atis and kinkajous have unusual skull architectures tion for hunting small prey in burrows. If so, the among carnivorans; coatis have the longest rostrum transition to a semi-aquatic lifestyle required rela- (snout) relative to braincase length among muste- tively simple skull changes. Otter skulls are similar loids, which is related to their omnivorous lifestyle in shape to those of weasels, with a long braincase and elongated rhinarium (hairless surface around and narrow, low lateral skull profile, although ot- the nostrils), which they use to search for food on ters have a more expanded basi-occipital area for the ground. In comparison, kinkajous are specialist attachment of powerful neck muscles (Lee and Mill herbivores that are peculiar outliers within the Car- 2004). Otters also have relatively weak zygomata, nivora and Procyonidae, owing to their very tall, indicating the greater importance of the tempora- globular skulls, with large orbits and high, straight lis muscle (for closing and pulling back the man- nasals. Some of these features occur also in red pan- dible), although its relative weight is less in otters das, but are less well developed (see Box 3.1).

Box 3.1 Red panda

Red pandas (Hu et al., Chapter 29, this volume) show re- to accommodate the temporalis muscles and provide ori- markable convergent evolution with giant pandas. This has gins for the masseter muscles for chewing a tough diet. The led to consistent confusion as to which family the red pan- mandibles are also robust with large condyles, tall rami, and das should be placed in. They have been variously treated as robust coronoid processes, reflecting the highly developed procyonids or in a separate family with the giant panda or in jaw musculature ( 2011). their own family, the Ailuridae (Pocock 1939; Kundrát 2011). Red pandas also posses a well-developed radial sesamoid Molecular phylogenies have established that red pandas are (often known as the ‘panda’s thumb’), which articulates in their own family, but they are a sister family to either pro- with the scapholunar bone of the wrist and has four mus- cyonids, mephitids, or a clade composed of mustelids and cles attached to it (see figure). The radial sesamoid assists procyonids (Kundrát 2011; see also Koepfli et al., Chapter 2, with holding bamboo stems while feeding. Although super- this volume). ficially similar to the even larger radial sesamoid of giant Morphological convergence with giant pandas is related pandas, its structure and ontogeny are quite different (Antón to their diets. Red pandas are unique among the musteloids, et al. 2006; Endo et al. 2001). There are different interpreta- because they are highly adapted to feeding on bamboo, al- tions of its anatomy; Endo et al. (2001) suggest that it acts though their overall diet is omnivorous (Fisher 2011). Like as a supporting ridge to help grasp bamboo stems, while giant pandas, Ailuropoda melanoleuca, red pandas have Antón et al. (2006) claim that the radial sesamoid and its well-developed premolar and molar teeth with accessory associated musculature affect the supination of the forearm cusps that create elaborate crowns for crushing bamboo (outward rotation) and adduction of the palm (moving to- shoots and leaves (Fig. 3.11), and a high arched skull for the wards the body), which is probably linked to efficient loco- attachment of well-developed temporalis muscles for a pow- motion along thin branches. It is this exaptation that allows erful grinding action (Fisher 2011; Figueirido et al. 2012). today’s red pandas to grasp slender bamboo stems for feed- The zygomatic arches are well developed and widely flared ing (Antón et al. 2006). continued

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Box 3.1 Continued

Abductor digiti I brevis and Oppones digiti I Flexor digitorum brevis manus Radial sesamoid Pisiform Tendon of Abductor digiti I longus Flexor retinaculum

Box, Figure 3.1 The radial sesamoid complex of the red panda. From Fisher 2011.

The numbers and form of musteloid teeth vary much shorter than M1, which is extremely long and ­considerably between clades and reflect feeding thick. The first upper molar (M1) varies consider- adaptations. Dental formulae are given in Table 3.4 ably between clades, so that in mustelids and me- and examples of dentitions are in Figure 3.12. Typi- phitids it is generally rectangular (more developed cally, procyonids retain the complete upper den- and larger in insectivorous skunks and badgers), tition of the (I3, C1, P4, M2), but the while in procyonids it is triangular and resembles lower jaw lacks the third molar. Carnassials have that of canids. Owing to this broad variation in evolved according to diet, so that predatory forms, tooth form and function, musteloids (and mustel- for example Mustela spp., spotted skunks (Spilogale ids in particular) are the most ‘polymorphic’ group spp.), and wolverines, have sharp, elongated teeth. among carnivorans (Crusafont Pairó and Truyols- Omnivorous badgers have a well-developed M1, Santonja 1957). Just as omnivory and carnivory owing to a very elongated crushing area, but P4 is are generally reflected in the relative proportions

03-Macdonald-Chap03.indd 117 31/05/17 7:03 PM 118 Biology and Conservation of Musteloids

AQ1 Table 3.4 Dental formulae of musteloids, adapted from Ewer (1973).

Taxon Incisors Canines Premolars Molars Total teeth

Mustelidae Mustela I3/3 C1/1 P3/2–3 M1/2 32–34 Poecilictis same same same same same Ictonyx same same same same same Taxidea same same same same same Martes I3/3 C1/1 P4/4 M1/2 38 Gulo same same same same same Meles same same same same same Arctonyx same same same same same Lyncodon I3/3 C1/1 P2/2 M1/1 28 Poecilogale same same same same same Mellivora I3/3 C1/1 P3/3 M1/1 32 Lutrinae I3/3 C1/1 P3–4/3 M1/2 34–36 Enhydra I3/2 C1/1 P3/3 M1/2 32 Galictis same same same same same Eira same same same same same Mephitidae Conepatus I3/3 C1/1 P2/3 M1/2 32 Mephitis I3/3 C1/1 P3/3 M1/2 34 Spilogale same same same same same Mydaus I3/3 C1/1 P3/4 M1/1 34 Procyoni- same same same same same dae Procyon I3/3 C1/1 P4/4 M2/2 40 Nasua same same same same same Nasuella same same same same same Bassari- same same same same same cyon Bassariscus same same same same same Potos I3/3 C1/1 P3/3 M2/2 36 Ailuridae Ailurus I3/3 C1/1 P3/4 M2/2 38

of crushing versus slicing areas of the teeth of ter- premolars evolved to crush tough exoskeletons of restrial musteloids, semi-aquatic otters have modi- molluscs and crustaceans (see Estes et al., Chap- fied dentitions in relation to aquatic diets. Sea otters ter 23, this volume). (and also clawless otters, Aonyx spp., to some ex- Musteloid dental forms are broadly correlated tent) have highly-developed molar crushing areas with jaw functionality and mandibular shape in both upper and lower premolars and molars. (Crusafont Pairó and Truyols-Santonja 1957; Meloro These bunodont molar teeth and highly-molarized et al. 2011). Small predatory mustelines have thin,

03-Macdonald-Chap03.indd 118 31/05/17 7:03 PM Form and function of the musteloids 119 , i.

Procyon , r. , r.

Conepatus chinga (f) (l) , q.

alitcitis vittata, h. Meles meles h. G alitcitis vittata, , g.

G ulo gulo Spilogale putorius , f. , f. , p.

ira barbara E ira (e) (k) , e.

Mephitis macroura , o.

Pekania penannti Pekania , d. nhydra lutris E nhydra , n. (d) (j)

Ailurus fulgens. , w. , w. Martes americana , c.

Pteronura brasiliensis Pteronura

Potos flavus Potos , m. , v. , v.

Neovison vison (c) (i) , b.

Lontra canadensis Lontra

, l. Bassaricyon gabbii , u.

Mustela erminea

Mellivora capensis Mellivora , k. (b) (h)

Bassariscus sumichrasti , t.

Melogale moschata

Nasua narica , j. , s. (a)

(g) Figure 3.12 a. u pper left dentition of musteloids. taxus Taxidea cancrivorus

03-Macdonald-Chap03.indd 119 31/05/17 7:04 PM 120 Biology and Conservation of Musteloids (r) (q) (w) (p) (v) (o) (u) (t) (n)

Continued (m) (s) Figure 3.12

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curved mandibles with well-developed lower car- locomotory forces transmit through the tarsals nassials, and relatively high, straight ramus (pos- and carpals, metapodials (metatarsals and meta- terior jaw that articulates with the cranium) for carpals—the long bones that connect the digits to the attachment of the temporalis; have the tarsals/carpals), and phalanges (digital bones), a thicker corpus (body of the jaw which the rather than just the phalanges as in digitigrady. teeth) and long crushing molar areas, so that cor- For this reason musteloids tend to show relatively pus thickness is even more pronounced posteriorly, longer propodial elements (bones forming the up- providing a larger area for masseter attachment, per segment of the limb) compared to metapodial while piscivores have short, anteriorly projected elements (Taylor, 1989; Van Valkenburgh, 1987). rami to optimize hydrodynamic skull shape The morphology of paws and claws is broadly (Bininda-Emonds and Gittleman 2000; Meloro and similar among musteloids. Many have enlarged O’Higgins 2011). The mandibles of red pandas and strong claws on their forepaws for digging, for ex- kinkajous show adaptations for herbivory, includ- ample, honey badgers (32–46 mm long, cf. 10–18 ing high condylar and coronoid processes, and mm on hind paws), European badgers (30–35 mm well-developed angular processes, which provide along the curve), and also ferret badgers, hog badg- greater attachment surface areas for both tempo- ers, American badgers, skunks, and stink badgers ralis and masseter muscles (Figueirido et al. 2010, (Pocock 1920b, 1921c, Figure 3.8). Terrestrial forms, 2012; Meloro 2011). for example, coatis, skunks (but less so in Spi- logale spp.), grisons, African striped polecats, and Locomotion ­Patagonian striped weasels, have long, powerful, slightly-curved blunt claws on their forepaws, with Paws and claws webbing up to the proximal ends of the digital pads (Pocock 1921c, 1927) as adaptations for digging for Musteloids have pentadactyl (five-digit) limbs food. Kinkajous, olingos (Bassaricyon spp.), ringtails and show none of the specializations evident in ­(Bassariscus astutus), and martens have similar paws, other carnivorans, which have resulted in reduc- but their claws are shorter, more curved and sharper tions of numbers of phalanges. All musteloids pos- for climbing (Pocock 1921a, Figure 3.8). Mustelines sess feet (Andersson 2004), although have shorter more curved claws for gripping, even certain groups tend to exhibit a semi-digitigrade though they are mostly terrestrial (Pocock 1921c). stance when moving (e.g. weasels, otter, badgers; The claws of martens, wolverines, fishers, and Polly and MacLeod 2008, Table 3.5). In plantigrady, ringtails are semi-retractile, presumably to prevent them becoming blunt when not used for climbing Table 3.5 Digitigrady and plantigrady in musteloids (Carrano 1997). (Harris and Ogan 1997; Poglayen-Neuwall and Toweill 1988). High-latitude species have heavily Plantigrade Semi-plantigrade Digitigrade furred pads, so that effective foot size is increased Eira Gulo Mustela for walking on snow without sinking. Wolverines Galictis Martes Vormela are renowned for these snowshoes, which are able Mellivora Lyncodon to bear a load of 27–35 g.cm−2, so that they can move Meles Poecilogale Arctonyx Poecilictis on crusty snow and easily kill much larger reindeer Melogale Ictonyx (Rangifer tarandus) or caribou (R. t. caribou), which Mephitis sink into the snow (Pasitschniak-Arts and Larivière Mydaus 1995). However, sable also have furred foot pads, Taxidea and stoats develop these in winter. Red pandas Lutrinae Procyon have fully furred pads, which are thought to allow Nasua better grip on wet branches (Pocock 1921a). Bassariscus Most mustelids have some webbing between the Bassaricyon toes, but semi-aquatic (Mustela lu- Potos treola) and otters have well-developed interdigital

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webbing, reaching near the distal end of the distal grip using a single-handed converging grip (Rensch phalanges (Pocock 1921b, c, Figure 3.8). Interest- and Ducker 1969; McClearn 1992). Coatis are good ingly, the American mink has no more interdigital at digging and shredding, and hence have little webbing than other terrestrial mustelids, but typi- need of manual dexterity, whereas arboreal kinka- cally swims and dives (Dunstone 1993; Harrington jous do, when foraging. et al. 2012b; Bagniewska et al. 2015). Otters’ toes are Some non-piscivorous otters (Aonyx spp., Lutro- also relatively longer to increase the area of webbing gale perspicillata, and Enhydra lutris) detect and catch for propulsion when swimming (Pocock 1921b). most of their food using forepaws. Like raccoons, Sea otters are most highly adapted to an aquatic these otters can roll food or other objects between lifestyle. Digits of the hind feet are united into a flip- two paws, exercising fine motor control of their per-like arrangement and fused to the ­distal-most digits for manipulating difficult food items such as phalanges, so that the digits do not appear seg- molluscs and crustaceans (Radinsky 1968). Sea ot- mented externally (Pocock 1928). Furthermore, the ters are renowned for using stones against which length of the phalanges of the sea otters’ hind feet they crack open hard-shelled prey. are reversed in order relative to most other mustel- ids with the longest digit in the outer fifth position. Skeletons and locomotion In Asian small-clawed otters webbing extends only to the proximal ends of the digital phalanges and Musteloids have the widest repertoire of locomotory African clawless otters have similar hindfeet. For adaptations within the Carnivora, including dig- many of these otters, webbing is reduced only until ging, climbing, swimming, and walking, which are the distal first phalanges on the forefeet, freeing the represented across a broad range of taxa. Therefore, shorter digits to allow manipulation of mollusc and skeletal form and function vary considerably within crustacean prey. As their names suggest clawless and between musteloid clades. However, a signifi- otters lack claws on their forefeet, and have only cant phylogenetic signal occurs in the long bone small flattish nails on the third and fourth digits of proportions of carnivorans (Samuels et al. 2013), so their hindfeet (Pocock 1921b). that musteloid skeletons are adapted for particu- Martens, procyonids, and red pandas use their lar locomotory behaviours, but within constraints foot pads and sharp, curved claws for climbing. of shared ancestry. Bertram and Biewener (1990) Red pandas have an enlarged radial sesamoid to identified isometric patterns of limb length in mus- aid their grip in climbing and for holding bamboo telids and procyonids. With their relatively small stems (see Box 3.1). body size and elongated body shape, this isometry Raccoons forage in shallow water and appear to was interpreted as size-­dependent change in limb ‘wash’ their food. Their forepaws are adapted for posture. For these animals, bone length and depth high manual dexterity with long claws and naked increase with body mass to maintain similar peak pads that lack interdigital webbing (Pocock 1921a), stresses in limb skeletons. Similarly, Heinrich and which leave the digits unencumbered when ma- Biknevicius (1998) identified strong positive allom- nipulating prey. Iwaniuk and Whishaw (1999) stud- etry in bone robusticity of different mustelids, rang- ied northern (or common) raccoons’ (Procyon lotor) ing from Mustela to Gulo. This trend was stronger in ability to manipulate food and found they were humeri than in femora, because of higher mechani- not especially dextrous, compared with kinkajous, cal stresses in the anterior body related to a scan- olingos, and non-piscivorous otters (see following sorial (climbing) mode of locomotion. However, paragraph), but were more dextrous than ringtails skunks (Mephitis mephitis and Spilogale putorius) ex- and coatis (Ewer 1973; McClearn 1992). Raccoons hibit similar scaling patterns in fore- and hindlimbs cannot grasp objects like primates, but grip food due to their generalized modes of locomotion between two forepaws, as a scissor grip between (mostly slow walk and gallop). More recently, Fabre digits of the same hand, and between apical digits et al. (2013a, b) showed that body mass has a signif- and carpal pad (Iwaniuk and Whishaw 1999), while icant effect on forelimb bone shape in musteloids. sitting or standing bipedally. Kinkajous and olingos Humerus and radius shapes appear to be better

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adapted for load bearing than the hindlimb bones, to the femoral head that tracks the attachment of although other factors, such as locomotory behav- the gluteus maximus muscle) and a relatively en- iour (including grasping ability) strongly interact larged, rounded femoral head. These features are with size and shape evolution (Andersson 2004). associated with well-developed hindlimb muscles Van Valkenburgh (1987) noted that arboreal car- that allow strong propulsion in half-bounding. As nivorans have significantly smaller body masses the spine flexes and extends, mechanical stresses than all other species, hence many musteloids on fore- and hindlimbs alternate. The gluteus mus- would be expected to climb trees. However, the cle complex is strongly involved in the propulsive smallest musteloids, weasels and stoats, are gener- phase, as seen also in the (Galictis ally terrestrial (although stoats are agile climbers, cuja, Ercoli et al. 2012). Weasels and grisons have see King et al., Chapter 10, this volume). Many an expanded lumbar region and strong develop- musteloids have scansorial adaptations (e.g. mar- ment of muscles responsible for tarsal joint move- tens, raccoons, and coatis), but the most specialized ments as adaptations for chasing prey in burrows, climbers are red pandas, ringtails, and kinkajous. using powerful hindlimb movements. In the fore- The most distinctive skeletal adaptations occur in limb, the humerus and radius–ulna complex are aquatic otters that are considerably different from relatively thin and gracile (Fabre et al. 2013a) and all the other carnivorans in the proportions of their limited in their movements along a vertical plane hindlimbs, which are adapted for different modes as expected for generally cursorial (running) car- of swimming propulsion (e.g. paddling or rowing, nivorans (Taylor 1989). Large mustelids with rigid Samuels et al. 2013). Digging musteloids have ad- backbones, for example badgers, trot or gallop and aptations that characterize the closely related, but do not bound. The larger scansorial martens share distinct, tribes of badgers (Melinae, Taxidiinae, and weasels’ morphological modifications in the lum- Mellivorinae) and the distantly related skunks, like bar region, where strong interspinous muscles at- Conepatus (Dragoo and Sheffield 2009). tach for efficient bounding or half-bounding (Salesa Previous interpretations of skeletal variation et al. 2008). Tree climbing requires very stable el- in mustelids supported a continuum in locomo- bow joints, so that humeri appear elongated with a tory modes and hence morphological adaptations reduced lateral epicondyle at the distal epiphysis. (Holmes 1980). Musteloids appear to have evolved The ulna is also characterized by a short olecranon skeletal morphology in a mosaic fashion. Look- with a large attachment area for the triceps brachii, ing at the first piece of mosaic in terrestrial muste- a muscle that extends the forearm for propulsion up loids, weasels move using the sinuous half-bound trees (Schutz and Guralnick 2007). Enlargement of (Taylor 1989). This is a form of gallop, where one the lesser trochanter of the femur allows efficient ro- forefoot touches the ground, closely followed by tation of the hip. Raccoons and coatis can climb and the other one, and the hindfeet touch the ground their skeletons share with martens modifications of together (Taylor 1989). Such a pattern is typical of the forearm apparatus (especially the trochlear rim carnivorans with elongated, thin bodies and short morphology; part of the elbow joint articulation) fore- and hindlimbs (Ewer 1973; Williams 1983b). but not the hindlimb (Heinrich and Rose 1997). Many mustelids with long, arching backs and short Most musteloids walk with symmetrical ambu- legs go from walking to bounding without trot- latory gaits, where each foot is on the ground for ting. Musteloids that bound or half-bound extend more than half the duration of a stride (Taylor 1989). and flex their vertebral columns to increase stride Some musteloids such as the omnivorous raccoons length, so vertebral columns are more flexible and and striped skunks only walk, and do not use ad- lack the heavy dorsal spines of gallopers. Conse- ditional gaits. Consequently, their skeletal morphol- quently, the back and abdominal-wall muscles are ogy is generalized, allowing a broad range of lateral well-developed in bounders, forcefully extending movements in both fore- and hindlimbs. Raccoons and flexing the back while running. Schutz and abduct their limbs more than those of cats and dogs, Guralnick (2007) noted that weasel femora have and their limbs do not move in the parasagittal an expanded gluteal tuberosity (a ridge posterior plane. Raccoons’ scapulae are inclined on the thorax

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at an angle of c.20° and supported by the clavicles, less specialized hindfeet to shift loose soil back- in contrast with cursorial species, such as , wards (Taylor 1989). Not surprisingly, the forelimb whose scapulae are perpendicular to the ground skeleton and muscles are well developed in fosso- and lack clavicles (Taylor 1989). Clavicles act as rial mustelids, which tend to have relatively large struts in raccoons to prevent shoulders compress- body masses. Van Valkenburgh (1987) and Samu- ing the thorax, especially when climbing. However, els et al. (2013) noted that the midshaft of the long thorax shape and humerus orientation determine bones of both fore- and hindlimbs of diggers are shoulder movements as much as the presence/ab- highly robust. This robusticity is related to bulky sence of clavicles. In raccoons the thorax widens muscles needed to generate high forces, especially sharply to splay the scapulae. Sea otters lack a clavi- at the shoulders (Taylor 1989). Consequently, badg- cle, which increases flexibility around the shoulder ers’ scapulae appear thick, with enlarged poste- for grooming and swimming (Taylor 1989). rior flanges for the attachment of the teres major A broad range of movements also influences the (a muscle that abducts and stabilizes the humero- hips and hindlimbs, so that femora appear to articu- scapula complex). Badger humeri are massive, late with a long, inclined fovea capitis (attachment with large heads, short shafts and heavy flanges of the ligament on the femoral head). Femora project for insertion of several muscles, for example the laterally and the articular cartilage in the acetabu- pectoralis, deltoid, latissimus dorsi, and teres ma- lum (hip joint articulation) of the pelvis is medial, jor. Distal epiphyses and medial epicyondyles are allowing much greater limb adduction when climb- enlarged, increasing areas of origin for manual ing or moving over uneven ground, whereas in cats and digital flexors, while lateral epicondyles are and dogs the femoral articulation is centred on the reduced. Such modifications are accompanied by acetabular (depression in acetabulum where long olecranon processes that support triceps mus- the ligament from the femoral head attaches to the cles for generating powerful digging forces at the pelvis) (Taylor 1989). In skunks, van de Graaff et al. distal ends of forearms (Van Valkenburgh 1987; (1982) noted how the femoral long axis intersects Taylor 1989). Humeri are supported internally by with the parasagittal plane at a relatively large angle well-developed trabeculae to resist forces while (25–40°), thus allowing a wide stance and femoral ab- digging. The deep trochlea adds stability and pre- duction. Schutz and Guralnick (2007) found no par- vents lateral displacement of forelimbs while dig- ticular modifications in the shape of the epiphyses of ging. Forces produced by the triceps are related to the humerus, ulna, femur, and tibia of ambulatory olecranon length on the ulna, which is longer in skunks, and concluded that their morphology is gen- diggers, giving a greater lever arm. For example the eralized and overlaps with that of other locomotory in-lever:out-lever ratio in non-diggers is 1:6 in mus- categories. Ankle movements are greater in skunks telids, but in diggers it is 1:3.5. American badgers’ compared with cats, and the primary ankle extensors ulnae have a cross-sectional shape similar to that of produce greater forces through a wider range of an- an I-beam, but the direction of forces is restricted gles than in cursorial carnivorans. This suggests the to the plane of the deepest part of the ulna, pro- skunks’ adaptations for ambulatory locomotion are viding maximum structural stiffness and strength. ancestral, as noted also in the study of their relative Radii are short and robust, with wide distal ends long bone proportions (Samuels et al. 2013). to articulate with scapho-lunars. European badg- Fossorial musteloids are scratch diggers (Tay- ers’ forefeet are digitigrade and carpi can hyperex- lor 1989) and include true burrowers (the honey tend by only 10°, but American badgers, which are badgers, Old World badgers, American badgers, more plantigrade, can hyperextend their carpi by and hog badgers) and burrow modifiers (the stink 50° (Taylor 1989). Hindlimbs are used in digging to badgers and ferret badgers). American badgers cut push back loose soil. Hence, fossorial musteloids’ through soil with the claw tips of their forefeet, femora have short necks and large attachments for which they use alternately. They may even rest the gluteus maximus and iliopsoas, while tibiae are their head against the opposite side of the burrow curved at the shaft to provide a larger surface for to gain extra purchase while digging, and use their hindfoot muscle attachment.

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Some musteloids are arboreal to different de- Forelimbs appear to sustain higher biomechanical grees. Taylor (1989) described three principal ar- stresses in arboreal compared with terrestrial lo- boreal locomotory modes, including horizontal comotion, although this may depend on the kind walking (e.g. red pandas), vertical looping (e.g. of locomotion. Owing to the high importance of ringtails), and jumping (e.g. martens and ring- supination (outward rotation of the forelimb), ar- tails). In horizontal walking, pads, claws, and a boreal musteloids’ scapulae and humeri are modi- high supinatory stance (limbs rotated outwards fied. For an effective and enlarged attachment of laterally) allow better grip and sufficient friction the teres major and subscapularis minor muscles, between feet and tree branches. Vertical looping re- red pandas, but also raccoons and coatis to a lesser quires coordinated actions of hind- and forelimbs extent, have a postscapular fossa on the scapula; for up-and-down vertical progression, while jump- the subscapularis muscle inserts on the head of the ing is much commoner among musteloids. Long humerus, where it prevents the humerus pulling jumps of up to 10 metres are recorded for martens away from its articulaton when climbing (Davis (Taylor 1989). Increased friction through paw pads 1949, Figure 3.13). The postscapular fossa is poorly is needed for vertical climbing, but as increasing developed in ringtails, which leap and jump body size overcomes friction, tree-climbers just around between branches, but it is very well devel- have to hang on. Red pandas use sharp recurved oped in very heavy bears, where the loads on the claws, but larger animals supinate (turn or rotate humerus are much higher. This adaptation is also outwards) their fore and hind limbs. When climb- well developed in arboreal kinkajous where the ing horizontally, the whole body is kept close to the postscapular fossa is large and its triangular sur- branch, but in vertical climbing the upper body is face extends caudally. Also in kinkajous, the distal closer. Ringtails may climb using vertical looping humeral epiphysis has a thin, long trochlea with or shinning, where fore- and hindlegs are moved a well-developed lateral condyle for attaching the separately from each other, but in unison, so that manus flexor muscles thus allowing better grasping the back is stretched and flexed, allowing ringtails ability (cf. diggers, Taylor 1989; Fabre et al. 2013b). to creep along tree trunks and branches. Therefore, The ulna has a short olecranon, ensuring limited even though being terrestrial imposes constraints lateral movements and greater supinatory stabil- on musteloid skeletal functional morphology, ar- ity. Pronation-supination (rotation about the long boreality requires an even narrower set of adapta- axis) is also favoured by the radial epiphysis, tions of whole body form and function. Arboreal which shows strong torsion (twisting) compared musteloids, such as martens, ringtails, and red with the distal one, a highly derived character only pandas, have long tails that generally act as bal- shared by kinkajous and coatis (Salesa et al. 2008). ancing organs, or possibly even as parachutes, The feet of jumping and leaping musteloids are when leaping. Kinkajous and , (Arctictis not as modified as scansorial species’, where the , a viverrid), the only carnivorans with a feet do the gripping (Taylor 1989). Wrist move- prehensile tail, have relatively long proximal cau- ment is considerable in scansorial species, which dal regions, both in overall length and number of have large radial sesamoids and pisiforms associ- caudal vertebrae, and more robust distal caudal ated with large radial and ulnar deviations. The vertebrae with expanded transverse processes, metacarpals are short, but the proximal phalanges compared with those of other arboreal carnivorans are long. The first metacarpal has a distinct waist (Youlatos 2003). These adaptations are associated and the proximal articular surface allows a high with enhanced flexion–extension of the proximal degree of adduction to grip branches more effec- tail and increased strength and flexing ability of the tively. Hindlimbs are also adapted for arboreality, distal tail, and are similar to those found in woolly because they must hold on, if the forelimbs lose (Lagothrix spp.), spider (Ateles spp.), and howler their grip. There must be sufficient joint mobility monkeys (Alouatta spp.). Van Valkenburgh (1987) to allow supination for different branch diameters. also listed other typical modifications for arboreal- Ringtails and kinkajous have ankle joints that are ity, such as elongated phalanges relative to carpals. fully flexible at the talo-crural joint, so they can be

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(a) (b)

(c) (d)

Figure 3.13 Postscapular flanges on the scapulae of arboreal musteloids. a. raccoon, b. , c. kinkajou. © National Museums Scotland.

reversed though 180°; these species can climb head (a) first down trees, holding on with their hind feet (Taylor 1989, Figure 3.14).­ Coatis and raccoons are able to partly reverse their hindfeet for head-first locomotion down trees (McClearn 1992).

Reproductive physiology: delayed (b) implantation and superovulation

Delayed implantation, where the blastocyst embryo does not implant into the uterine wall for several weeks up to several months (Figure 3.15), is char- acteristic of the reproductive cycles of many muste- loids, especially the mustelids (Table 3.6). Coupled with superovulation, where individual females may ovulate and fertilize eggs serially over peri- ods of several weeks or even months (Yamaguchi et al. 2006), these two reproductive strategies may (c) explain part of the mustelids’ global success. De- layed implantation appears to be ancestral among mustelids (Lindenfors et al. 2003; Thom et al. 2004b), but is not retained by all species today, although it is especially common in mustelids. Of the 53 mam- mal species that display delayed implantation, 40% are mustelids and 49% are musteloids (Lindenfors et al. 2003; Thom et al. 2004b). Several theories at- tempt to explain why mustelids use delayed im- plantation, for example, as allowing mating when parents are in prime condition and births when Figure 3.14 The flexible talo-crural joint of the kinkajou. From resources are optimal, effects of winter on sperm Taylor 1989.

03-Macdonald-Chap03.indd 126 31/05/17 7:04 PM Form and function of the musteloids 127

M I I I P P M P M2 1 M

Mustela erminea M. frenata Neovision vison

I P I M I P P M M

Martes pennanti M. zibellina M. americana

IIP I M P P M M

Lutra canadensis Meles meles (France) Taxidea taxus

M I M I P P

Figure 3.15 delayed implantation in musteloids. From Spilogale (western) Spilogale (eastern) Ewer 1973.

Table 3.6 Musteloids with delayed implantation (Lindenfors production and encounter rates for mating, limiting et al. 2003; Thom et al. 2004b). population size by restricting breeding to one litter annually, or even no adaptive value at all (Linden- Mustelidae Mephitidae Ailuridae fors et al. 2003). It is problematic to attempt to find Mustela erminea Conepatus mesoleucos Ailurus (fulgens) a one-size-fits-all explanation for delayed implan- Mustela frenata Mephitis mephitis fulgens tation that may have evolved in different families, Neovison vison Spilogale gracilis Ailurus (fulgens) Martes americana styani including and bears, for different reasons Martes zibellina compared with mustelids. However, in general, car- Martes martes nivorans with delayed implantation tend to live at Martes foina much higher latitudes, live longer, and have lower Martes flavigula Martes gwatkinsii maternal investment (gestation plus lactation) in Pekania pennanti their young, but no factors appear to explain the Gulo gulo variable length of diapause (Thom et al. 2004b). Vormela peregusna Taking a closer look at mustelids, they are mostly Mellivora capensis smaller than other carnivorans, they live at low Arctonyx collaris1 Meles meles2 population densities, and rely mostly on scent Taxidea taxus marking to communicate. Females in oestrus may Lontra longicaudis have difficulty in finding territory-holding males Lontra canadensis in short time periods to allow for successful mat- Enhydra lutris ing. Induced ovulation gets over the problem of 1probably also in Arctonyx hoeveni, and A. albogularis 2probably also in Meles anakuma, M. amurensis, M. canescens, and M. leucurus wasted egg production without mating. However

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if females mate with suboptimal males, which may The daylight-mediated hormonal pathway that be at risk from losing their home range, the females elicits pelage moult in mustelids (see Pelage insu- may risk losing their young through infanticide by lative properties), also stimulates production of incoming males, thereby wasting reproductive ef- progesterone, causing blastocysts to implant and fort. By extending the period in which females can restart their development (King and Powell 2007). mate by superovulation (Macdonald et al. 2015a), Therefore, increasing day length synchronizes blas- females can choose when, who, and how many tocyst development, which may result from mat- males to mate with, and presumably how many ings with different males at different times. If the young to produce, thereby maximizing or optimiz- reproductive cycle depends on spring ovulation, in- ing their reproductive success to prevailing ecologi- volving oestrogen, this may be interrupted by hor- cal conditions. monal changes associated with pelage moult and Interestingly, carnivoran baculum length is not progesterone production. Either ovulation would linked to induced ovulation, but it is greater at be delayed until after moult, providing sufficient higher latitudes in areas with greater accumula- time in the rest of the year for litters to grow and tions of snow, where population densities are low become independent, or moult would be delayed, and multi-male mating systems occur, such as in which may compromise thermoregulation and, in many mustelids (Ferguson and Larivière 2004). some species, cryptic coloration, leading to higher ­Females may assess male quality through baculum probability of predation. size (and musteloids in general have large bacula, Figure 3.16) by mating with multiple males, which, Winter torpor linked with superovulation and delayed implanta- tion, could explain part of the success of mustelids, Some musteloids have evolved physiological ad- particularly at higher latitudes. Baryshnikov et al. aptations for surviving winter, when food may be (2003) examined variability and scaling of bacula in unavailable or limited. Northern raccoons build up mustelids and other carnivorans. In general mus- large fat deposits, on which they depend in higher telines and procyonids have longer bacula relative latitudes by sitting out the coldest winter peri- to skull size than other carnivorans, whereas otters ods, but body temperatures and metabolic rates and mephitids have shorter bacula. Otters, includ- are not reduced, and heart rates are higher than ing the sea otter, have bacula that are believed to in summer (Lotze and Anderson 1979). Striped facilitate mating in water, even though they may skunks, ­American badgers, European badgers, mate on land.

(a) (b) (c) (d)

(g) (f) (e) (h)

(i) (j) (k)

Figure 3.16 Bacula of musteloids. a. Mustela putorius, b. Mustela luteola, c. Mustela nivalis, d. Mustela erminea, e. Martes martes, f. Martes foina, g. Procyon lotor, h. Procyon cancrivorus, i. Nasua nasua, j. Nasua narica, k. Potos flavus. From Didier 1947, 1950.

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and Japanese badgers (Meles anakuma) all undergo demands on adipose tissue and was most closely forms of torpor or hibernation to survive winters. linked to photoperiod, but ambient external tem- To undergo torpor, these musteloids deposit large peratures and precipitation were also influential. amounts of fat, providing an energy store during Japanese badgers have also been recorded enter- the winter when food consumption is severely lim- ing into winter torpor for 42–80 days (Tanaka 2006). ited. For example, American badgers reach their From December to March the mean body tempera- maximum fat deposits (c.31% of body weight) in ture of a male cub varied between 32°C and 35°C November and these reduce by 37% during the and it lost 32.1% of its body weight. Although mod- winter, when they spend up to 93% (70 days) of est compared with body temperature decreases their time in burrows where ambient temperatures (from a mean of 37°C) in European badgers, this re- are higher and more stable (0–4°C) (Harlow 1981, duction in body temperature would reduce the loss see Weir et al., Chapter 19, this volume). During of adipose tissue for metabolism. this time they enter torpor up to 30 times, when heart rate is reduced by 50% (from 55 down to 25 Adaptations for an aquatic lifestyle beats per minute) and body temperature is reduced by 9°C (to 29°C), giving mean torpor cycle periods Musteloids are unique among carnivorans in of 29 hours. The torpor cycle comprises 15 hours that they include semi-aquatic and aquatic spe- entering into torpor, 8 hours in torpor and 6 hours cies. The resulting diversity in form and function in arousal. The energetic benefit is profound, with among mustelids required to meet the demands of torpor reducing energy expenditure by 27% or 81 these disparate lifestyles is remarkable, especially kcal per cycle (Harlow 1981). when compared to specialist terrestrial carnivoran During winter in southeast Saskatchewan, Can- lineages, such as the and (Van ada, solitary striped skunks enter daily torpor Valkenburgh 1999). Malleability of three morpho- spontaneously, reaching body temperatures as low physiological characters were key to the successful as 26.0°C for 50 out of 120 days (Hwang et al. 2007). occupation of water by mustelids: 1) hair and pelage Only some that lived in communal dens went into modification for thermoregulation while immersed; daily torpor, but then it was shallow and occurred 2) limb and paw anatomy for locomotor efficiency infrequently. On average solitary skunks entered in water; and 3) specific adaptations for diving. torpor for 7.8 hours and reached body temperatures of 26.8°C when active compared with 5.4 hours and Thermoregulation 30.9°C for communal skunks, but only when they were resting diurnally (Hwang et al. 2007). Not The thermal challenges for aquatic mammals surprisingly, solitary skunks emerged from win- are well documented (Irving 1973; Whittow ter with lower fat deposits (mean 9.3% body mass) 1987; Williams­ 1998; Yeates et al. 2007; Thometz compared with communal skunks (mean 25.5% et al. 2014), and demonstrate the difficulty of sus- body mass) (Hwang et al. 2007). Clearly, commu- taining the semi-aquatic habits of many mustelid nal denning has energetic advantages for surviving species. Disparate thermal properties for air and winter. water, for example in heat capacity and conduc- European badgers were also recorded entering tivity, result in a 25-fold increase in heat transfer torpor or winter lethargy during winters in Scot- from the body when animals are immersed com- land, but this differs from the periodic bouts of pared to when exposed to air of similar tempera- torpor of American badgers (Fowler and Racey, ture (Schmidt-Nielsen 1997). Comparatively small 1988). Body temperatures reduced by up to 8.9°C size, elongated body shapes, and resultant high to 28–34°C between October and March, and ac- surface-area-to-volume ratios of mustelids promote tivity levels decreased outside setts by up to 90%, heat transfer, exacerbating problems of maintain- indicating that badgers took advantage of higher ing thermal stability for aquatic foragers, such as ambient temperatures within setts compared with mink and otters. Therefore, mustelid bodies can outside. Overall, winter lethargy reduced energetic cool rapidly during underwater hunting, especially

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in smaller species. For example, the core body tem- next to the skin. By physically preventing infiltra- perature of a 1 kg mink begins to decline within 2 tion of water, heat loss is diminished. Among semi- to 4 minutes of immersion, with the rate of cooling aquatic and marine otters, pelage density, hair dependent on activity level and seasonal insulation length and shape, as well as surface architecture provided by the pelage (Williams 1986). For female of individual hairs, are correlated with degree of mink, resting for 12 minutes in water at 24.6°C, core aquatic specialization (Fish et al. 2002; Kuhn and body temperature declined by 3.3°C compared to Meyer 2010b). Liwanag et al. (2012) documented no change for the same animals resting in air at ap- a continuum in gross morphology (hair cuticle proximately the same temperature. Interestingly shape, circularity, length, and density) of individ- the rate of cooling for swimming mink was greatest ual hairs as well as thermal conductivity of pelage at intermediate swimming speeds when convective as mammals move from terrestrial to semi-aquatic heat losses associated with limb movements ex- to fully aquatic lifestyles. In general, aquatic mus- ceeded the level of heat produced by exercise (Wil- telids have significantly flatter, shorter hairs and liams 1986). Such high activity levels and associated increased overall pelage density compared to those heat production, as may occur with clustering dives of terrestrial forms (Figure 3.17). Interestingly, into bouts, may explain in part the ability of free- mustelid exploitation of aquatic habitats has coin- ranging mink to offset excessive heat loss and for- cided with some of the highest fur densities meas- age for periods longer than expected by simple heat ured for carnivorans, giving an unprecedented loss models based on individual dives (Bagniewska range of values within a family. Thus, the fur den- et al. 2015). sity of stoats (97 hairs per mm2) is similar to that Likewise, the rate of body cooling in 7 kg Eura- of other terrestrial carnivorans, while that for sea sian otters, foraging in 2–16°C freshwater lochs otters (>1200 hairs per mm2) is 12 times higher and in Scotland, averages 2.3°C per hour during short is the densest pelage for any (Liwanag feeding bouts (Kruuk 1995), which is 12 times the et al. 2012; see also ­Table 3.2). Semi-aquatic North average level measured in 27 kg sea otters feeding American mink, North American beaver (Castor in 10–19°C coastal waters. Despite being the larg- canadensis), and muskrat (Ondatra zibethicus), have est mustelids, even sea otters experience sequen- fur densities between these extremes, averaging tial variations of >1.5°C in core body temperature c.350 hairs per mm2, which indicate the importance throughout the day, with increases and declines of an aquatic lifestyle rather than being a mustelid matched to activity level and the digestion of food in determining this trait (Fish et al. 2002; see also (Yeates 2006; see also Estes et al., Chapter 23, this Table 3.2). volume). Overall, aquatic mustelids are often only Elongated cuticular scales on both guard hairs marginally successful at maintaining stable core and underfur are also evident with increased aquatic body temperatures when immersed, with the tim- specialization by mustelids (Figure 3.17). Such geo- ing and duration of aquatic forays by mink (Wil- metric scale patterning promotes interlocking or liams 1986; Dunstone 1993; Bagniewska et al. 2015), ‘felting’ of fine underhairs (Weisel et al. 2005; Kuhn Eurasian otters (Kruuk 1995), and sea otters (Yeates et al. 2010; Kuhn and Meyer 2010a). Together, these 2006) dictated by the balance between activity- characteristics assist in establishing and maintain- induced heat production and the threat of hypo- ing the insulating air layer, especially as the pelage thermia. This physiological challenge, along with flattens with compression during immersion. breath-holding capabilities (Stephenson et al. 1988), Grooming the fur to ensure the integrity of such undoubtedly influences foraging and requires fur- specialized, waterproof pelage is both time con- ther investigation, particularly in small mustelids. suming and metabolically expensive for aquatic Lacking a significant blubber layer, as found in mustelids. In general, the degree of water salinity cetaceans, sirenians, and pinnipeds (Williams and appears to dictate investment in grooming and Worthy 2002), the pelage is the primary insulat- successful colonization of different waterways by ing barrier for aquatic mustelids. A suite of unique mustelids (Kruuk and Balharry 1990; Kruuk 1995). morphological adaptations enable the pelage of River otters may spend 6% of their day groom- aquatic mustelids to trap an insulating layer of air ing, depending on exposure to fresh or salt water

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Coyote Ermine River otter Sea otter

20μm 820X 40μm 600X 60μm 400X 40μm 530X

40μm 540X 40μm 600X 20μm 700X 40μm 530X Figure 3.17 Scanning electron micrographs of guard hairs (upper pictures) and underhairs (lower pictures) for terrestrial (ermine), semi-aquatic (river otter), and fully marine (sea otter) mustelids. A non-mustelid, terrestrial carnivore () is shown for comparison. Magnifications are noted on the scale bars. Micrographs provided by H. Liwanag, Adelphi University, NY.

(Nolet and Kruuk 1989). This increases to 8% of the otter). An additional metabolic mechanism, the day for marine otters (Lontra felina, Medina-Vogel specific dynamic action from digestion of prey, pro- et al. 2006), and sea otters (Yeates 2006). Often vides endogenous heat for sea otters that can last 4 grooming involves high-intensity rolling, rubbing, to 5 hours. This allows post-prandial sea otters to and fur pleating that can be energetically costly. slow body cooling while resting in water (Yeates Somersaulting, vigorous kneading, and fur blowing 2006), and probably contributed to their ability to by grooming sea otters raised metabolic rates to 22 develop a fully aquatic lifestyle.

mlO2 per kg per minute, a 64% increase over resting values that even exceeded the cost of submerged Locomotor efficiency on land and in water swimming (Williams 1989). Metabolic responses that enhance heat produc- Elongate body shapes and aquatic or semi-aquatic tion, including shivering and non-shivering ther- habits present unique challenges to locomotion mogenesis, increased skeletal muscle activity, and for mustelids foraging in water and on land. Body the processing of food, are important for defraying streamlining, short legs, and enlarged plantar excessive heat loss in aquatic mustelids. American surface areas that enhance propulsive efficiency mink (Williams 1986; Bagniewska et al. 2015), Eura- during swimming (Fish 1993) can result in both sian otters (Kruuk 1995), and sea otters (Costa and energetic and biomechanical disadvantages dur- Kooyman 1984; Yeates 2006) delay or mitigate cool- ing running. Yet, these species may travel long ing through increased heat generated by being ac- distances and move across extensive home ranges tive. These activities may occur in water (American both on land and in water. Home-range length mink, sea otter) or on land prior to a dive (Eurasian varies from 1 to 5 km along edges of waterways

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for American mink (Gerell 1970; Dunstone 1993; (Figure 3.18). Therefore, gait transitions in aquatic Macdonald et al. 2015a) and is similar to the daily mustelids occur at slower speeds in aquatic mus- running distances of much smaller weasels (Chap- telids than predicted for other mammals (Heglund pell et al. 2013). Otter movements are even greater. et al. 1974), with the greatest discrepancies between Home ranges can exceed 40 km for transient Eura- measured and predicted transition speeds, coincid- sian otters in Shetland (Kruuk 1995), and may cover ing with the degree of aquatic specialization of the hundreds of kilometres for sea otters on the Califor- limbs. Thus, the observed gait transition speed for nian coast (Kage 2004). Therefore, this is a highly running sea otters (0.83 m per s) is less than one mobile group that takes advantage of a wide vari- quarter of the predicted transition speed (3.4 m per ety of resources across different habitats regardless s) for terrestrial long-legged quadrupeds. of apparent locomotory disadvantages. Despite marked differences in body mass, maxi- Among aquatic mustelids, morphological adap- mum voluntary running speeds for sea otter, North tations for swimming have required compromises American mink, and river otter averaged 2.0 m in biomechanics, locomotor speed, and energetic ef- per s (Scaramozzino 2000). These speeds are not ficiency on land. In comparing the running biome- remarkable, considering the 0.8–1.4 m per s maxi- chanics of American mink, North American river mum speed range of diminutive terrestrial wea- otters, and sea otters, Scaramozzino (2000) found sels (Chappell et al. 2013) and the 2.8–3.3 m per s that degree of aquatic specialization correlated running speed range of 3 to 4 kg fishers (Powell with progressive decreases in predicted stride fre- 1979b). This occurs even though aquatic mustelids quency, stride length, and speed at the walk/bound partially overcome mechanical limitations of their gait transition. While all three species use walk- limb morphology by employing spinal flexion to ing gaits at low speeds and change to bounding or lengthen their stride to achieve greater maximum half-bounding at high speeds (Tarasoff et al. 1972; speeds, a strategy especially notable for the sea ot- Williams 1983b), distinguishing between these ter (Figure 3.18). gaits, particularly at intermediate speeds, becomes Like running, swimming by aquatic mustelids complicated with increased hindfoot plantar area shows a biomechanical progression in moving from

SWIMMING Mink River otter Sea otter

RUNNING

Mink

River otter

Sea otter

0.0 0.5 1.0 1.5 2.0 2.5 3.0 Speed (m.s–1)

Figure 3.18 running and swimming speeds of aquatic mustelids. Swimming includes surface (hatched bar) and submerged (grey bars) routine activities. Running is divided into walking (black bar) and bounding/half-bounding (white bars) gaits. Spinal flexion and footfall patterns during maximum extension and flexion for bounding North American mink, river otter, and sea otter are shown in the illustrations. Length of the lines denotes the relative length between the shoulder and tail. Redrawn from Williams 1983b and Scaramozzino 2000. Additional data are from Dunstone 1993, Williams 1989, and Nolet et al. 1993.

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terrestrial to semi-aquatic and fully aquatic life- per s ­(Figure 3.19).­ In comparison to semi-aquatic styles. Mustelids that swim at the surface demon- mustelids, sea otters show considerable variation strate inefficient swimming styles in terms of thrust in swimming styles when at the water surface, production. This includes thrust-recovery paddling ­alternating between ventral-down and ventral-up by semi-aquatic American mink (Figure 3.19, Wil- positions, depending on swimming speed and as- liams 1983a) and river otters (Fish 1994), in which sociated behaviours (i.e. eating, resting, patrolling). all four limbs or alternate limbs move posteriorly to Rowing and sculling by surface-swimming sea move them forward in the same manner as swim- ­otters, in which hind flippers moved alternately or ming by terrestrial mustelids, including stoats (King simultaneously to provide propulsion, are used pri- et al. 2013) and ferrets (Fish and Baudinette 2008). marily for slow transects at <0.8 m per s (Williams For these species the body is held horizontally at 1989). Also, as witnessed by any casual observer of the water surface, with limbs remaining submerged wild otters and mink, swimming sprints of short throughout the stroke cycle. Swimming speeds duration, especially when chasing fish or cohorts, for thrust-recovery paddling are comparatively may be even faster. slow. For example, the range of surface speeds for Higher speeds and greater efficiency are achieved American mink in a water flume is 0.13–0.70 m under water (Fish 1993). In addition to reducing

1

2

3

4

5

Figure 3.19 Swimming mechanics for one stroke cycle for the North American mink (left) and North American river otter (right). Note that all four limbs are used for propulsion with diagonal limbs moving in synchrony for the mink. Reprinted from Williams 1983a. In contrast, body undulation provides the major propulsive force for the submerged river otter. Reprinted from Fish 1994.

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overall drag, submergence allows otters to employ running costs that reduce as they change from body undulation when swimming (Figure 3.19). walking to bounding gaits (Williams 1983b). Lastly, When submerged, the body and tail are moved North American river otters, the most aquatically dorso-ventrally to provide thrust. Otters generally adapted mustelid for which running energetics have long dorso-ventrally flattened tails that are have been measured, show the greatest difference thick at the base for this form of locomotion, and between measured and predicted values. The mini- sea otters’ tails are especially thick and muscular. mum net transport cost is 6.63 J per kg per min for For both river otters and sea otters dorso-ventral river otters running at 1.43 m per s, and is 34–46% undulation of the body replaces simple limb move- higher than predicted for similarly sized terrestrial ments as the major propulsive mechanism (Tarasoff mammals (Williams et al. 2002). et al. 1972; Williams 1989; Fish 1994). This mode Swimming imposes even higher energetic costs of swimming achieves higher transit speeds when for aquatic mustelids. In general, the metabolic cost submerged (Figure 3.19). The average underwater of surface swimming in semi-aquatic mammals, swimming speed for North American river otters including American mink, is 2.4–5.1 times that of in pools is approximately 1.4 m per s (Fish 1994). marine mammal specialists (Williams 1999). This This compares with estimated swimming speeds of is due primarily to two factors, elevated hydro- 0.26 m per s for wild Eurasian otters, when slowly dynamic drag associated with surface-wave gen- searching for fish along the water bottom, and 1.52 eration, and low propulsive efficiency coincident m per s during routine rectilinear movements (No- with thrust-recovery propulsion (Fish 1993). The

let et al. 1993). By changing from surface to sub- total cost of transport (COTTOTAL) for semi-aquatic merged swimming modes, sea otters nearly double ­surface-swimming mammals is: their travelling speed to 1.4 m per s (Williams 1989), COT = 26.81 body mass −0.18 (1) but they can swim much faster for short periods. TOTAL

The energetic consequence of a semi-aquatic life- where COTTOTAL is in J per kg per minute and body style by mustelids is increased costs of locomotion mass is in kg (Williams 1999). By submerging and for both running and swimming when compared changing to undulatory swimming, transport costs with transport costs of terrestrial and marine mam- are reduced significantly for aquatic mustelids. mal specialists. The cost of transport, defined as the Consequently, the minimum transport cost for sea amount of energy it takes to transport one unit of otters decreases by nearly 60% when they change body weight over a unit distance (Schmidt-Nielsen from surface to underwater swimming (Williams 1972), shows consistent but modest elevations for 1989). Similar decreases were demonstrated for sub- running in both terrestrial and semi-aquatic mus- merged swimming by Eurasian otters (Pfeiffer and telids. Depending on species, these elevated run- Culik 1998). However, the energetic costs of swim- ning costs occur because of: 1) inherent high resting ming for Eurasian and sea otters remain higher than metabolic rates of mustelids (Iverson 1972; Yeates predicted for highly adapted marine mammals, et al. 2007; Thometz et al. 2014); 2) unique biome- such as pinnipeds and cetaceans (Williams 1999). chanical costs in musteloids (Williams 1983b), and Despite the biomechanical and energetic chal- 3) postural costs from supporting long, slender lenges of a semi-aquatic lifestyle, many mustelid bodies on short legs (Williams et al. 2002; Chappell species move successfully between terrestrial and et al. 2013). By subtracting resting metabolism from aquatic habitats. This includes species other than total energetic costs during locomotion, the con- North American mink and otters that have tradi- founding effects of elevated resting metabolic rates tionally not been thought of as semi-aquatic. For of some mustelid species can be accounted for. The example, ferrets are proficient swimmers capable resulting net cost of transport for running fishers of foraging for fish and demonstrate a transport (Powell 1979b) and weasels (Chappell et al. 2013) cost for swimming similar to those of semi-aquatic remains 26% and 35–37% higher than predicted mammals (Fish and Baudinette 2008). Similarly, for other terrestrial quadrupeds, respectively. stoats appear to move easily between the mainland American mink show similar greater-than-expected and offshore islands of New Zealand in search of

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prey (Taylor and Tilley 1984; King et al. 2013; King developed compared with its hindlimbs, with short et al., Chapter 10, this volume), such that they are metacarpals and poorly developed insertion sur- now considered significant wide-ranging predators faces on the humerus, whereas the femur is robust, of native shorebirds in wetland areas. but very short, and the distal hindlimb elements are elongated for specialized hindlimb propulsion (Tarasoff et al. 1972; Mason and Macdonald 1986; Skeletal adapations for swimming Mori et al. 2015). Therefore, the sea otter’s hind- Swimming imposes challenges for carnivoran skel- feet show extreme modification to provide efficient etons and it is not surprising, therefore, that otters’ paddling in water. The sea otter’s hands have very body form is hydrodynamic with a fusiform shape. short digits, used primarily for manipulating food; The cervical vertebral segment is shorter than the they are held against the body during swimming. thoracolumbar vertebral segment for body stream- As a result sea otters seldom go more than 75 metres lining and to provide stronger support for propul- from the shore, owing to their poor adaptations for sion (Taylor 1989). Active swimming requires strong terrestrial locomotion (Rosevear 1974; Taylor 1989; propulsion and imposes constraints on hindlimbs, Lambert 1997). Overall these features make the sea so that otter femora and tibiae are particularly otter a fully aquatic mammal, contrasting with all stocky bones. Femora are straight and short, while other semi-aquatic Lutrinae. In contrast, the Ameri- tibiae are longer and curved to maximize hindlimb can mink is often considered semi-aquatic, although muscle insertion (especially those involved in dor- studies by Williams (1983a, b) demonstrated that it siflexion, inversion, and plantar flexion). The glu- is not as well adapted for swimming as otters due to teus muscles provide strong propulsion, hence the its typical streamlined musteline body shape. greater trochanter and femoral tuberosity are well developed (Schutz and Guralnick 2007). Schutz and Conclusion Guralnick (2007) noted that the tibia shaft is unusu- ally curved for the broadening of the flexor hallucis The diversity of form and function among the longus groove. This region allows passage of ten- musteloids is remarkable among carnivorans, and dons of the posterior leg muscles involved in dorsi- provides unique opportunities for understanding flexion, inversion, and plantar flexion. the morphological, behavioural, and physiological In the otter forelimb, the humeri are also curved trade-offs associated with successful exploitation midshaft for increased muscle attachment to the of different ecological niches. The mustelids, in anterior forelimb, with large heads and expanded particular, are highly successful in terms of species medial epicondyles, as are the olecranon process diversity and global distribution. There are sev- and tibial tuberosities, while the metatarsals are eral morphological and physiological adaptations elongated (Samuels et al. 2013). The expanded dis- that are key to their diversification, including a tal humerus allows for large attachment areas for small, elongated body plan with short legs allow- muscles that flex, pronate, and supinate the fore- ing exploitation of a wide array of niches, a highly arm, and flex and extend the wrist (Schutz and Gu- insulating pelage that can be moulted seasonally ralnick 2007). The radius and ulna are also curved allowing survival at high latitudes, powerful teeth midshaft and the metacarpals are characteristically and jaws for killing often larger prey, anal sacs that short relative to the metatarsals (Taylor 1989). All are effective in intraspecific communication at low these modifications relate to improvement in pro- population densities and/or utilization as chemical pulsion by the action of the forelimbs and paddling weapons to deter predators, and a combination of by the hindlimbs (Schultz and Guralnick 2007). superovulation and delayed implantation, allowing The sea otter is more adapted to an aquatic life- females to choose (and find) when and whom to style than other musteloids. It has a higher bone mate with, but synchronizing births in the spring. density than that of other terrestrial mustelids, but Although none of these is exclusive to the mustelids bigger animals exhibit higher bone densities (Fish among carnivorans, they form a unique combina- and Stein 1991). The sea otter’s forelimbs are poorly tion for their global success.

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