Philander canus ( Osgood, 1913 )

Voss, Robert S., Díaz-Nieto, Juan F. & Jansa, Sharon A., 2018, A Revision of Philander (Marsupialia: Didelphidae), Part 1: P. quica, P. canus, and a New Species from Amazonia, American Museum Novitates 2018 (3891), pp. 1-72 : 38-46

Philander canus ( Osgood, 1913)

Metachirus canus Osgood, 1913: 96 ; type locality Peru, San Martín, Moyobamba (6°03′ S, 76°58′ W; Stephens and Traylor, 1983).

Metachirus opossum crucialis Thomas, 1923: 604 ; type locality Bolivia, Santa Cruz, Santa Cruz de la Sierra (17°48′ S, 63°10′ W; Paynter, 1992).

Philander mondolfii Lew et al., 2006: 229 ; type locality Venezuela, Bolívar, Reserva Forestal de Imataca , Unidad V, between Tumeremo and Bochinche (8°00′ N, 61°30′ W).

Philander olrogi Flores et al., 2008: 17; type locality Bolivia, Santa Cruz, 7 km N Santa Rosa (17°03′ S, 63°35′ W) .

TYPE MATERIAL: The holotype (by original designation, FMNH 19347) consists of the skin and skull of an adult male collected by W.H. Osgood and M.P. Anderson on 4 August 1912. Although the skin is well preserved, the skull is broken and incomplete (the left zygomatic arch, the left squamosal, and the left bulla are all missing).

DISTRIBUTION AND SYMPATRY: Sequenced specimens and other examined material that we refer to Philander canus have been collected in central and western Brazil, northern Argentina, Paraguay, eastern Bolivia, eastern Peru, northeastern Colombia, and Venezuela ( fig. 9 ). Although we have not examined specimens from northeastern Peru (Loreto), eastern Ecuador, or southeastern Colombia (Caquetá, Putumayo), future collecting may eventually fill in this geographic hiatus. Philander canus occurs sympatrically with P. andersoni in southern Venezuela (at El Platanal in Amazonas state), with P. mcilhennyi in eastern Peru (e.g., at Balta, in Ucayali department) and western Brazil (at Sobral, in Acre state), and with P. pebas in eastern Peru (e.g., at Balta, in Ucayali department).

Brazil, Tocantins (50): JF281038 Brazil, Tocantins (50): JF281037 , Tocantins (50): JF281039 , Tocantins (49): JF281036 , Pará or Tocantins: JF281034 , Pará or Tocantins: JF281040 , Pará (38): JF281035 , Mato Grosso (29): KT153573 , Mato Grosso (29): LPC392 Acre (12) : MNFS1453 Mato Grosso (28) : LPC584 Santa Cruz (9): NK11830 Grosso do Sul (27): KT153575 , Meta (52): JAWK402 Mato Grosso do Sul (27): KT153576 , Trujillo (91): JAWK281 canus , Chaco (1): JQ778956 , Ñeembucú (76): KM188486 , Presidente Hayes (78): KM188487 Formosa (2): JQ778957 Chaco (1): JQ778962 Ñeembucú (76): GD066 Grosso do Sul (27): KT153574 Alto Paraguay (75): KM188488 Formosa (2): JQ778958 Grosso do Sul (27): LPC596 8): NK13894: NK13172 Bolívar (90): TK19152 NK13171 : LAR299 : LAR298 Amazonas (19): DQ236271 Amazonas (19): DQ236275 (16) : JLP15395 Amazonas (19): DQ236276 (16) : U34678 , Amazonas (19): DQ236274 Amazonas (19): DQ236273 Amazonas (19): DQ236272 pebas Amazonas (19): DQ236277 Dios (85): NW579 80): TK73935 81): KM 188489 80): TK73919 Ecuador, Orellana (57): F40358

DESCRIPTION: Dorsal pelage short (usually <14 mm) and uniformly grayish, usually without any trace of darker middorsal pigmentation; fur of crown (between the ears) usually grizzled gray; pale preauricular spot often present; ventral fur continuously self-whitish, -cream, or -buffy, at least along the midline, but sometimes with broad lateral zones of graybased hairs; pinnae pale (unpigmented) basally, but blackish distally; dorsal pelage of hind feet usually pale, but sometimes indistinctly darker over lateral metatarsals (never distinctly marked with black); scaly part of tail usually <½ white distally but seldom <¼ white. Nasal bones short (about 46% of condylobasal length on average), never extending posteriorly to or between postorbital processes. Unworn third upper premolar (P3) apparently always with complete labial cingulum extending along entire base of tooth; crown length of upper molar series 13.0 ± 0.4 mm (sexes combined; observed range 12.2–14.1 mm, N = 99); enameled lingual surfaces of upper molars smooth, not crenulated; pre- and postcingula consistently absent; lower molar postcingulids absent.

PHYLOGEOGRAPHY AND GEOGRAPHIC VARIATION: Our phylogenetic analysis of 32 sequences of Philander canus reveals no comprehensible phylogeographic structure, with haplotypes from northern populations (in Colombia and Venezuela) mixed in among those from central Brazil, Bolivia, Paraguay, and northern Argentina ( fig. 16 ). Uncorrected sequence divergence at the cytochrome- b locus among haplotypes that we assign to P. canus is only about 0.8% despite the very wide geographic dispersion of collecting localities. Although we have not statistically tested for geographic variation in morphology among our samples, this appears to be another phenotypically rather uniform species despite modest sample differences in pelage pigmentation (some populations tending to have self-whitish or -cream underparts, whereas others have self-buffy ventral fur).

COMPARISONS: Morphological comparisons of Philander canus with P.quica have already been described (see above) and comparisons with P. pebas will be described subsequently (see below). It remains to compare this species with members of the P. opossum complex, which—as defined earlier in this report—includes P. opossum , P. andersoni , and P. mcilhennyi .

Philander canus is superficially similar to P. opossum , with which it has long been associated as a subspecies or synonym (e.g., by Cabrera, 1958; Patton and da Silva, 1997, 2008; Gardner, 2005; Chemisquy and Flores, 2012; Hice and Velazco, 2012). Although the geographic ranges of P.canus and P. opossum are not currently known to come into contact, it seems plausible that these species are sympatric or parapatric in the Brazilian states of Mato Grosso, Tocantins, and southern Pará, where Cerrado vegetation comes into contact with southeastern Amazonian rainforest. Philander canus is substantially smaller, on average, than P. opossum in several same-sex univariate comparisons ( table 11), notably in condylobasal length (CBL), nasal length (NL), least interorbital breadth (LIB), least postorbital breadth (LPB), palatal length (PL), and maxillary toothrow (MTR). Despite some overlap in observed ranges for all dimensions, measured samples of these species have nonoverlapping multivariate distributions ( fig. 17 ), and general-size-adjusted shape coefficients indicate that nasal morphology accounts for much of the observed divergence ( table 12). Visual comparisons suggest that the posterior portion of the nasals of P. canus are typically much broader than those of P. opossum , do not extend as far posteriorly, and lack the deep posterolateral notches that are often present in the latter species ( fig. 18 ). Philander canus and P. opossum both have uniformly grayish dorsal fur, mostly pale hind feet, and self-colored ventral fur, but tail pigmentation might be useful for field identification. Whereas the scaly part of the tail is almost always <½ white in specimens of P.canus , the scaly part of the tail is typically ≥½ white in specimens of P. opossum , and this modal difference might be expected to become even more pronounced in sympatry. 9

9 We suspect (although there is no behavioral evidence to support our conjecture) that the black-and-white tail markings of Didelphini have some social-signaling function that might be coopted for species recognition in sympatry.

differences (Shape) for multivariate analyses of Philander canus versus P. opossum a

Philander canus is much smaller, on average, than either P. andersoni or P. mcilhennyi , from which it also differs in nasal shape as described and illustrated above (all members of the P. opossum complex have long, narrow nasals that are often laterally notched and often extend posteriorly to or between the postorbital processes). Large generalized distances (appendix 4) suggest that multivariate ordinations of P. canus with either P. andersoni or P. mcilhennyi would show nonoverlapping distributions, but we have not performed those analyses because these species are easy to tell apart by other characters. The dorsal pelage pigmentation of P. canus (uniformly gray; fig. 10 ) is quite unlike that of P. andersoni (with a distinctly blackish middorsal stripe) and P. mcilhennyi (some specimens of which are completely blackish). The self-whitish, -cream, or -buffy underparts of P. canus likewise contrast with the mostly gray-based ventral pelage of P. andersoni and the almostblackish ventral fur of P. mcilhennyi ( fig. 11 ). Whereas the hind feet of P.canus are covered dorsally with pale fur, the hind feet of P. andersoni and P. mcilhennyi are either completely blackish or have black metatarsals and abruptly whitish digits. Lastly, the scaly part of the tail is almost always <½ white in P.canus but apparently always ≥ ½ white in P. andersoni and P. mcilhennyi .

REMARKS: As understood herein, Philander canus includes the nominal taxa crucialis, mondolfii , and olrogi . The latter are represented in our molecular analyses by: (1) a CYTB sequence we obtained from a Bolivian specimen (AMNH 260034) that was collected near the type locality of crucialis and that resembles the holotype of crucialis in qualitative and morphometric traits; (2) two CYTB sequences, one from a Colombian specimen (KU 123943) and another from a Venezuelan specimen (KU 120245) that were part of Lew et al.’s (2006) original material of mondolfii ; and (3) CYTB sequences that we obtained from two specimens (AMNH 261271, 261272) that were part of Flores et al.’s (2008) original material of olrogi . All these specimens conform to our morphological diagnosis of P.canus , so the conclusion that the nominal taxa in question are conspecific seems straightforward, but brief comments on each synonym are appropriate.

PC1

SIZE

Thomas (1923) described crucialis on the basis of a single specimen, which he compared only with azaricus (= P.quica ; see above). Later, with more Bolivian material at hand for comparison with topotypical specimens of Osgood’s species, he ( Thomas, 1928) judged crucialis and canus to be indistinguishable. We agree.

Lew et al. (2006) described mondolfii based on several dozen specimens from Colombia and Venezuela that the authors compared carefully with other species of Philander known to occur in or near those countries, including P. andersoni , P.deltae , P. “ fuscogriseus ” (= P.melanurus ), and P. opossum , but they did not compare mondolfii with P.canus . Although we have not examined the holotype or paratypes of mondolfii —all currently inaccessible in Venezuelan museums—we did examine 16 specimens that were part of Lew et al.’s (2006) original material. These specimens (AMNH 16951, 30709, 30711–30714, 133119, 133120, 136163, 136167–136169, 139221; KU 120233, 120245, 123943) so closely resemble the type of P.canus and other referred material from eastern Peru that we could not find any phenotypic basis for retaining mondolfii even as a subspecies.

Flores et al. (2008) described olrogi on the basis of seven specimens from Bolivia and Peru. Although we have not seen the holotype, we examined the skull of a paratype (AMNH 246441) as well as several other specimens that were part of Flores et al.’s (2008) original material (AMNH 261269–261272). Despite careful study, we confess ourselves unable to consistently distinguish these specimens from material that the authors referred to P. opossum canus . Although they reported a principal-components analysis that was said to support the recognition of olrogi as a distinct taxon, canus and olrogi have overlapping distributions in their illustrated results ( Flores et al., 2008: fig. 5 ). In the absence of compelling evidence for the phenotypic distinctness of these genetically indistinguishable nominal taxa, we interpret the allegedly diagnostic traits of olrogi to be aspects of intraspecific morphological variation within P. canus .

Cabrera (1958: 35) listed nigratus as a synonym of canus (which he ranked as a subspecies of P. opossum ), but the holotype (BMNH 0.7.7.62) and other material that we refer to nigratus 10 are larger animals (LM = 14.7–16.4 mm) with much darker dorsal fur, completely gray-based ventral fur, blackish feet, shorter white tail-tips (less than ¼ of the tail is unpigmented in most specimens), and an incomplete labial cingulum on P3. Although we do not know whether nigratus is a valid species, its phenotype more closely resembles those of species in the P.opossum complex than that of P.canus .

Hershkovitz (1997) used the name Philander opossum quica for many specimens that we refer to P. canus , including all the material he listed from central Brazil (Goiás, Mato Grosso) and Bolivia; among the material that he listed from eastern Peru are specimens that we refer to both P. canus and P. pebas . The “dichromatism” that he ( Hershkovitz, 1997: 49) noted among specimens of “ P. o. quica ” from Balta (in the Peruvian department of Ucayali) is the result of sympatry rather than polymorphism: of the six specimens in question that we examined, three (LSUMZ 12006, 12008, 12009) are P.canus and the others (LSUMZ 12007, 12010, 14011) are P. pebas (see Specimens Examined for both taxa, below; a third congener, P. mcilhennyi , also occurs at Balta).

The western Amazonian specimens that Patton et al. (2000) referred to Philander opossum canus include examples of both P.canus and P. pebas . Of the five that we were able to examine— the others having been returned to Brazil —four (MVZ 190343–190346) are P. pebas ; only one (MVZ 190347, from the state of Acre, near the Peruvian border) is actually P.canus . The central Amazonian specimens that Nunes et al. (2006) identified as P. canus are also examples of P. pebas . 11 The only other material of P.canus that we have seen from the Brazilian Amazon (besides the MVZ specimen from Acre) is a small series collected many years ago along the lower Rio Madeira (in Amazonas state) and a single specimen from the upper Madeira (in Rondônia).

HABITATS: The geographic range of Philander canus extends over a wide range of biomes or ecoregions (including the Cerrado, Chaco, Pantanal, Llanos, and Amazonia), and it is possible that the species occurs in a corresponding variety of habitats, but definite ecological information associated with collected specimens is hard to find. Other species of Philander are

10 From the eastern Andean foothills of Junín and Ayacucho departments, Peru: BMNH 94.10.1.16, 94.10.1.17, 28.5.1.20; FMNH 65782; LSUMZ 16398, 16399; MUSM 71 .

11 We are indebted to S.E. Pavan, who kindly examined the MPEG voucher specimens from Nunes et al.’s (2006) study at our request.

known to live in rainforest, so collection records from biomes dominated by savanna vegetation and/or dry forest (e.g., the Cerrado, Chaco, and Llanos) seem anomalous, but the literature on Cerrado mammals provides a few relevant observations.

In the Cerrado landscapes of eastern Bolivia, Philander canus is apparently restricted to tall evergreen gallery forests and does not seem to occur in the savannas and dry forests that cover much of the landscape ( Emmons et al., 2006). In the Cerrado of central Brazil, P. “ opossum ” (presumably P.canus ) is also said to be a gallery-forest species ( Mello and Moojen, 1979; Redford and Fonseca, 1986; Alho, 2005), but in one report of a multiyear trapping study P. “ opossum ” was said to prefer gallery forest but to occur frequently in other local habitats, including open grassland, shrub savanna, and dry forest ( Alho et al., 1986). Following Pulliam’s (1988) ecological terminology, we conjecture that gallery forests are probably the source habitat for P.canus in Cerrado landscapes, whereas open formations (including dry forests) are likely to be sink habitats. In the Chaco of northern Argentina, Philander “ opossum ” (presumably P. canus ) is also said to occur in gallery forests ( Huck et al., 2017).

Information about the habitat distribution of Philander canus appears to be unavailable from trapping studies in the Pantanal and Llanos, but we suspect that it is largely restricted to gallery forests in those ecoregions as well. Nevertheless, Lew et al.’s (2006) summary of macrohabitats where Philander “ mondolfii ” (= P.canus ) has been collected in Venezuela (including lowland and submontane rainforest, semideciduous forest, and tree savannas) suggest that it has broad ecological tolerances, at least where other sympatric congeners are not known to occur.

We have not found any published accounts of where specimens that can definitely be identified as Philander canus have been collected in Amazonia. Although the natural climax vegetation throughout this enormous ecoregion can be broadly characterized as lowland rainforest, local disturbance (e.g., from lateral migration of rivers within their meander belts) and edaphic factors can result in a surprising diversity of natural vegetation types at many Amazonian localities ( Pires and Prance, 1985; Puhakka and Kalliola, 1995), and anthropogenic habitats are also scattered throughout the region. The geographic distribution of Amazonian collection localities for P.canus provides no habitat clues, because these localities are not clustered around savanna enclaves, human settlements, or other obvious landscape features. The known Amazonian range of P.canus broadly overlaps those of P. andersoni , P. mcilhennyi , and P. pebas , so it would be reasonable to suppose that competitive interactions with sympatric congeners might restrict the habitat occupancy of this species to some extent, but the information compiled for this report is entirely inadequate even for conjecture.

SPECIMENS EXAMINED (N = 154): Bolivia — Beni, Arruda ( FMNH 114701 ) , Camiaco ( AMNH 210402 ) , Casarabe ( AMNH 261269–261272 ; MSB 55854), 8 km N Exaltación ( AMNH 210403 ) , Magdalena ( FMNH 114714 ) , Mamore River ( AMNH 210409 ) , 4 km SE Palacios (210410), Puerto Caballo ( AMNH 210411 ) , Puerto Siles ( AMNH 210413 , 210414 ) , Río Tijamuchi ( AMNH 261273 ) , San Joaquin ( FMNH 114685 , 114694 , 114707 ) ; Pando, Bella Vista ( MSB 57006, AMNH 262413 ) ; Santa Cruz, 7 km E aserradero Moira ( EBD 8736 ) , 6 km W Asención ( MSB 55855) , Ayacucho ( USNM 390564 ) , Becerra (390565), 2 km N Chapare River mouth ( AMNH 210416 ) , 2 km SE Cotoca ( MSB 59887) , Estancia Cachuela Esperanza ( AMNH 260034 , MSB 55073), Hamecas ( AMNH 135887 ) , La Laguna ( MSB 55856) , 3 km SE Montero ( AMNH 263964 , MSB 67025), Palmar ( USNM 390562 ) , San Miguel Rincón ( AMNH 260037 , MSB 55074, 55075 ), 10 km N San Ramón ( AMNH 261277 , 261278 ) , Santa Cruz de la Sierra ( BMNH 47.11 .22.15 [holotype of crucialis]), 15 km S Santa Cruz ( AMNH 263966 , MSB 58517), 7 km N Santa Rosa ( AMNH 246441 [paratype of olrogi ]), near Warnes ( USNM 390005 , 390009– 390012 ) . Brazil — Acre, Sobral on Rio Juruá ( MVZ 190347 ) ; Amazonas, Auara Igarapé on Rio Madeira ( AMNH 91749 , 91750 ) , Borba on Rio Madeira ( AMNH 91748 ) , Lago Sampaio on Rio Madeira ( AMNH 92761 , 92762 ) , “Santo Antonio de Uayara” on Rio Madeira (= Santo Antonio de Guajará ; AMNH 92293 ) ; Goiás, Anápolis ( AMNH 133043 , 133046 , 133047 , 133055 , 133056 , 133062 , 133064 , 133068–133070 , 133073–133075 , 133082 , 133084–133086 , 133091–133094 , 133096–133101 , 133123 , 133172 , 133171 , 133182 , 133192 , 133195 ) , 24 km SE Formoso ( LACM 10086–10088 ) ; Mato Grosso, Caceres ( USNM 390014 ) , Fazenda São Luis ( MVZ 197403 ) ; Mato Grosso do Sul, Corumba ( USNM 390013 ) , Passo do Lontra ( MVZ 197402 ) ; Rondônia, Porto Velho ( USNM 390001 ) . Colombia — Boyacá, Río Cobaría ( FMNH 92297 ) ; Meta, Finca El Capricho ( KU 123943) , Restrepo ( AMNH 133119 ) , Villavicencio ( AMNH 136168 , 136169 , 139221 ) . Paraguay — Alto Paraguay, Estancia Doña Julia ( TTU 79753) ; Central , 17 km E Luque ( MVZ 144304 ) ; Presidente Hayes, Estancia Loma Porá ( TTU 80404) . Peru — Cusco, Camisea ( MUSM 14150 ) , Hacienda Cadena ( FMNH 66412 , 68332 ) , Quincemil ( FMNH 75094–75096 ) ; Huánuco, Moyuna ( MUSM 83 ) ; Madre de Dios, “Albergue Lodge Cuzco Amazonico” (= Cusco Amazónico ; MVZ 157613 , 165927 ) , Boca Río Colorado ( FMNH 84247 ) , Lago Sandoval ( MVZ 157614 ) , mouth of Río La Torre ( LSUMZ 24591 ) , 6 km W Río Tambopata ( USNM 39002 ) ; 2.75 km E Shintuya ( FMNH 169815 ) ; Pasco, San Pablo ( AMNH 230034 ) , Nevati ( AMNH 230028 , 230030 , 230031 , 254509 ) ; San Martín, Bellavista ( MUSM 92 ) , Moyobamba ( FMNH 19347 [holotype of canus ]), Rioja ( MUSM 88 ) ; Ucayali, Balta ( LSUMZ 12006 , 12008 , 12009 ) , 59 km SW Pucallpa ( USNM 499001 , 499002 ) , Boca Río Urubamba ( AMNH 75906–75908 ) , Lagarto ( AMNH 76636 ) , Santa Rosa ( AMNH 75909 ) . Venezuela — Amazonas, El Platanal ( EBD 8954 , 8956 ) ; Apure, 29 km SSW Santo Domingo ( USNM 418545 , 418546 ) ; Bolívar, 20 km W La Paragua ( USNM 388403 ) , Maripa ( AMNH 16951 ) , Río Yuruán ( AMNH 30709–30714 ) ; Trujillo, 9.8 km NNE Motatán ( KU 120233, 120245 , 120246 , 120251 ) , 19 km W Valera ( USNM 371322 ) ; Zulia, 60 km WNW Encontrados ( USNM 418548 ) .

Figures

FIG. 9. Collection localities of examined specimens of Philander quica, P.canus, and P. pebas. The symbol for sympatry marks localities where P.canus and P. pebas have been collected together.

FIG. 16. Relationships among 46 cytochrome-b sequences of Philander canus and P. pebas. This subtree shows the full details of the cartooned clades labeled “canus” and “pebas” in figure 5.

FIG. 17. Projections of specimen scores on the first two principal components (A) and on factors representing general size and size-invariant shape differences (B) from analyses of craniodental measurements of Philander canus (open triangles) and P. opossum (filled circles). The coefficients of these axes are provided in table 12.

FIG. 18. Dorsal view of the rostrum in Philander canus (A, AMNH 133096) and P. opossum (B, AMNH 96608), illustrating differences in nasal morphology.

FIG. 10. Dorsal pelage of cis-Andean species of Philander compared in the text. From left to right: P. quica (MVZ 183246), P. canus (LACM 10086), P. pebas (MVZ 190343, holotype), P. mcilhennyi (LSU 16393), P. andersoni (LACM 91620), P. opossum (AMNH 266996). The dorsal fur of these species is always grayish or blackish in life, but museum skins often acquire brownish tones after long storage.

FIG. 11. Ventral pelage of cis-Andean species of Philander compared in the text. From left to right: P.quica (MVZ 183246), P. canus (LACM 10086), P. pebas (MVZ 190343, holotype), P. mcilhennyi (LSU 16393), P. andersoni (LACM 91620), P. opossum (AMNH 266996).

FIG. 5. Ultrametric tree from BEAST analysis of cytochrome-b sequences of Philander with putative species represented as cartooned terminals. Dashed vertical line indicates the threshold between Yule and coalescent processes as estimated by the likelihood implementation of the general mixed Yule coalescent model (GMYC). Bases of triangles at branch tips are proportional to the number of sequences belonging to each clade. Filled semicircles at each internal node indicate strong support from Bayesian (BEAST: PP) and maximum-likelihood (GARLI: BS) analyses of these data.