Systematic Review of Endemic Sulawesi Squirrels (Rodentia, Sciuridae), with Descriptions of New Species of Associated Sucking Lice (Insecta, Anoplura), and Phylogenetic and Zoogeographic Assessments of Sciurid Lice

Abstract Analyses of fur color patterns, morphometric data derived from external, cranial, and dental dimensions, and distributions of collection sites for voucher specimens form the basis for a taxonomic revision of Sulawesi's endemic squirrel fauna. Eight species of tree squirrels in Rubrisciurus and Prosciurillus and two species of ground squirrels in Hyosciurus are recognized. All are diurnal and inhabit primary forest formations. Diet consists of fruit, nuts, seeds, and arthropods. Rubrisciurus rubriventer, the largest in body size, forages on the ground and in the lower canopy layer, is found throughout Sulawesi where primary forest persists, and occurs through an altitudinal range embracing tropical lowland evergreen and lower montane rain forests; it is absent from upper montane rain forest. Five species of arboreal squirrels comprise the Prosciurillus leucomus group, a cluster of species occupying the upper forest canopy: P. leucomus, known only from lowland and montane habitats in the northern peninsula and one offshore island; P. alstoni, recorded from lowland tropical evergreen rain forest in the eastern section of Sulawesi's central core, the east-central and southeastern arms, and two southeastern islands; P. weberi, represented by a few specimens from the coastal lowlands of the southern core of Sulawesi; P. topapuensis, endemic to the western mountain block in Sulawesi's central core and occurring along an altitudinal gradient from lowland evergreen rain forest to upper montane rain forest; and P. rosenbergii, the only species of squirrel collected on islands in the Sangihe Archipelago north of the northeastern tip of the northern peninsula. The Prosciurillus murinus group contains two species of small body size: P. murinus, found throughout Sulawesi and in all forest formations, from the coastal lowlands to mountaintops, and a forager in the lower canopy layers; and P. abstrusus, known only from montane forest habitats on Pegunungan Mekongga in the southeastern peninsula. Of two species of ground squirrels, Hyosciurus heinrichi occupies montane forest habitats in the western mountain block of Sulawesi's central core. It is altitudinally parapatric to H. ileile, which inhabits lowland evergreen and lower montane rain forests in the western mountain block and northeastern lowlands of central Sulawesi, and montane forest on the northern peninsula. A slightly revised classification of Sciuridae is provided in which a new tribe, Exilisciurini, is proposed for the Bornean and Philippine Exilisciurus. Previously published results of morphological and molecular analyses point to Rubrisciurus, Prosciurillus, and Hyosciurus as a monophyletic cluster, the Hyosciurina, nested within a larger clade, the Nannosciurini, which along with Exilisciurini n. tribe and Funambulini, comprise the Nannosciurinae, one of the three subfamilies constituting Sciuridae, and one that contains most of the Indomalayan genera. The present diversity of species endemic to Sulawesi was derived from an ancient lineage that crossed a sea barrier from the Sunda Shelf to Sulawesi during the late Miocene. Eight new species of hoplopleurid sucking lice (Insecta, Anoplura) are described as parasitizing 8 of the 10 species of squirrels endemic to Sulawesi: Hoplopleura rubrisciuri from Rubrisciurus rubriventer, Hoplopleura leucomus from Prosciurillus leucomus, Hoplopleura alstoni from Prosciurillus alstoni, Hoplopleura topapuensis from Prosciurillus topapuensis, Hoplopleura murinus from Prosciurillus murinus, Hoplopleura abstrusus from Prosciurillus abstrusus, Hoplopleura heinrichi from Hyosciurus heinrichi, and Hoplopleura ileile from Hyosciurus ileile. Examples of Prosciurillus weberi and P. rosenbergii were surveyed but no lice were recovered. A phylogenetic analysis based on cladistic principles for six species of Sulawesian squirrel lice for which both sexes were available is presented and the results discussed with respect to host relationships. These new data are incorporated into a discussion covering zoogeography of global sciurid-sucking louse associations, emphasizing the Indomalayan squirrel fauna. Globally, members of 11 genera of Anoplura parasitize sciurids, a figure far exceeding the number of anopluran genera associated with any other mammalian family. Nine of these (the enderleinellids, Atopophthirus, Enderleinellus, Microphthirus, Phthirunculus, and Werneckia; the hoplopleurid, Paradoxophthirus; and the polyplacids, Johnsonpthirus, Linognathoides, and Neohaematopinus) are primary parasites of sciurids. The remaining two (the hoplopleurid Hoplopleura, and the polyplacid Polyplax) include representatives that are acquired (secondary) parasites of sciurids—the majority of species in these two louse genera parasitize other groups of mammals but a small number of species have transferred to squirrel hosts. Sciurid hosts and geographic distributions of these 11 anopluran genera are discussed. Historically, representatives of Hoplopleura colonized different sciurid hosts on several separate occasions with one known species on a North American tree squirrel (Sciurus), two described species on North American flying squirrels (Glaucomys), two species parasitizing North American species of chipmunks (Tamias and Eutamias), 14 described species from Indomalayan nannosciurine squirrels (Callosciurus, Tamiops, Rubrisciurus, Prosciurillus, Hyosciurus, and Funambulus), and one species parasitizing a Chinese xerine ground squirrel (Sciurotamias). The zoogeography of the seven sciurid-infesting louse genera known from Southeast Asia is discussed using data from nine different countries or regions (China, Taiwan, Thailand, peninsular Malaysia, Sumatra, Java, Borneo, the Philippines, and Sulawesi). A reduction in the number of sciuirid-infesting anopluran genera and species is apparent from mainland northern/western regions to insular southern/eastern regions with members of seven genera and 23 species described from China but only one genus and eight species from Sulawesi. The absence of known species of Hoplopleura from Bornean and Javanese squirrels suggests that such a fauna may await discovery on one or both of these islands. Six of the eight species of Hoplopleura found parasitizing species of endemic Sulawesi squirrels were recovered as a monophyletic clade from a phylogenetic analysis employing anatomical structures associated with male and female lice. (Two species of Sulawesi Hoplopleura are based on females and nymphs only and were not incorporated into the analysis.) The monophyletic cluster formed by the Sulawesian squirrel lice joined with the monophyletic assemblage containing the three Sulawesi squirrel genera—Rubrisciurus, Prosciurillus, and Hyosciurus—suggest that the ancestral squirrel lineage that arrived in Sulawesi during the late Miocene may have been carrying its unique Hoplopleura parasite.