Journal of Medical Entomology Advance Access published August 4, 2015 VECTOR/PATHOGEN/HOST INTERACTION,TRANSMISSION The Fleas of Endemic and Introduced Small Mammals in Central Highland Forests of Madagascar: Faunistics, Species Diversity, and Absence of Host Specificity STEVEN M. GOODMAN,1,2,3 H. RICO RANDRENJARISON ANDRINIAINA,4 2 5 VOAHANGY SOARIMALALA AND JEAN-CLAUDE BEAUCOURNU J. Med. Entomol. 1–9 (2015); DOI: 10.1093/jme/tjv113 ABSTRACT Data are presented on the flea species of the genera Paractenopsyllus (Ceratophyllidae, Leptopsyllinae) and Synopsyllus (Pulicidae, Xenopsyllinae) obtained from small mammals during two 2014 seasonal surveys at a montane humid forest site (Ambohitantely) in the Central Highlands of Madagascar. The mammal groups included the endemic family Tenrecidae (tenrecs) and subfamily Nesomyinae (rodents) and two introduced families Muridae (rodents) and Soricidae (shrews); no fleas were recovered from the latter family. The surveys were conducted at the end of the wet and dry seasons with 288 individual small mammals captured, including 12 endemic and four introduced species. These animals yielded 344 fleas, representing nine species endemic to Madagascar; no introduced species was collected. Some seasonal variation was found in the number of trapped small mammals, but no marked difference was found in species richness. For flea species represented by sufficient samples, no parasite– host specificity was found, and there is evidence for considerable lateral exchange in the local flea fauna between species of tenrecs and the two rodent families (endemic and introduced). The implications of these results are discussed with regards to small mammal species richness and community structure, as well as a possible mechanism for the maintenance of sylvatic cycles of bubonic plague in the montane forests of Madagascar. KEY WORDS fleas, species richness, seasonality, Ambohitantely, small mammal While considerable advances have been made in the hedgehog-like animals that are part of the Afrotheria past few decades on the taxonomy of fleas parasitizing radiation (Springer et al. 1997; Stanhope et al. 1998) native and introduced small mammals of Madagascar and the endemic rodent subfamily Nesomyinae, with (Duchemin 2003a, b, 2004; Duchemin and Ratovonjato 27 currently recognized species placed in the family 2004; Hastriter and Dick 2009; Beaucournu and Good- Nesomyidae (Musser and Carleton 2005; Soarimalala man 2014), little is known about their ecology and lev- and Goodman 2011). Within the Tenrecidae is the spe- els of host specificity. Such information is important ciose genus Microgale, often referred to as shrew- from a medical entomology perspective, as portions of tenrecs, with 23 species and, among the Nesomyinae, Madagascar, particularly the Central Highlands, have the genus Eliurus with 12 species (Soarimalala and reoccurring epidemics of bubonic plague in humans Goodman 2011). These two mammalian groups are transmitted by fleas (Duplantier et al. 2005; Chanteau respectively monophyletic and each can be explained 2006; Andrianaivoarimanana et al. 2013), as well as pro- by a single colonization event of the island and subse- viding insights into the evolutionary history of these quent adaptive radiations (Poux et al. 2008). In Mala- ectoparasites and their mammalian hosts. gasy humid forests, considerable small mammal species The native nonvolant small mammals of the island diversity occurs at the same site and many taxa live in are placed in the endemic family Tenrecidae, com- near sympatry. For example, in the montane forest at posed of 32 different species of shrew-like or Tsinjoarivo in the Central Highlands, 17 species of Ten- recidae, including 13 Microgale, have been docu- mented in close proximity (Goodman et al. 2000). A few small mammal species have been introduced 1 Field Museum of Natural History, 1400 South Lake Shore Drive, to Madagascar and include three Muridae rodents, Chicago, IL 60605. 2 Association Vahatra, BP 3972, Antananarivo 101, Madagascar. Mus musculus, Rattus rattus,andR. norvegicus;the 3 Corresponding author, e-mail: [email protected]. second taxon has broadly invaded native forest forma- 4 De´partement de Biologie Animale, Universite´d’Antananarivo, BP tions and occurs in sympatry with tenrecs and neso- 906, Antananarivo 101, Madagascar. myine rodents (Soarimalala and Goodman 2011). The 5 Laboratoire de Parasitologie et Zoologie applique´e, Faculte´de Me´decine, et Institut de Parasitologie de l’Ouest, 2 Ave., du Profes- second introduced group includes two species of Sorici- seur Le´on Bernard, F-35043 Rennes cedex, France. dae shrews, Suncus etruscus and S. murinus,bothof VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] 2JOURNAL OF MEDICAL ENTOMOLOGY which occur in urban, rural, and native forest habitats Small Mammal Collection. Different trap types (Hutterer and Tranier 1990; Omar et al. 2011; Soarima- were used to capture small mammals: 1) two styles of lala and Goodman 2011). The island’s endemic flea live traps, Sherman (LFA folding trap, H. B. Sherman fauna is relatively rich, only a few introduced species Traps, Tallahassee, FL) and National (201 collapsible are present (Duchemin et al. 2003), and new species to trap, Tomahawk Live Trap, Hazelhurst, WI), intended science continue to be described (Hastriter and Dick to capture Nesomyinae and Muridae rodents and to a 2009; Beaucournu and Goodman 2014). lesser extent Tenrecidae; and 2) pit-fall buckets used The notable level of simplicity of this system, with to trap Tenrecidae and to a lesser extent rodents. regard to the origin of the native small mammal fauna, This latter type of trap was composed of 11 plastic two colonization events followed by extensive specia- buckets, each with a capacity of 15 liter, placed 10 m tion, relatively high sympatric species diversity, and apart, buried in the earth, so that the upper many taxa having broad geographical distributions, pro- rim was flush with the ground surface, and with a vides a natural experiment in testing patterns of specif- 100-m-long 0.75-m plastic drift fence stapled to icity between ectoparasites and their small mammal vertical posts and bisecting each bucket. For further hosts. These patterns overlaid on the fleas of intro- information on these different trapping techniques, see duced small mammals, specifically those that occur in Raxworthy and Nussbaum (1994) and Goodman and sympatry with the native fauna, provide the means to Carleton (1996). contrast cospeciation between fleas and their hosts, as A live trap in place for a 24-h period, from dawn to compared to lateral transfer across different small dawn, is considered one “trap night” and a pit-fall mammal families. Further, these patterns might pro- bucket in place during the same period is a referred to vide insight into the circulation of bubonic plague, par- as “pit-fall trap night”. Research involving live animals ticularly what has been referred to as the “wild” or followed guidelines for the capture, handling, and care “sylvatic” cycle in natural forest areas of highland of mammals approved by the American Society of Madagascar (Chanteau 2006). Mammalogists (Sikes et al. 2011). Research permits for On the basis of flea collections from small mammal the capture and collection of small mammals were hosts made at a montane humid forest in the Central issued by Direction du Syste`me des Aires Prote´ge´es, Highlands of Madagascar, during dry and wet season Direction Ge´ne´rale de l’Environnement et des Foreˆts, visits, we examine herein the following five aspects: 1) and Madagascar National Parks (N 077/14/MEEF/ document the species of fleas occurring on the native SG/DGF/DCB.SAP/SCB and 238/14/MEEF/SG/DGF/ and introduced small mammal fauna; 2) investigate the DCB.SAP/SCB) and following regulations of Malagasy level of specificity of different flea species with regards national authorities. Captured mammals were identi- to their small mammal hosts to examine possible para- fied based on the long-term experience of two of the site–host coevolution; 3) determine possible seasonal coauthors (S.M.G. and V.S.), as well as the published aspects of parasitism; 4) ascertain possible ectoparasite literature (e.g., Carleton 2003; Jenkins 2003; Olson transfers between native and introduced small mam- et al. 2004; Soarimalala and Goodman 2011). On one mals; and 5) consider different life history traits of the occasion during the March–April survey, too many island’s small mammal community to explain some small mammals were captured during the night that observed patterns. Aspects concerning the flea fauna of could be processed the following morning and, in this Ambohitantely, specifically taxonomic considerations case, 8 of 25 R. rattus were not examined for their associated with this collection, are presented elsewhere ectoparasites. However, this should not have biased any (Beaucournu et al. 2015). interpretation of the fleas occurring on these rodents, as in total 112 of the 122 R. rattus captured were inspected for fleas (see below). Small mammal voucher Materials and Methods specimens were deposited in the Field Museum of Study Site. Small mammal surveys were conducted Natural History (FMNH), Chicago, and the Universite´ during two different visits in 2014 to the Ambohitantely d’Antananarivo, De´partement de Biologie Animale Forest (Fig. 1). The inventoried