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Stick-Tight Fleas in the Nostrils and Below the Tongue: Evolution of An Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2007? 2007 1491 117137 Original Article EXTRAORDINARY INFESTATION SITE IN HECTOPSYLLAS. M. BLANK ET AL. Zoological Journal of the Linnean Society, 2007, 149, 117–137. With 28 figures Stick-tight fleas in the nostrils and below the tongue: evolution of an extraordinary infestation site in Hectopsylla (Siphonaptera: Pulicidae) STEPHAN M. BLANK1*, CHRISTIAN KUTZSCHER1, JUAN F. MASELLO2,5, ROBERT L. C. PILGRIM4 and PETRA QUILLFELDT3,5 1Deutsches Entomologisches Institut im ZALF, Eberswalder Strasse 84, 15374 Müncheberg, Germany 2University of Bristol, School of Biological Sciences, Ecology of Vision Group, Woodland Road, Bristol BS8 1UG, UK 3Cardiff University, School of Biosciences, Main Building, Museum Avenue, PO Box 915, Cardiff CF10 3TL, UK 4Department of Zoology, University of Canterbury, PB 4800, Christchurch, New Zealand 5Max Planck Institute for Ornithology, Vogelwarte Radolfzell, Schlossallee 2, 78315 Radolfzell, Germany Received August 2005; accepted for publication January 2006 Association with terrestrial mammals as hosts and a sessile mode of life in females are ground plan traits of the stick-tight fleas associated with Hectopsylla + Tunga. Hectopsylla comprises the lineages H. pulex + [H. psittaci- group + H. broscus-group]. The stem species of the H. psittaci-group has switched to birds. Hectopsylla narium sp. nov. infests the nestlings of the burrowing parrot (Cyanoliseus patagonus patagonus; Psittacidae). The infestation sites inside the nasal cavity, and later during the breeding season also below the tongue, are unique among fleas. These sites provide a concealed habitat for the sessile, immobile females, where they are safe against cleaning activ- ities of their host and the host’s parents. The fleas are able to disperse actively within the bird colony. Their dispersal over long distances can only be assumed to happen accidentally, as fleas have never been found on adult parrots dur- ing field studies in Río Negro, Patagonia, Argentina. Data on the species bionomics, morphological descriptions and illustrations, and an identification key for H. narium and related taxa are presented. A lectotype is designated for H. psittaci. The family group name Tunginae is proposed as a new synonym of Hectopsyllinae. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 117–137. ADDITIONAL KEYWORDS: bionomics – host relationship – identification – morphology – new species – phy- logeny – Psittaciformes – spatial dispersal – Tunga penetrans. INTRODUCTION endoparasitic adaptation (Hopkins & Rothschild, 1953; Holland, 1964; Cheetham, 1988). The species of The pulicid stick-tight fleas are commonly known from this clade have a Neotropic origin (including Mexico). the sand flea Tunga penetrans (Linné, 1758), which Tunga Jarocki, 1838 comprises eight Neotropic and causes a human disease called tungiasis. Females typ- two Chinese species and Hectopsylla Frauenfeld, 1860 ically infest the feet, where they burrow into the skin 13 Neotropic species. Tunga and most Hectopsylla spe- and attach with their heavily denticulate maxillary cies appear to be restricted to terrestrial mammals as laciniae (Heukelbach, 2004). The sessile mode of life their primary hosts, but three Hectopsylla species are is typical for females of Tunga and of its sister-group associated with birds and one with bats (Hopkins & Hectopsylla, although Tunga exhibits an extreme Rothschild, 1953; Hastriter & Méndez, 2000; our present data). In a project ongoing since 1998, extensive studies on *Corresponding author. E-mail: [email protected] the life history of the burrowing parrot Cyanoliseus © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 117–137 117 118 S. M. BLANK ET AL. patagonus patagonus (Vieillot, 1818) have been con- long stick. Adult fleas (140ǩ and 830Ǩ) were collected ducted in Argentina (e.g. Masello & Quillfeldt, 2004a, from nestlings of the parrot and from nest material. b; Masello et al., 2004). In a breeding colony near the For light microscopic study some of the adults were village of El Cóndor (province of Río Negro, Patagonia) mounted in Canada balsam on slides. Larvae (34) nestlings in particular have been regularly examined were collected from the sandy bottom of the nest for ectoparasites. Two chewing lice species (Phth- chamber. The larvae were prepared and stained by iraptera; Mey, Masello & Quillfeldt, 2002) and a using Pilgrim’s (1992) method and mounted in Canada parasitic bug species (Heteroptera; J. Deckert, ZMHB, balsam. The drawings were produced using a camera Berlin, Germany, personal communication) have been lucida and digital photographs. For the SEM study of detected. During the investigation single fleas have the male genitalia whole specimens were dehydrated accidentally been discovered fleeing from nostrils and stepwise with ethanol (70–98%) and acetone (100%), bills of the nestlings. Closer scrutiny revealed that the critical-point dried, mounted on minute pins with con- fleas infest the nasal cavity and the area below the ductive glue or fixed on conductive pads, and sput- tongue, which is a unique phenomenon among fleas. tered with gold and palladium. Coating was repeated The fleas collected from more than 200 parrot nest- after the stepwise dissection of sclerites and control of lings turned out to belong to a new Hectopsylla spe- the dissection result by SEM. Images were made on cies, H. narium sp. nov. the SEM JSM-6060LV (JEOL) mostly at 8 kV acceler- We describe and illustrate this new species and pro- ation voltage. vide a key to the Hectopsylla species occurring on The following abbreviations are used in the figures birds and bats. The outline of the bionomics of (terminology mostly after Snodgrass, 1946; Cheetham, H. narium is the most detailed existing for a Hectop- 1988): bcl, body of clasper; cr, crochet; dls, dorsal lon- sylla species. It includes data on the larva, which are gitudinal strut; fs, Ford’s sclerite; l1, l2, l3, distal arm the first reported for a species of Hectopsylla. A phy- of sternum 9, lobe 1, 2, 3; lc, lacinia (maxillary stylet); logenetic hypothesis for the evolution of the major lin- man1, man2, manubrium 1 and 2; msp, lateral process eages of Hectopsylla is presented, which provides a of mesosternum; mtp, metepimeron; mts, metepister- scenario for the switch of host associations within this num; mxl, palpus-bearing lobe of maxilla; mxp, max- taxon. New faunistic and bionomic data and taxo- illary palpus; p1, p2, p3, process 1, 2, 3 of clasper; nomic notes on selected Hectopsylla species are pa9, proximal arm of sternum 9; pha, phallosome included. (= aedeagus); pmtp, process of metepimeron; pop, pos- toral process; psp, lateral process of prosternum; rd, rod of closing apparatus of spiracle; sit, sclerotized MATERIAL AND METHODS inner tube; sen, sensilium; st, sternum; stf, stalk of the Adults and larvae of Hectopsylla narium were col- fulcrum; t1, t2 . , tergum 1, tergum 2 . ; tra, tra- lected during field studies on the breeding biology of chea; utp, unguitractor plate. the Patagonian race of the burrowing parrot, Cyanol- Counts of setae and pits refer to one body side iseus patagonus patagonus (Psittacidae). The studies unless expressively stated otherwise. Variable ranges were carried out in the largest colony and most impor- are noted in the pattern ‘7–8 (6–10) setae’, meaning tant breeding site of the parrot species from October that most specimens bear 7–8 setae but 6–10 setae 1998 to February 1999, November 1999 to January may be observed on the whole sample. 2000 and November 2001 to January 2002. The stud- The identification of H. narium required the study ied colony covers 9 km of sandstone cliffs at the Atlan- of some similar taxa. Collection material, which tic coast near the village El Cóndor, province of Río belongs to the following institutions, has been stud- Negro, Patagonia (Masello & Quillfeldt, 2004a). The ied: BMNH, The Natural History Museum, London, cliffs are characterized almost exclusively by grey or UK (T. Howard); DEI, Deutsches Entomologisches yellowish sandstone (Angulo & Casamiquela, 1982). Institut, Müncheberg, Germany; FMNH, Field The colony is the largest known colony for the entire Museum of Natural History, Chicago, USA (P. P. Psittaciformes and contains about 35 000 active nests Parrillo); NHMW, Naturhistorisches Museum Wien, (Masello et al., 2006). The parrots excavate their own Vienna, Austria (U. Aspöck); RLCP, R.L.C. Pilgrim nest burrows by tunnelling into faces of the cliff. The Collection, Department of Zoology, University of Can- nests are 0.8–3.0-m-long, depressed cylinders in the terbury, Christchurch, New Zealand; USNM, United sandstone’s softest layers, terminating in the nest States National Museum, Washington DC, USA (N. chamber (Leonardi & Oporto, 1983). Adams); ZSM, Zoologische Staatssammlung, Munich, Continuous observations inside nest tunnels were Germany (E.-G. Burmeister); ZMHB, Museum für carried out using a miniature security camera Naturkunde der Humboldt Universität, Institut für (Masello et al., 2001). Samples of the sandy bottom of Systematische Zoologie, Berlin, Germany (H. Wendt); the nest chamber were taken using a spoon fixed to a ZMUH, Zoologisches Institut und Museum der © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 149, 117–137 EXTRAORDINARY INFESTATION SITE IN HECTOPSYLLA 119 Universität Hamburg, Germany
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