A review of the flea genus Phalacropsylla Rothschild, 1915 (Siphonaptera, Ctenophthalmidae, Neopsyllinae, Phalacropsyllini) with new host and distributional records

Abstract A redescription of the genus Phalacropsylla Rothschild is provided. Six species are recognized: Phalacropsylla allos Wagner, P. hamata Tipton and Mendez, P. morlani Eads and Campos, P. nivalis Barrera and Traub, P. oregonensis Lewis and Maser, and P. paradisea Rothschild. Phalacropsylla hamata is designated herein as a junior synonym of P. paradisea. The distribution of P. paradisea is more extensive than previously thought, extending from Arizona through southern Colorado, into New Mexico, Texas, and northern Mexico (State of Nuevo León). It is the least host-specific of all species of Phalacropsylla, occurring on 13 different host species including cricetid, heteromyid, murid, and sciurid rodents and several carnivores, although it most commonly occurs on Neotoma albigula Hartley. The range of P. oregonensis is expanded from eastern Oregon to southeastern Idaho. Numerous records are documented for the most common and ubiquitous species, P. allos, which is found in British Columbia, central to northern California, Idaho, Montana, Colorado, Nevada, Utah, Wyoming, Arizona, and New Mexico. Neotoma cinerea Ord is the principal host of P. allos. Phalacropsylla allos is a winter flea west of the Rocky Mountains, but it has been reported in warmer months of the year on the eastern slopes of the Rocky Mountains in Larimer County, Colorado. A distribution map and key are provided for all species in the genus Phalacropsylla.


Introduction
The flea genus Phalacropsylla Rothschild, (Neopsyllinae: Phalacropsyllini) is represented by six species (P. allos Wagner, P. hamata Tipton and Mendez, P. morlani Eads and Campos, P. nivalis Barrera and Traub, P. oregonensis Lewis and Maser, and P. paradisea Rothschild). Recent phylogenetic studies based on morphology and molecular characters found that the tribe Phalacropsyllini may be divided in two genera: Phalacropsylla and Strepsylla Traub the former in western North America, the latter in Central America (Acosta and Morrone 2013). During the current study, many previously undocumented specimens of Phalacropsylla were examined from the Brigham Young University flea collection (BYUC) and the collection of the late Glenn E. Haas (now a part of the BYUC). Many of those specimens were collected from nests and those important associated host relations are discussed. The validity of several species of Phalacropsylla is addressed and the original generic description by Rothschild (1915) which was supplemented by Eads and Campos (1982) is expanded.

Materials and methods
Specimens were obtained on loan from the following institutions: Brigham Young University flea collection, Monte L. Bean Life Science Museum, Brigham Young University, Provo, Utah, USA (BYUC); The Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA (CMNH); Colección de Siphonatera, Museo de Zoología, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de Mexico, Mexico (MZFC-S); the Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA (USNM).
The most stable and representative characters for the genus Phalacropsylla are found in the modified abdominal segments of the male [T-IX (basimere and telomere), distal arm of S-IX, and the aedeagus]. The majority of Phalacropsylla listed under "Materials Examined" that are listed as part of the BYUC was part of the Glenn E. Haas flea collection. A designated collector for most of the fleas from his collection was not indicated on his slides but were undoubtedly collected by him. The map was prepared with ESRI ® ArcGIS version 10.5. Flea images were illustrated with the aid of an Olympus BX61 Compound Microscope and an Olympus CC12 digital camera accompanied with an Olympus Microsuite™ B3SV program.

Siphonaptera Ctenophthalmidae, Phalacropsyllini
Phalacropsylla Rothschild, 1915Phalacropsylla Rothschild, 1915Ewing, 1924Ewing, : 346, 1930Jordan, 1937: 268;Ewing & Fox, 1943: 85;Hubbard, 1947: 338;Traub, 1950: 76;Hopkins & Rothschild, 1962: 299;Eads & Campos, 1982: 243-244;Holland, 1985: 125. Genotype. Phalacropsylla paradisea Rothschild, 1915 Description. Frons broadly rounded, without frontal tubercle. Inter-antennal suture (falx) well developed in both male and female. Antennal groove shallow, opened posteriorly. Antenna asymmetrical, extending onto prosternosome in male, female antenna shorter. Margin of pedicel with short setae, none extending much beyond base of clavus. Occipital area with three oblique rows of setae. Pre-antennal area (anterior to eye) with two rows of setae. Head lacking setae below or posterior to eye. Eye elliptical and pigmented; central unpigmented sinus present. Eye contiguous with two overlapping, darkly pigmented spines; lateral anterior spine broader and shorter than longer narrow mesal spine. Maxilla very elongated, extending half the length of forecoxa. Labial palpus long, extended to or beyond apex of trochanter. Pronotum with complete row of long setae anterior to 14-18 broad, bluntly pointed ctenidial spines. Mesonotal collar with several pseudosetae per side. Pleural arch well developed [an unusual characteristic for a true nest flea, Eads and Maupin (1982), Lewis and Maser (1978), and Barrera and Traub (1967)]. Suture dorsad to lateral mesonotal area expanded into a distinct rounded incrassation at posterior margin abutting pleural arch. Meso-and metasterna protruding downward producing a lobe between coxae (especially so in metasternum). Meso-and metacoxae with three long stout setae at apico-caudal margin. Fore tibia with six dorsal notches; mid-and hind tibiae each with seven dorsal notches. Distotarsomeres each with four pairs of plantar bristles with a fifth pair shifted onto plantar surface between first proximal lateral pair. More anterior terga with small marginal pigmented spinelets. Terga with two rows of slender setae; anterior row small and posterior main row long with intercalaries. Abdominal spiracles blunt at apex. Three long antesensilial bristles; middle bristle longest of three. Sensilium slightly convex; with 12 sensilial pits per side. Eighth tergum of female with caudal lobe bearing marginal row of five to seven stout long setae and six to eight short stout, more anterior setae. Eighth tergum reduced in male. Caudal margin of female S-VII with rounded dorsal lobe sub-tended by broad sinus. Bulga of spermatheca pyriform with slender hilla much longer than bulga. Duct of bursa copulatrix narrow, longer than spermatheca, sclerotized, with apical hyaline bursa copulatrix. Male distal arm of S-IX club-shaped; broader at apex than proximal portion. Always bearing various arrangements of spiniform setae near apex. Male basimere very broad and robust; manubrium narrow and elongated with parallel sides. Basimere not divided into lobes but may or may not possess a sinus on ventral margin. Telomere narrow (at least five times as long as widest dimension); fovea variously placed on dorsal margin. Aedeagus structurally narrower at apex than at middle. Crochet and dorsal armature on sclerotized inner tube present.
Remarks. Phalacropsylla allos is the most widely spread species of Phalacropsylla, occurring in southern British Columbia, Arizona, central to northern California, Colorado, Idaho, Montana, Nevada, New Mexico, Utah, and Wyoming (Fig. 1). It is sympatric with P. paradisea in Arizona, Colorado, and New Mexico. The vast majority of specimens examined were recorded from N. cinerea throughout it range, with single records from N. mexicana (1♂), Onychomys leucogaster (2♀), and P. maniculatus (1♂, 1♀). No other species of Phalacropsylla have been collected from N. cinerea (Table 1). Most of the specimens from nests of N. cinerea were collected during the cooler fall and winter months from September through February. Only one collection of three males was reported in a warmer period (June) and this site was inside a cool mine shaft (Buckley Mine) located at an elevation of 2896 m. We did not examine specimens of P. allos reported by Eads and Campos (1982) from N. mexicana (1♂),   Peromyscus difficilis (J.A. Allen) (3♂, 1♀), P. maniculatus (1♂, 1♀), Reithrodontomys megalotis (Baird) (1♀) from Larimer County, Colorado; however, these specimens reported from the eastern slopes as P. allos by Eads and Campos (1982) were collected from March through August during the warmer months at elevations from 1600-1900 m. Although they collected during all months of the year, P. allos specimens were not collected from September through February. This seasonal disparity is enigmatic and warrants future collecting and studies.

Phalacropsylla morlani Eads & Campos, 1982
Phalacropsylla morlani Eads & Campos, 1982: 241-243;Lewis & Lewis, 1985: 149;Adams & Lewis, 1995: 68;Fagerlund et al., 2001: 95;Ford et al., 2004: 16. Diagnosis. The apico-ventral margin of the basimere is entire, without a sinus, a feature shared only by P. allos and P. oregonensis (Figs 2, 4). Readily distinguished from both by the shape of the distal arm of S-IX which is wider basally than at apex. The apex of the distal arm of S-IX (DA9) also lacks modified long spiniform setae, as in P. allos, whereas P. oregonensis possesses modified setae (Fig. 4). The female of P. morlani has not been described. Remarks. The description of P. morlani was based on one male from Santa Fe County, although Eads and Campos (1982) indicated that a second male had been lost. The discrepancy in the month the holotype was collected (October or November) was not resolvable. Eads and Campos (1982) stated correctly in their diagnosis that P. morlani has a pronotal comb of 18 teeth but erroneously recorded 20 in their key (couplet 6.). Although P. allos is documented from adjacent Bernalillo and Sandoval counties, P. allos has not been found in Santa Fe County. Dedicated collection efforts are needed to determine if P. allos and P. morlani are sympatric at high elevations in Santa Fe County and to collect and describe the female and additional males of P. morlani. Since P. morlani was collected from a pika (O. princeps), additional collecting might best be directed at collecting both O. princeps and N. cinerea in Santa Fe County.
Remarks. Known only from type material from Popocatépetl mountain, Mexico. Specimens were taken from two different hosts: Neotoma and Peromyscus. Phalacropsylla nivalis is the most extreme southern species of the genus, occurring many hundreds of kilometers from its closest allied species, P. paradisea.
Of the two species whose lobes on the margin of S-VII are wider than long, the lobe of P. oregonensis is more triangular, bluntly pointed, and curved downward than that of P. paradisea. The latter is broadly rounded at apex.  Thomas, 15 V 1975, C.O. Maser, holotype ♂ USNM No. 75247; same data except P. maniculatus, allotype ♀ [MWH re-mounted holotype and allotype, as original medium was crystalized] (USNM).
Remarks. Tipton and Mendez (1968) described P. hamata from one male from Cerro Potosí, Nuevo León, Mexico. Eads and Maupin (1982) described the female of P. hamata from two specimens collected from Bernalillo County, New Mexico and considered an additional four males as P. hamata. These were collected from Peromyscus leucopus (Rafinesque) and N. albigula. With the recent accession of the Glenn E. Haas flea collection (now part of the BYUC), many specimens of Phalacropsylla were available for study from the vast areas of Arizona, Colorado, New Mexico, and Texas. These specimens were identified as either P. hamata or P. paradisea. While studying this material, it was impossible to distinguish females accurately from one or the other. To date, males have been distinguished primarily by the presence of various numbers of long spiniform setae on the apico-ventral margin of the distal arm of S-IX. The diagnosis of the male of P. hamata provided by Tipton and Mendez (1968) included: 1) A deep sinus in the caudal margin of the immovable process of the clasper (basimere), 2) four long bristles on the apical and subapical portion of basimere, 3) two hook-like spiniform setae near the apex of the distal arm of S-IX, and 4) the bifid portion of the proximal arm of S-IX as angulate. The sinus on the caudal margin of the basimere, long bristles on the apex of basimere, the number of hook-like spiniform setae present at the apex of the distal arm of S-IX, and shape of the bifid portion of proximal arm of S-IX, each proved to be quite variable within series from the same study sites and even among specimens from the same host. Based on these comparative studies, we concluded that P. hamata is not a valid species and consider it to be a junior synonym of P. paradisea. Phalacropsylla paradisea is representative of the genus in the southern portion of its distribution with records ranging from central Arizona, southern Colorado, through New Mexico, Texas, and into northern Mexico. Phalacropsylla nivalis is the only species occurring further south than P. paradisea. Although P. allos is the most commonly collected species of Phalacropsylla, P. paradisea has been collected from a much more diverse group of rodent host species (n = 10) ( Table 1).
During studies on plague in the Western United States by the U.S. Army in the mid-1970s, the junior author (MWH) identified two specimens (previously unreported) of P. paradisea that were collected on N. albigula (one specimen among 37 hosts examined) and Peromyscus boylii (Baird) (one from 10 hosts examined) from Fort Huachuca, Cochise County, Arizona. Although the whereabouts of these two specimens are unknown, they are documented in unpublished reports of the U.S. Army Environmental Hygiene Agency-Regional Division West, Aurora, Colorado.
In the latter years of his life, Dr. Glenn Haas concentrated his studies on the fleas in nests of small mammals, primarily the nests of Neotoma and arboreal Tamiasciurus. He placed the nests in breathable paper grocery bags, maintained humidity with moist paper towels, and meticulously hand-picked the emerging adult fleas over a period of weeks and months. Thus many of his mounted specimens were teneral and often not yet expanded from their recent pupal state. These "rearing" studies document the importance of species of Neotoma, particularly N. albigula, as the primary hosts of P. paradisea.

Key to males of Phalacropsylla
The key to females of Phalacropsylla by Eads and Maupin (1982) is adequate; however, all existing keys to males requires simplification. Therefore a key for the male sex follows.