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New bird host records for Ornithoctona fusciventris (Diptera: Hippoboscidae) in Mexico.

The family Hippoboscidae Samouelle, 1819, includes more than 150 species of obligate blood-feeding ectoparasites on birds and mammals (Maa and Peterson, 1987). There are 13 genera distributed in the Americas; all except Hippobosca Linnaeus (represented by one introduced species) are known in the Neotropical region (Wood, 2010). Information on louse flies occurring in Mexico is scarce, with nearly all the information summarized by Lopez Campos (1988).

In addition to the direct effects that blood-sucking flies have on hosts due to their bites, louse flies are known vectors of avian pathogens such as Trypanosoma and Haemoproteus (Baker, 1967; Santiago-Alarcon et al., 2012). The earliest record of a hippoboscid fly acting as vector of an avian Haemoproteus parasite was by Aragao (1908; see also Adie, 1915) and, more recently, other bird pathogens transmitted by hippoboscid flies have been detected (e.g., Haemoproteus multipigmentatus, Valkiunas et al., 2010; Santiago-Alarcon et al., 2012). Hence, this fly family has important implications for wild and domestic animal health, and their study falls within the framework of conservation medicine (Aguirre et al., 2012). In this work, we report new host records for the louse fly Ornithoctona fusciventris (Wiedemann, 1830) (Diptera: Hippoboscidae), the infection prevalence of this fly parasite on birds captured in the surroundings of Xalapa City in the state of Veracruz, Mexico, and a positive infection with haemosporidian parasites for one of the birds parasitized by O. fusciventris.

We conducted this study in central Veracruz, Mexico during 2013 and 2014. Our sampling sites are located in the surroundings of Xalapa City, including the municipality of Coatepec, and San Andres Tlalnelhuayocan (Fig. 1). The climate of this region is humid and mild with three seasons: a cold moist season from November-March, a warm dry season during April and May, and a rainy season from June-October. Mean annual precipitation is 1,500-1,650 mm; mean annual temperature is 14-16[degrees]C (Williams-Linera et al., 2002). Currently, the region is composed of a matrix dominated by shade coffee plantations, cattle ranches, secondary forest patches, and cities that are rapidly expanding (Williams-Linera, 2007). Our sampling sites include an urban green area (Molinos de San Roque) located inside Xalapa City, a suburban forest (Santuario de Bosque de Niebla) located in the periphery of Xalapa City, a shade coffee plantation and a cloud forest in the Municipality of Coatepec, and a cattle pasture surrounded by patches of cloud forest and second growth vegetation in San Andres Tlalnelhuayocan (Fig. 1).

We captured birds during the dry (March-April) and rainy (June-July) seasons in 2013 and 2014 using 10 mist nets of 12 x 2.5 m. We sampled each site for at least 5 h a day for 5 days, with a total of 25 sampling days per season. Mist nets were opened at dawn and closed at noon. We thoroughly examined the plumage of each captured bird searching for hippoboscid flies. Diptera ectoparasites were retrieved with care from the bird's body surface, preserved in 70% ethanol, and labeled with the field and host information. Hippoboscids were studied with the use of an SMZ800 Nikon stereomicroscope (Nikon Instruments Inc., Melville, New York) and identified following the taxonomic treatments of Maa and Peterson (1987) and Wood (2010) for generic level and Maa (1969a) for species level.

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We extracted DNA from blood of those birds parasitized by hippoboscids using the DNeasy blood and tissue extraction kit, QiagenT (Qiagen, Hilden, Germany) following manufacturer's instructions. We performed a nested PCR with specific primers for haemosporidian parasites (Hellgren et al., 2004) to determine infection status and to amplify a fragment of the mtDNA cytochrome b gene (~480 bp) of Plasmodium, Haemoproteus, and Leucocytozoon parasites. Due to lack of funding, we did not send out positive samples to sequence. We did not have a blood sample for the Basileuterus rufifrons individual because the fly parasitizing this bird was provided to us from another project taking place in the same area; hence, only blood samples for Sayornis nigricans and Chlorospingus flavopectus were screened for haemosporidians.

We captured a total of 1,616 birds belonging to 61 genera and 79 species. Hippoboscid flies parasitized only three birds of different species. In the two sampling years, we detected an infection prevalence of 0.6% in C. flavopectus (n = 150), 1.8% in B. rufifrons (n = 56), and 50% in S. nigricans (n = 2). We collected one fly specimen per each host; all hippoboscid specimens corresponded to O. fusciventris (Wiedemann, 1830). We found a positive infection by Plasmodium/Haemoproteus parasites in C. flavopectus.

Genus Ornithoctona Speiser, 1902, is recognized by the following characteristics: antennal pedicel, as viewed from above, broadened, leaf-like, 2-3 times as long as wide; antennae separated from each other by less than width of one antenna; thoracic sterna bare or at most with soft recumbent setae; scutellum with less than 30 anterior short bristles which are not arranged to form a comb; laterotergite without prominent projection; wings functional, with vein Cu[A.sub.2] forming a closed cell cup and tarsi with apical tooth of claw deeply cleft so the entire claw seems trifid (Wood, 2010).

Details of O. fusciventris (Wiedemann, 1830) material examined are as follows: Mexico, Veracruz, municipality of Xalapa, Santuario Bosque de Niebla (19[degrees]30'52"N, 96[degrees]56'12"W; 1,344-1,372 elevation); 25 February 2013, ex Chlorospingus flavopectus, D. Santiago-Alarcon, col./F. Gonzalez, bird det./S. Ibanez-Bernal, insect det. 1 [female]; 23 October 2013, ex Basileuterus rufifrons, C. Hernandez-Lara, col./D. Santiago-Alarcon, bird det./S. Ibanez-Bernal, insect det. 1 [female]; municipality of Coatepec, Rancho Viejo, Rancho Don Felix (19[degrees]31'37"N, 96[degrees]59'7"W; 1460-1525 elevation), potrero, 5 March 2013, ex Sayornis nigricans, D. Santiago-Alarcon, col./F. Gonzalez, bird det./S. Ibanez-Bernal, det. 1 [female] (material deposited in Instituto de Ecologia, A. C.).

Diagnosis of material examined is as follows: female, interocular space wider than eye; posterior orbit length as long as greatest width of inner orbit; anterior ocellus situated at level of posterior margin of eye; antennal flagellomere with outer margin evenly convex; wing 5.5-7.5 mm long, cells [r.sub.3] and mx covered with setulae at least in part, as well as apex of [r.sub.2]; humeral callus with sparse setae, longer than 2.0 times the length of the great diameter of anterior spiracle; anterior mesosternal process narrow, longer than basal width; scutellar anterior bristles weak; sternum 1 about 0.75 times as long as wide, basal margin widest; sclerites of tergum 6 small, about 0.20-0.23 mm in length and width, bearing 2-4 moderately strong bristles; setae on membranous interspace between ventilator openings 3 and 5 more than two times as long as those on dorsal area of the abdomen; with 3 median tergal plates; basal papillae of bristles at sides and apex of abdomen less than 0.5 as wide as spiracles; posterior marginal bristles of laterite 2 long and strong (Maa, 1969 a).

Twelve species of Ornithoctona are recognized worldwide (Wood, 2010). Maa (1969a) reviewed this genus and presented a key for 11 species. Five species are distributed in the Americas, with four reported in Mexico: Ornithoctona erythrocephala (Leach, 1817), O. fusciventris (Wiedemann, 1830), Ornithoctona nitens (Bigot, 1885), and Ornithoctona orizabae (Bequaert, 1953). In the present study only three specimens of O. fusciventris were found.

Ornithoctona fusciventris is distributed from Canada (Quebec) and Washington (United States) south to Argentina (Maa, 1969a, 1969b) and Chile (Lopez Campos, 1988). In Mexico it has been reported from the state of Oaxaca (Sierra Madre del Sur, Rio Molina, ex Cypseloides rutilus (=Streptoprocne rutila (Vieillot, 1817)) (Apodiformes: Apodidae) [Maa, 1969a]); from Chiapas, localities of Santa Rosa and San Cristobal de las Casas, ex Junco phaeonotus fulvescens (Wagler, 1831) (Passeriformes: Emberizidae), Piranga leucoptera leucoptera (Trudeau, 1839) (Passeriformes: Cardinalidae), and Momotus momota lessonii Lesson, 1842 (Coraciiformes: Momotidae); and in Veracruz, locality of Orizaba, but without mention of the host (Lopez Campos, 1988). In other countries, it has been documented as a parasite of Seiurus aurocapilla (Linnaeus, 1766) (Passeriformes: Parulidae) from New York (Kierans, 1967) and Florida (Hribar, 2013); Piranga rubra (Linnaeus, 1758) (Passeriformes: Cardinalidae) from Massachusetts (Main and Anderson, 1970); on Ciccaba virgata (Cassin, 1849) (Strigiformes: Strigidae) and Catharus ustulatus (Nutall, 1840) (as Hylocichla ustulata) (Passeriformes: Turdidae) in Costa Rica (Tonn and Arnold, 1963); and on Zonotrichia capensis (Muller, 1776) (Passeriformes: Emberizidae), Chiroxiphia caudata (Shaw and Nodder, 1793) (Passeriformes: Pipridae), Schiffornis virescens (Lafresnaye, 1838) (Passeriformes: Tityridae), and Thamnophilus caerulescens Viellot, 1816 (Passeriformes: Thamnophilidae) in Parana, Brazil (Graciolli and de Carvalho, 2003). All of these records are additions to the O. fusciventris host list of 53 genera and 21 families of birds elaborated by Bequaert (1955, 1957) and summarized by Maa (1969b), none of which are the genera reported here.

New hosts found for O. fusciventris in this study include: C. flavopectus Cabanis, 1847 (Passeriformes: Thraupidae) (common name in Mexico: Chinchinero comun); B. rufifrons (Swainson, 1838) (Passeriformes: Parulidae) (common name in Mexico: Chipe gorra rufa); and S. nigricans (Swainson, 1827) (Passeriformes: Tyrannidae) (common name in Mexico: Papamoscas negro).

This is the second record of O. fusciventris in the state of Veracruz and the first on C. flavopectus, B. rufifrons, and S. nigricans. Maa (1969a, 1969b) and Bequaert (1953) mentioned the Order Passeriformes as hosts, particularly the families Muscicapidae, Thraupidae, and Fringillidae. With the exception of the family Thraupidae, this is the first time in which O. fusciventris is recorded from hosts belonging to the families Parulidae and Tyrannidae, with no previous records either from these three bird genera or from these three species.

Hippoboscid flies are known vectors of parasites of the genus Trypanosoma and Haemoproteus (Santiago-Alarcon et al., 2012). In particular, they transmit parasites of the subgenus Haemoproteus, which are known to parasitize only nonpasserine birds (Santiago-Alarcon et al., 2012, 2014). Hence, we believe that the infected passerine bird detected in this study was carrying a parasite not transmitted by louse flies. Our hippoboscid sample size is small, and to determine what are the likely blood parasites transmitted by this fly species we need to further characterize the bird parasite community and search for parasite developmental stages and DNA both in abdomens (mid-gut) and thoraxes (salivary glands).

This study was funded by Consejo Nacional de Ciencia y Tecnologia (CONACYT, project number CB-2011-01-168524). Sampling permit number SGPA/DGVS/05057/13 was provided by SEMARNAT. We thank C. Hernandez-Lara, D. Aguirre, A. P. Degante, A. Sandoval-Comte, A. Lobato, E. Rivera-Garcia, P. Carbo-Ramirez, and S. Baltazar-Hernandez for their assistance during fieldwork. We thank landowners (Don Felix, Don Albino, Don Hernan, and Fernando Cervantes) for allowing us to work on their private properties.

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Submitted 4 February 2015.

Acceptance recommended by Associate Editor, Jerry Cook, 24 August 2015.

SERGIO IBANEZ-BERNAL, FERNANDO GONZALEZ-GARCIA, AND DIEGO SANTIAGO-ALARCON *

Red Ambiente y Sustentabilidad, Instituto de Ecologia, A. C. (INECOL), Laboratorio de Sistematica y Ecologia de Insectos con Interes

Medico y Veterinario. Carretera antigua a Coatepec 351, El Haya, Xalapa, C. P 91070, Veracruz, Mexico (SIB)

Red Biologia y Conservacion de Vertebrados, INECOL. Laboratorio de Ecologia de Vertebrados e Interacciones Parasitarias (FGG, DSA)

* Correspondent: diego.santiago@inecol.mx
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Title Annotation:Notes
Author:Ibanez-Bernal, Sergio; Gonzalez-Garcia, Fernando; Santiago-Alarcon, Diego
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Dec 1, 2015
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