Composition and distribution of lice (Insecta: Phthiraptera) on Colombian and Peruvian birds: New data on louse-host association in the Neotropics.

The diversity of permanent ectoparasites is likely underestimated due to the difficulty of collecting samples. Lice (Insecta: Phthiraptera) are permanent ectoparasites of birds and mammals; there are approximately 5,000 species described and many more undescribed, particularly in the Neotropics. We document the louse genera collected from birds sampled in Peru (2006-2007) and Colombia (2009-2016), from 22 localities across a variety of ecosystems, ranging from lowland tropical forest and Llanos to high elevation cloud forest. We identified 35 louse genera from a total of 210 bird species belonging to 37 avian families and 13 orders. These genera belong to two suborders and three families of lice: Amblycera, families Menoponidae (present on 131 bird species) and Ricinidae (39 bird species); and Ischnocera, family Philopteridae (119 bird species). We compared our bird-louse associations with data in Price et al. (2003) and recently published Neotropical studies. The majority of bird-louse associations (51.9%) were new, with most of these coming from Passeriformes, the most diverse avian order, with the most poorly known louse fauna. Finally, we found geographical variation in louse infestation and prevalence rates. With this study, we report the first comprehensive documentation of bird-louse associations for Colombia and substantially increase the known associations documented for Peru.

Introduction

Parasites are one of the most common forms of life on the planet (Price 1980). They have evolved repeatedly in every major clade (Poulin and Morand 2000). Although parasites are amongst the most diverse organisms in the world, few are well studied. Permanent ectoparasites are particularly difficult to study because they live their entire life cycle on hosts (Marshall 1981) and require capturing the host to sample them.

Lice (: ) are permanent parasites occurring on both birds and mammals. There are approximately 5,000 described species of lice, about 3,000 of which are known from birds (Price et al. 2003, Smith et al. 2011). The taxonomic diversity of lice is positively correlated with the taxonomic diversity of their hosts (Eichler 1942, Vas et al. 2012). Colombia and Peru harbor the richest avifaunas in the world (Jetz et al. 2012), with 1,878 and 1,852 bird species, respectively (Avendaño et al. 2017), and, correspondingly, the highest diversity of avian lice is thought to be found in these regions (e.g. Valim and Weckstein (2013)). Currently, however, there is limited knowledge of louse-host associations and louse diversity from these countries (e.g. Clayton et al. (1992) and the Neotropics in general (Clayton et al. (1992), Marini et al. (1996), Valim and Weckstein (2013). This is due in part to the poor representation of louse specimens in museum collections and the lack of louse specialists and field workers who sample parasites when collecting or handling birds. Therefore, the diversity of known louse species at regional scales is not on par with lists of avian host diversity from these countries. Our main objective is to provide novel information about the composition and distribution of lice on Colombian and Peruvian birds.

From large collections of louse specimens from birds in Peru, Clayton et al. (1992) and Clayton and Walther (2001) examined how host ecology and morphology influence louse diversity across a sample of 127 bird species. These two studies, amongst other taxonomic studies published using the same specimens e.g. Price and Clayton (1995), Price and Clayton (1989), provide most of the known louse-host associations from Peruvian birds. Much less information is available for Colombia, apart from the work of Melbourne A. Carriker (1879–1965), who collected mostly non-passerine birds and their associated lice and a study by Parra-Henao et al. (2011) where they identified lice from 18 bird species from the Cordillera Central near Medellín (Valle de Aburrá). Although this previous work provides an excellent starting point for understanding the diversity of lice in the Neotropics, the numbers of birds examined for lice is a small sample of the total avian diversity in this region.

In this study, we provide data from extensive sampling and description of louse-host associations from Colombia and Peru. Material was collected from 22 localities over nine years. From these samples, we identified 36 unique genera of lice and compared our results with those found in previous studies and with data compiled in the published checklist in Price et al. (2003). We found that over 50% of the louse-host associations were previously unreported and suggest that further data from these collections will be important to identify factors associated with louse diversity in the Neotropics. The data presented here provide the foundation for a long-term project sampling louse diversity across the Andes. This dataset will provide the basis for answering large-scale questions about patterns of diversity along elevational, habitat and host taxonomic gradients. The long-term project will include species level identification, taxonomic description and exploration of macro-ecological patterns along with archiving and storage of louse specimens.

Material and methods

Lice were collected at 22 localities in Peru (2006–2007) and Colombia (2009–2016) (Table 1). In Peru, samples were collected by GAL and JEJ at four stations from Andean foothill forest (800 m a.s.l.) to high elevation cloud forest (3,000 m a.s.l.) inside Manu National Park or its buffer zone along a contiguously forested altitudinal gradient (Fig. 1a). In Colombia, samples were collected by GAL, JEA and JSP at 18 sites across the country, which ranged in elevation and habitat from 100 m a.s.l. to 2,800 m a.s.l., including savannah and gallery forest, lowland tropical forest and humid premontane and montane cloud forest (Fig. 1b).

Table 1.

Sampling localities in Peru (2006–2007) and Colombia (2009–2016).

Country	Department	Locality	Coordinates	Elevation (m a.s.l)	Habitat	Collector (s)
Peru	Cusco	1. Buenos Aires (Mun. Paucartambo)	13°9'S, 71°35'W	2480-2550	Highland cloud forest	GAL-JEJ
	Cusco	2. Tono (Mun. Patria)	12°57'S, 71°34'W	800-1100	Andean foothill forest	GAL-JEJ
	Cusco	3. Lodge Gallito de las rocas (Mun. San Pedro)	13°03'S, 71°32'W	1200-1500	Montane cloud forest	GAL-JEJ
	Cusco	4. Wayqecha Biological Station (Mun. Paucartambo)	13°10'S, 71°35'W	2600-3000	Highland cloud forest	GAL-JEJ
Colombia	Santander	5. El Rasgón Reserve (Mun. Piedecuesta)	07°02'N, 72°59'W	2200	Primary cloud forest and borders	JEA
	Antioquia	6. Remedios (Mun. Remedios)	06°54'N, 74°34'W	500	Lowland humid forest	GAL
	Santander	7. Salabuga farm (Mun. San Andrés)	06°45'N, 72°46'W	2650	Primary cloud forest and borders	JEA
	Santander	8. El Tablón farm (Mun. San Andrés)	06°43'N, 72°49'W	2770-2800	Primary cloud forest and borders	JEA
	Santander	9. La Rinconada farm (Mun. San Andrés)	06°43'N, 72°47'W	2880	Primary cloud forest and borders	JEA
	Risaralda	10. Montezuma, Tatama Nationla Park (Mun. Pueblo Rico)	05°13'N, 76°05'W	1200-2500	Forest types from foothills, to mid and high elevation cloud forests	GAL
	Casanare	11. El Porvernir farm (Mun. Aguazul)	05°13'N, 72°30'W	350-400	Secondary humid tropical forest	JEA
	Meta	12. Universidad de los Llanos (Mun. Villavicencio)	04°4'N, 73°35'W	400-440	Secondary humid tropical forest	JEA
	Meta	13. Mitimiti farm (Mun. Puerto Gaitán)	04°31'N, 71°48'W	141	Savannah, gallery forest	JEA
	Cundinamarca	14. San Antonio farm (Mun. Medina)	04°26'N, 73°24'W	570	Secondary humid tropical forest	JEA
	Meta	15. Manacacías farm (Mun. Puerto Gaitán)	04°10'N, 72°02'W	200-250	Savannah, gallery forest	JEA
	Valle del Cauca	16. La Minga farm (Mun. La Cumbre)	03°33'N, 76°35'W	2000	Cloud forest on top of the Western cordillera	GAL
	Valle del Cauca	17. Icesi University research station, Zygia, Farallones de Cali National Park (Mun. Cali)	03°27'N, 76°46'W	2400	High elevation cloud forest	GAL
	Valle del Cauca	18. Danubio (Mun. Cali)	03°24'N, 76°39'W	2200	High elevation cloud forest	GAL-JSP
	Guaviare	19. Laguna Grande (Mun. San José del Guaviare)	02°33'N, 72°39'W	400	Savannah, gallery forest	JEA
	Cauca	20. Mirabilis-Swarovski Reserve (Mun. El Tambo)	02°31'N, 76°59'W	2270	Primary humid montante forest	JEA
	Cauca	21. Tambito Reserve (Mun. El Tambo)	02°30'N, 76°59'W	1500	Primary premontane forest	JEA
	Nariño	22. El Pangán Reserve (Mun. Barbacoas)	01°21'N, 78°05'W	710	Primary humid tropical forest	JEA

Figure 1a.

Peru

Figure 1b.

Colombia

At each site, 10 to 20 netting stations were run and, at each station, 10 mist nets were opened for three days to capture birds. Each netting station was sampled twice during each 4 to 6 month field season. After removing birds from the nets, each individual host was placed in a clean cloth bag until processing for ectoparasites. We used three methods for collecting ectoparasites, detailed in Clayton and Drown (2001): 1) Post-mortem ruffling, 2) visual examiniation and, for the majority of samples 3) dust-ruffling. To dust-ruffle the birds, we applied ~1 ml of EverGreen pyrethrum dust (McLaughlin Gormley King Company, MN, USA) to captured birds and then ruffled feathers from all body regions except the head. Five minutes after we applied the powder, we ruffled each bird's feather tracts over a plastic sheet for 30 to 60 seconds to remove powder and ectoparasites. We transferred all powder and ectoparasites that fell on to the sheet to a 1.5ml Eppendorf tube filled with 96% ethyl alcohol and inserted a label with host metadata.

JEA also collected ectoparasite specimens using Clayton and Drown's (2001) post-mortem ruffling method for euthanised avian hosts. These hosts were collected and prepared as museum voucher specimens. To collect ectoparasites, JEA placed each euthanised host in a Ziploc bag with cotton soaked in ethyl acetate for 20 minutes. He then removed the bird from the bag and ruffled the plumage for 60 seconds over a white sheet of paper. Each specimen was returned to its Ziploc bag (with cotton soaked with ethyl acetate), ruffling the plumage two additional times, at intervals of 15 minutes. The ectoparasites were collected from the paper with a small brush and placed in a vial with 96% ethyl alcohol with a label including host specimen metadata. Bird voucher specimens were deposited in the bird collection of Instituto de Ciencias Naturales (ICN) of Universidad Nacional (Bogotá, Colombia) and the Museum of Natural History (MHNU) at Universidad de los Llanos (Villavicencio, Meta, Colombia). Lice were separated from the other ectoparasites, placed into individual vials and identified to genus using taxonomic keys Price et al. (2003). Host taxonomy followed the South American Classification Committee Remsen et al. (2017). Many louse species require microscopic examination of a slide-mounted specimen for species level identification. As this will be the focus of future work, these lice were only identified to genus. All specimens are stored at -80C for later DNA extraction and slide mounting at the Universidad Icesi, Cali Colombia. Vouchered, slide-mounted specimens will be made available at Universidad Icesi in Colombia and The Museum of Natural History at the University of Nevada, Reno in the U.S. The Colombian permit was approved by the ANLA by the Resolución 509 del 21 de mayo del 2014 and the Peruvian permit was approved by the Institutional Animal Care and Use Committee at the University of Florida (Protocol #: 201106068) and by permits from the government of Peru (0239-2013 MINAGRI-DGFFS/DGEFFS 2013).

We compared our findings with the world checklist of chewing lice in Price et al. (2003) and recently published taxonomic literature on Neotropical lice in Price et al. (2005), Price et al. (2008), Price and Dalgleish (2006), Sychra et al. (2007), Kounek et al. (2011a), Kounek et al. (2011b), Valim et al. (2011). Using these resources, for each host species in our study, we classified the louse fauna documented amongst our samples combined from both Colombia and Peru into one of four categories.

0) Not previously reported - avian species with no louse association data reported.

1) Same as reported - avian species for which our study found the same louse genera as reported.

2) Fewer than reported - avian species for which our study found fewer louse genera than reported

3) More than reported - avian species for which our study found more louse genera than reported

Results

In Colombia, we sampled 1,032 individual birds from 280 species. Just over half, 51.6% (532), of these birds were infected with ectoparasites (i.e. feather mites, ticks, parasitic flies, fleas and lice) and we found lice on 30% (310) of individual hosts from 138 avian species, 36 avian families and 13 avian orders (Table 2). In Peru, we found lice on 262 individual birds from 98 species, 19 families and 5 orders (Table 3). In both countries combined, we identified 35 louse genera on 210 bird species from 37 avian families and 13 avian orders. Lice documented in this study are from two suborders and three families: Suborder ( and ); and suborder ().

Table 2.

Louse-host associations from birds captured in Colombia. N - number of birds examined, Ni - Number of infected birds. Superscripts A and I represent louse suborders or and * indicates a previously unrecorded louse host association.

Bird taxa	Louse genera	N	Ni
Tinamiformes
Tinamidae (1)
Crypturellus soui	Strongylocotes sp. I	1	1
Galliformes
Odontophoridae (1)
Colinus cristatus	Gonioides sp.I	2	2
	Lipeurus sp.I
	Oxylipeurus sp.I
Columbiformes
Columbidae (3)
Leptotila rufaxilla	Columbicola sp.I	2	2
	Physconelloides sp.I
Columbina talpacoti	Columbicola sp.I	2	2
	Physconelloides sp.I
Zentrygon frenata	Campanulotes sp.I	1	1
Cuculiformes
Cuculidae (2)
Crotophaga ani	Osborniella sp.A	1	1
	Vernoniella sp.I
Piaya cayana	Cuculoecus sp.I	1	1
Caprimulgiformes
Caprimulgidae (2)
Systellura longirostris	Mulcticola sp.I,*	1	1
Nyctidromus albicollis	Mulcticola sp.I	3	3
Apodiformes
Apodidae (1)
Chaetura meridionalis	Eureum sp.A,*	1	1
Trochilidae (2)
Anthracothorax nigricollis	Trochiliphagus sp.A	2	2
Thalurania colombica	Myrsidea sp. A,*	1	1
Charadriiformes
Scolopacidae (1)
Gallinago paraguaiae	Saemundssonia sp. I	1	1
	Rhynonirmus sp.I,*
Jacanidae (1)
Jacana jacana	Rallicola sp.I	1	1
Accipitriformes
Accipitridae (1)
Accipiter striatus	Degeeriella sp.I	1	1
Coraciiformes
Alcedinidae (3)
Chloroceryle americana	Alcedoffula sp. I	2	2
Chloroceryle inda	Alcedoffula sp. I	2	2
Chloroceryle aenea	Alcedoffula sp. I	3	2
Momotidae (2)
Momotus momota	Philopterus sp. I	2	2
Momotus aequatorialis	Brueelia s.l. I,*	4	1
Galbuliformes
Bucconidae (1)
Hypnelus ruficollis	Picicola sp. I,*	3	3
Piciformes
Capitonidae (1)
Eubucco bourcierii	Penenirmus sp.I	3	1
Ramphastidae (1)
Aulacorhynchus haematopygus	Austrophilopterus sp.I	4	1
Picidae (6)
Picumnus squamulatus	Penenirmus sp.I,*	1	1
Melanerpes formicivorus	Penenirmus sp.I	1	1
Melanerpes rubricapillus	Brueelia s.l. I,*	1	1
Picoides fumigatus	Brueelia s.l. I,*	5	1
Colaptes rubiginosus	Penenirmus sp. I,*	1	1
Dryocopus lineatus	Picicola sp.I,*	1	1
Psittaciformes
Psittacidae (3)
Brotogeris cyanoptera	Psittacobrosus sp.A	1	1
Forpus conspicillatus	Psittacobrosus sp. A	1	1
Eupsittula pertinax	Psittacobrosus sp. A	2	2
	Paragoniocotes sp.I
Passeriformes
Thamnophilidae (3)
Dysithamnus puncticeps	Ricinus sp.A,*	1	1
Myrmotherula schisticolor	Ricinus sp.A,*	6	1
Formicivora grisea	Myrsidea sp.A,*	1	1
Conopophagidae (1)
Conopophaga castaneiceps	Formicaphagus sp.I,*	1	1
Grallaridae (1)
Grallaria alleni	Picicola sp.I,*	1	1
Rhynocrhyptidae (1)
Scytalopus griseicollis	Rallicola sp.I,*	3	1
Furnariidae (12)
Dendrocincla fuliginosa	Rallicola sp.I	10	2
	Ricinus sp.A,*
Glyphorhynchus spirurus	Rallicola sp.I	23	1
Xiphorhynchus obsoletus	Rallicola sp.I,*	2	2
Dendroplex picus	Rallicola sp.I,*	3	2
Anabacerthia variegaticeps	Philopterus sp.I,*	1	1
Syndactyla subalaris	Rallicola sp. I,*	8	1
	Myrsidea sp.A
Clibanornis rubiginosus	Rallicola sp.I,*	2	2
Thripadectes ignobilis	Rallicola sp.I,*	2	2
Thripadectes virgaticeps	Rallicola sp.I,*	4	2
	Myrsidea sp.A
Premnoplex brunnescens	Rallicola sp.I	10	1
	Myrsidea sp.A
Cranioleuca vulpina	Rallicola sp.I,*	1	1
	Myrsidea sp.A
Synallaxis unirufa	Rallicola sp.I,*	2	1
Tyrannidae (13)
Elaenia flavogaster	Myrsidea sp.A	1	1
Elaenia parvirostris	Ricinus sp.A,*	1	1
Elaenia chiriquensis	Menacanthus sp.A,*	1	1
Elaenia pallatangae	Myrsidea sp.A,*	2	1
Mecocerculus leucophrys	Menacanthus sp.A,*	2	1
Mionectes striaticollis	Myrsidea sp.A,	28	12
	Philopterus sp. I,*
Mionectes olivaceus	Myrsidea sp.A	13	4
	Philopterus sp.I,*
Mionectes oleagineus	Myrsidea sp.A	18	2
Leptopogon amaurocephalus	Philopterus sp.I,*	16	3
Atalotriccus pilaris	Philopterus sp.I,*	1	1
Rhynchocyclus olivaceus	Myrsidea sp.A	4	1
Platyrinchus coronatus	Myrsidea sp.A,*	2	1
Myiarchus tyrannulus	Philopterus sp.I,*	1	1
Cotingidae (3)
Pipreola riefferii	Cotingacola sp.I	26	8
	Philopterus sp. I,*
	Myrsidea sp.A,*
Pipreola arcuata	Pseudocophorus sp.I	1	1
Pipreola jucunda	Ricinus sp.A,*	1	1
Pipridae (4)
Chloropipo flavicapilla	Philopterus sp.I,*	7	2
Manacus manacus	Ricinus sp.A	9	2
	Philopterus sp.I
Pipra filicauda	Ricinus sp.A,*	7	6
	Philopterus sp.I,*
	Myrsidea sp.A,*
Machaeropterus regulus	Ricinus sp.A	21	3
Tytiridae (1)
Pachyramphus polychopterus	Myrsidea sp.A,*	3	3
	Ricinus sp.A
Corvidae (1)
Cyanocorax violaceus	Brueelia s.l.I	1	1
	Myrsidea sp.A
Hirundinidae (1)
Progne tapera	Philopterus sp.I,*	2	2
	Myrsidea sp.A
Troglodytidae (2)
Troglodytes aedon	Penenirmus sp.I	6	2
Cyphorhinus thoracicus	Penenirmus sp.I,*	8	1
Turdidae (10)
Myadestes ralloides	Philopterus sp.I,*	29	15
	Myrsidea sp.A,*
Catharus ustulatus	Philopterus sp.I,*	10	4
	Myrsidea sp.A
Entomodestes coracinus	Brueelia s.l.I,*	8	4
	Myrsidea sp.A
	Myrsidea sp.A
Turdus leucops	Brueelia s.l.I,*	13	2
Turdus leucomelas	Myrsidea sp.A	4	4
	Brueelia s.l.I
Turdus nudigenis	Myrsidea sp.A	6	6
	Brueelia s.l.I,+
Turdus ignobilis	Myrsidea sp.A	1	1
	Brueelia s.l.I,*
Turdus fuscater	Myrsidea sp.A,*	2	1
	Brueelia s.l.I,*
Turdus serranus	Myrsidea sp.A,*	19	12
	Brueelia s.l.I,*
Turdus albicollis	Myrsidea sp.A,*	2	2
	Brueelia s.l. I,*
Thraupidae (34)
Paroaria nigrogenis	Myrsidea sp.A,*	1	1
	Brueelia s.l.I,*
Schistochlamys melanopis	Myrsidea sp.A	1	1
Hemispingus atropileus	Myrsidea sp.A,*	2	1
Hemispingus frontalis	Myrsidea sp.A,*	7	1
Ramphocelus carbo	Myrsidea sp.A	15	15
	Brueelia s.l.I,*
	Ricinus sp.A
Ramphocelus flammigerus	Myrsidea sp.A,*	3	2
Bangsia edwardsi	Myrsidea sp.A,*	2	2
Bangsia aureocincta	Philopterus sp.I,*	3	1
	Myrsidea sp.A,*
Buthraupis montana	Myrsidea sp.A,*	2	2
Chlorornis riefferii	Myrsidea sp.A,*	3	1
Anisognathus somptuosus	Myrsidea sp.A,*	10	6
Iridosornis rufivertex	Myrsidea sp.A,*	1	1
Chlorochrysa phoenicotis	Myrsidea sp.A,*	4	2
Thraupis palmarum	Myrsidea sp.A	3	2
	Ricinus sp.A
Thraupis cyanocephala	Myrsidea sp.A	3	2
	Brueelia s.l.I,*
Tangara heinei	Myrsidea sp.A,*	4	2
Tangara cayana	Myrsidea sp.A	9	9
	Machaerilaemus sp.A,*
Tangara vitriolina	Myrsidea sp.A,*	1	1
Tangara rufigula	Myrsidea sp.A,*	3	3
Tangara nigroviridis	Myrsidea sp.A,*	5	1
Tangara gyrola	Myrsidea sp.A	1	1
Tangara arthus	Myrsidea sp.A,*	8	1
Tangara icterocephala	Myrsidea sp.A	3	3
	Ricinus sp.A,*
Tersina viridis	Menacanthus sp.A,*	1	1
Diglossa albilatera	Myrsidea sp.A,*	14	2
Diglossa caerulescens	Myrsidea sp.A,*	4	2
	Philopterus sp.I
Catamblyrhynchus diadema	Myrsidea sp.A,*	3	2
Haplospiza rustica	Philopterus sp.I,*	2	1
Saltator maximus	Myrsidea sp.A	2	2
Saltator coerulescens	Myrsidea sp.A,*	1	1
Volatinia jacarina	Myrsidea sp.A,*	2	2
Sporophila minuta	Ricinus sp.A,*	1	1
Sporophila crassirostris	Philopterus sp.I,*	1	1
Coereba flaveola	Brueelia s.l.I,*	1	1
Emberizidae (6)
Oreothraupis arremonops	Myrsidea sp.A,*	3	1
Chlorospingus flavigularis	Myrsidea sp.A,*	3	2
Chlorospingus flavopectus	Myrsidea sp.A	10	9
	Ricinus sp. A,*
	Philopterus sp. I,*
	Penenirmus sp.I,*
Chlorospingus semifuscus	Myrsidea sp.A,*	8	5
	Philopterus sp.I,*
	Brueelias.l.I,*
Arremonops conirostris	Myrsidea sp.A	3	3
Arremon brunneinucha	Myrsidea sp.A	18	8
	Brueelia s.l. I
Cardinalidae (1)
Habia cristata	Myrsidea sp.A,*	1	1
	Brueelias.l.I,*
Parulidae (5)
Setophaga fusca	Ricinus sp.A	2	1
Myiothlypis fulvicauda	Menacanthus sp.A,*	1	1
Myiothlypis coronata	Myrsidea sp.A,*	17	7
	Brueelias.l.I,*
Basileuterus tristriatus	Myrsidea sp.A,*	18	4
	Menacanthus sp. A,*
	Myrsidea sp.A
Myioborus miniatus	Ricinus sp.A,*	7	2
Icteridae (4)
Psarocolius decumanus	Myrsidea sp.A	1	1
Cacicus cela	Myrsidea sp.A	1	1
	Brueelia s.l. I
Cacicus chrysonotus	Myrsidea sp.A,*	4	1
	Brueelia s.l. I
Gymnomystax mexicanus	Myrsidea sp.A,*	1	1
Fringillidae (3)
Euphonia chlorotica	Myrsidea sp.A,*	1	1
Euphonia laniirostris	Myrsidea sp.A	1	1
Chlorophonia pyrrhophrys	Philopterus sp.I,*	1	1
	Brueelias.l.I,*
TOTAL (138)		641	310

Table 3.

Host-louse associations from sites in Peru. Ni Number of birds infested. Superscripts A and I represent the suborders of lice and , * represents new host-louse association reported in this study. New genus reported for a host species with louse associations known (No) Number of host species representing each bird family.

Bird taxa	Louse genera	Ni
Columbiformes
Columbidae (1)
Geotrygon montana	Columbicola sp.I	1
Apodiformes
Trochilidae (2)
Coeligena violifer	Trochiloecetes sp.A, *	1
Thalurania furcata	Trochiliphagus sp.A,*	1
Coraciiformes
Momotidae (1)
Baryphthengus martii	Brueelia s.l.I	1
Piciformes
Capitonidae (1)
Eubucco versicolor	Myrsidea sp.A, *	1
Passeriformes
Thamnophilidae (7)
Thamnophilus caerulescens	Formicaphagus sp.I, *	1
	Macharilaemus sp.A, *
Dysithamnus mentalis	Formicaphagus sp.I, *	3
	Myrsidea sp.A, *
Pyriglena leuconota	Formicaphagus sp.I	1
Myrmoborus myotherinus	Formicaphagus sp.I, *	1
Sciaphylax hemimelaena	Ricinus sp.A, *	1
Rhegmatorhina melanosticta	Ricinus sp.A, *	1
	Myrsidea sp.A, *
Phlegopsis nigromaculata	Myrsidea sp.A, *	1
Grallaridae (1)
Grallaricula flavirostris	Myrsidea sp.A, *	1
Formicariidae (1)
Chamaeza campanisona	Myrsidea sp.A, *	1
Furnariidae (15)
Dendrocincla fuliginosa	Rallicola sp.I	1
Glyphorhynchus spirurus	Myrsidea sp.A	3
	Rallicola sp.I
Xiphocolaptes promeropirhynchus	Rallicola sp.I, *	1
Xiphorhynchus triangularis	Rallicola sp.I	2
Anabacerthia striaticollis	Philopterus sp.I,*	3
	Ricinus sp.A,*
Syndactyla ucayalae	Myrsidea sp.A, *	1
Clibanornis rubiginosus	Myrsidea sp.A, *	2
	Rallicola sp.I
Thripadectes holostictus	Furnariphilus sp.I, *	2
	Myrsidea sp.A, *
Thripadectes melanorhynchus	Myrsidea sp.A, *	5
	Rallicola sp.I
Automolus ochrolaemus	Myrsidea sp.A	2
Automolus subulatus	Myrsidea sp.A, *	1
	Rallicola sp.I
Premnoplex brunnescens	Myrsidea sp.A	1
Margarornis squamiger	Rallicola sp.I	1
Asthenes helleri	Philopterus sp.I, *	2
Synallaxis azarae	Furnariphilus sp.I, *	1
Tyrannidae (16)
Phylloscartes poecilotis	Myrsidea sp.A, *	1
Phylloscartes ophtalmicus	Philopterus sp.I, *	1
	Myrsidea sp.A
Mionectes olivaceus	Myrsidea sp.A	17
Mionectes striaticollis	Myrsidea sp.A	26
	Philopterus sp.I, *
Mionectes oleagineus	Myrsidea sp.A	6
Leptopogon superciliaris	Myrsidea sp.A, *	7
	Philopterus sp.I
Myiotriccus ornatus	Myrsidea sp.A, *	1
Lophotriccus pileatus	Philopterus sp.I, *	1
Myiophobus inornatus	Ricinus sp.A, *	1
Pyrrhomyias cinnamomeus	Philopterus sp.I, *	1
Mitrephanes olivaceus	Philopterus sp.I, *	1
Ochthoeca frontalis	Philopterus sp.I, *	6
	Myrsidea sp.A
Ochthoeca pulchella	Philopterus sp.I, *	6
	Myrsidea sp.A, *
Ochthoeca cinnamomeiventris	Philopterus sp.I, *	1
Ochthoeca rufipectoralis	Philopterus sp.I, *	2
Conopias cinchoneti	Philopterus sp.I, *	1
Cotingidae (2)
Pipreola intermedia	Myrsidea sp.A, *	2
	Philopterus sp.I, *
Pipreola pulchra	Myrsidea sp.A, *	1
Pipridae (4)
Chiroxiphia boliviana	Myrsidea sp.A, *	6
	Philopterus sp.I
	Ricinus sp.A
Lepidothrix coeruleocapilla	Myrsidea sp.A, *	8
	Philopterus sp.I, *
	Ricinus sp.A, *
Pipra fasciicauda	Myrsidea sp.A, *	1
	Philopterus sp.I, *
Machaeropterus pyrocephalus	Philopterus sp.I, *	2
	Ricinus sp.A
Troglodytidae (1)
Henicorhina leucophrys	Myrsidea sp.A, *	1
Turdidae (6)
Myadestes ralloides	Myrsidea sp.A, *	4
	Philopterus sp.I, *
	Brueelia s.l.I, *
Catharus ustulatus	Myrsidea sp.A	5
	Brueelia s.l.I
Entomodestes leucotis	Myrsidea sp.A, *	4
	Brueelia s.l.I
	Sturnidoecus sp.I, *
Turdus leucops	Myrsidea sp.A, *	1
Turdus fuscater	Myrsidea sp.A, *	1
	Philopterus sp.I
Turdus serranus	Myrsidea sp.A, *	3
	Menacanthus sp.A
	Philopterus sp.I
	Brueelia s.l.I, *
	Ricinus sp.A
Thraupidae (25)
Hemispingus superciliaris	Ricinus sp.A, *	1
Hemispingus melanotis	Myrsidea sp.A, *	4
	Ricinus sp.A
Trichothraupis melanops	Myrsidea sp.A, *	3
Thlypopsis ruficeps	Philopterus sp.I, *	2
	Ricinus sp.A
Ramphocelus carbo	Myrsidea sp.A	2
Buthraupis montana	Myrsidea sp.A, *	1
Chlorornis riefferii	Myrsidea sp.A, *	1
Iridosornis analis	Myrsidea sp.A, *
	Brueelia s.l.I, *	5
Iridosornis jelskii	Myrsidea sp.A, *
Chlorochrysa calliparaea	Myrsidea sp.A, *	1
Thraupis cyanocephala	Myrsidea sp.A	1
Tangara cyanicollis	Myrsidea sp.A, *	1
	Brueelia s.l.I, *	2
Tangara punctata	Myrsidea sp.A, *
Tangara nigroviridis	Myrsidea sp.A, *	2
Tangara chilensis	Myrsidea sp.A	2
Tangara gyrola	Myrsidea sp.A	1
Tangara schrankii	Myrsidea sp.A, *	1
Tangara arthus	Myrsidea sp.A, *	2
Conirostrum albifrons	Ricinus sp.A, *	2
Diglossa mystacalis	Myrsidea sp.A, *	2
Diglossa brunneiventris	Myrsidea sp.A, *	2
Diglossa glauca	Myrsidea sp.A, *	1
	Ricinus sp.A, *	1
Diglossa cyanea	Myrsidea sp.A, *
Saltator maximus	Brueelia s.l.I,+	3
Coereba flaveola	Myrsidea sp.A	1
Emberizidae (6)
Chlorospingus flavigularis	Myrsidea sp.A, *	8
Chlorospingus parvirostris	Myrsidea sp.A, *	2
Chlorospingus flavopectus	Myrsidea sp.A	1
Arremon taciturnus	Myrsidea sp.A	2
Arremon brunneinucha	Brueelia s.l.I	1
Atlapetes melanolaemus	Ricinus sp.A, *	4
Cardinalidae (1)
Piranga leucoptera	Myrsidea sp.A, *	1
Parulidae (5)
Myiothlypis luteoviridis	Myrsidea sp.A, *	5
	Ricinus sp.A, *
Myiothlypis signata	Myrsidea sp.A, *	3
	Menacanthus sp.A, *
	Picicola sp.I, *
	Ricinus sp.A, *
Myiothlypis bivittata	Myrsidea sp.A, *	5
	Ricinus sp.A
Myiothlypis coronata	Myrsidea sp.A, *	7
	Brueelia s.l.I, *
Myioborus miniatus	Myrsidea sp.A	6
	Menacanthus sp.A, *
	Ricinus sp.A, *
Icteridae (1)
Amblycercus holosericeus	Philopterus sp.I, *	1
Fringillidae (2)
Euphonia mesochrysa	Ricinus sp.A, *	1
Euphonia xanthogaster	Myrsidea sp.A, *	7
TOTAL (98)		262

- Six menoponid louse genera were distributed on 131 bird species: Waterston 1915 (120 bird species), Neumann 1912 (8), (3), Harrison 1915 (2), (1) and Thompson 1948 (1).

– Three ricinid louse genera were distributed on 39 bird species: De Geer 1778 (36 bird species), Carriker 1960 (2) and Paine and Mann 1913 (1).

– Twenty six philopterid genera were distributed on 119 bird species: (42 bird species), (30), Johnston and Harrison 1911 (18), Clay and Meinertzhagen 1938a (7), Carriker 1957 (5), Clay and Meinertzhagen 1938a (4), Clay and Meinertzhagen 1939 (3), Ewing 1929 (3), Price and Clayton 1995 (2), (2), Ewing 1927 (2), (1), Kéler 1939 (1), Carriker 1956 (1) (1), (1), Nitzsch 1818 (1), (1) Mjöberg 1910 (1), Cummings 1916 (1), (1), Thompson 1935 (1), Tachenberg 1882 (1), Timmermann 1936 (1), (1) and Guimarães 1942 (1).

In total, including the two louse suborders, 131 bird species had one louse genus, 61 had two louse genera, 16 had three louse genera, 1 had four and 1 had five louse genera.

We compared our findings with the world checklist of chewing lice in Price et al. (2003) and more recent publications. We report new louse generic associations for 109 of 210 bird species (51.6% of the host species sampled; Tables 2 and 3). For 52 bird species (24.8% of the host species sampled), we found the same number of louse genera as previously reported and, in 29 bird species (13.8% of the host species sampled), we found fewer genera than previously reported. In addition, for 20 bird species (9.5% of the host species sampled), we found more louse genera than previously reported Fig. 2.

Figure 2.

Bird-louse associations included in each category described in the methods above. The Y axis represents the number of bird species and the X axis indicates the categories in which bird species were grouped according to reported louse-bird associations.

Data resources

The dataset is the result of several trips to 22 localities to study Neotropical bird communities in Colombia and Peru Table 1. In this study, we report lice on a total of 572 individual hosts totalling 210 bird species from 37 avian families and 13 orders. We identified 35 louse genera from two suborders and three families: Suborder ( and ); and suborder () Suppl. material 1

Discussion

In the present study, we report the genera of lice collected from 210 bird species at 22 sites in Colombia and Peru. We compared the louse-host association found in our study with the known genera of lice from these species of birds. We used Price et al. (2003), the most complete published bird-louse association list, along with recent Neotropical host-louse faunistic and taxonomic publications to assess the novelty of the host-parasite associations documented by our study.

We report 109 novel host-louse generic associations. This was not unexpected as we sampled several lowland and Andean habitats which have previously had few studies of bird-louse associations.

The majority (87.1%) of these new records were from . Knowledge of lice from many is relatively poor compared to non-passerines Sychra et al. (2007) and thus the diversity and number of undescribed parasites from these hosts is likely high e.g. Valim and Weckstein (2013), as confirmed by recent taxonomic descriptions and new associations of lice from Neotropical birds in the families Price et al. 2005, Price and Johnson 2009Price et al. 2005, Price and Johnson 2009, Sychra et al. 2007, Kounek et al. 2011a and , and Kounek et al. 2011b. These studies are likely only the beginning of describing new species in these mega-diverse louse groups found on Neotropical passerine birds. For example, Valim and Weckstein (2013) point out that louse genera such as harbour large numbers of undescribed species. Our data show that the majority of sampled (64.5%) have and many of them are likely to be new species.

The distribution of lice is related to the distribution of their hosts Rózsa and Vas (2015) and many orders and families typically have parasites of distinctive louse faunas Smith (2001). Our data are consistent with generalised patterns across avian groups. For example, members of the are known to infect hummingbirds and small , whereas members of the are widely distributed across most avian families Rózsa and Vas (2015). Similarly, we found lice from the genus on 36 species of from 11 host families. is a broadly distributed, mega-diverse genus Valim and Weckstein (2013), found mostly on and is considered to have a high degree of host-specificity Price and Dalgleish (2007). We also found that the louse genus , from the family , was distributed on 120 bird species, two of which were non-.

In , the family is widely distributed on birds Rózsa and Vas (2015). The various genera of are often specialised morphologically and behaviourally for living on a single microhabitat in the plumage (e.g. wing, head and/or body feathers) where lice can avoid host preening Johnson et al. (2012). This microhabitat specialisation may in part explain the host specificity and diversity of these lice. The three most common genera of found in our study were , and Of these, was the most widely distributed genus in this family, occurring on a diverse array of passerine host families and a single non-passerine host species (42 bird species). , the most speciose genus of lice in the family , infects avian hosts from many orders, including , and Valim and Weckstein (2011) Valim and Weckstein (2013) Gustafsson and Bush (2017). Similarly, we found on 30 bird species, including two species of , two species of and 26 species of . Finally, the third most frequently collected genus was , found on 18 bird species, including one host species in the order and 17 host species in the order . is one of the most speciose of ischnoceran louse genera and has been reported from the avian host orders , , and Price et al. (2003), Smith (2001).

Thirty percent of the Colombian birds sampled (138 host species) were infected with lice. In Peru, Clayton et al. (1992) found that 48% of birds examined (127 host species) were infected by lice, whereas in Brazil, Marini et al. (1996) and Oniki (1999) found that 20% of 313 individual birds (53 species) and 63% of 60 birds (38 species) had lice, respectively. Enout et al. (2012) found that 65% of 57 avian host species sampled were infected with lice. These studies suggest that louse prevalence may vary geographically. For example, for the flycatcher, , in Brazil, Marini et al. (1996) and Oniki (1999), sampled two and one individual hosts respectively and all were infected with lice, whereas Enout et al. (2012) found two of three individuals sampled infected with lice. We found that in Remedios, Colombia, only 16.6% (n=12) of individuals were infected. However, other host species had similar prevalence rates as reported in previous studies. For example, in Brazil, Oniki (1999) found that 67% of sampled (n=3) were infected with lice and we found that all individuals of sampled at two localities by us (n=4) were infected. However, a second Brazilian study conducted by Enout et al. (2012) found a 43% infestation rate (n=35) for the same bird species. It is difficult to determine the drivers behind variation in prevalence. It is possible that we are seeing an ecological pattern due to differences in humidity at the different sampling localities Moyer et al. (2002), Bush et al. (2009), host distributions or due to the different methods used by researchers to collect the lice. Additional work, examining sites where lice were collected with the same methodology, will help to address these issues.

Conclusions

This manuscript presents data on avian lice from 210 host species. We report and document significant new host-louse association records from poorly sampled yet diverse regions of the world. This information provides an important basis for future studies in the tropics and further enriches our knowledge of the parasite fauna associated with Neotropical birds.

Lice from Colombian and Peruvian birds

Data type: Taxonomic

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