Contributions to the knowledge of lice diversity (Phthiraptera: Amblycera and Ischnocera) in birds from Peru

Peru has a great diversity of birds, having more than 1870 species in its territory. However, studies on chewing lice (Phthiraptera) in birds from Peru are still limited. The objective of this study is to contribute to the knowledge of the diversity of lice in birds of Peru. The material used comes from the Zoological Collection of the Natural History Museum of the Universidad Nacional Federico Villarreal, Lima, Peru. Ten species of lice distributed in three families were identified: three species of the Menoponidae family, five species of Philopteridae and two species of Ricinidae collected from seven species of birds. This work records for the first time Hohorstiella lata Piaget, 1880, Quadraceps eugrammicus (Burmeister, 1838), Trochiloecetes illumani Carriker, 1960 and Ricinus frenatus Burmeister, 1838 in Peru; likewise, four new hosts of the order Passeriformes are registered for Mayriphilopterus ernsti Mey, 2004, Threnetes leucurus (Linnaeus, 1766) as a new host for T. illumani and two new hosts for R. frenatus; Larus belcheri Vigors, 1829 is also reported as a new host for Quadraceps eugrammicus (Burmeister, 1838) and Austromenopon transversum Denny, 1842.

& Cribillero, 2015). Lice can be highly specific to their hosts, as several species have been identified in a single host; while some species of lice have been recorded in other closely related birds (Tavera et al., 2019). For example, lice of the genus Acidoproctus Piaget, 1878, are the most common in wild birds, having a predilection for the families Anatidae and Anseranatidae (Arnold, 2006). In the same way, it is mentioned that lice of the genera Austromenopon Bedford 1939, Quadraceps Clay and Meinertzhagen, 1939, Saemundssonia Timmermann, 1936and Ciconiphilus Bedford, 1939, are closely associated with birds of the order Charadriiformes (Figueiredo et al., 2010;Tavera et al., 2019).
The importance of the study of chewing lice in birds contemplates two points of view, which the phylogenetic that encompasses common parasites in different hosts, which confers close kinship relationships (Saavedra-Orjuela et al., 2014), and the pathological one since many lice act as biological and mechanical vectors of pathogens such as rickettsia, and the direct damage they cause due to their eating and fixation behavior in different parts of the body (Parra-Henao et al., 2011).
In Peru, studies of lice in birds have been addressed in recent years with the work of several researchers (Gomez-Puerta & Lujan 2018;Soto-Patiño et al., 2018;Tavera et al., 2019, among others), who recorded new hosts and geographic range extensions for many species of lice. Despite this, there is still a significant fraction of birds that do not present any study on ectoparasites in various regions of Peru; the present study aims to contribute to the knowledge of the diversity of lice in birds from Peru.

MATERIAL AND METHODS
The specimens studied were taken from the collection of Helminths Parasites and Related Invertebrates (HPIA-ZOO) from the Zoological Collection of the Museum of Natural History of the National University Federico Villarreal (MUFV). Hosts, locations, harvest dates and collectors are mentioned in the results section.
The morphologic study of the specimens followed the methodology proposed by Palma (1978), which consisted of rinsing the specimens in a 20% Potassium hydroxide (KOH) solution for 12 h. Then the samples were kept in distilled water for 1 h, they were dehydrated in successive series of ethanol (50%, 70%, 90% and 100%), 30 min in each solution, subsequently diaphanized in Eugenol for 24 h. Finally, the samples were mounted in Balsam of Canada. The specimens were dried at 50 -60 °C in an oven, for three weeks (Tavera et al., 2019).
The procedures for collecting parasitic fauna in the birds was approved by resolution 2558-2018-CU-UNFV that includes the code of ethics for research at the Universidad Nacional Federico Villarreal (UNFV) and by Director's Resolution N°024-2014-SERFOR-DGGSPFFS. For the management of the parasitic fauna, the guidelines of the protection and animal welfare law of Peru were followed (Law No. 30407: Article 19). The collection of the parasitic fauna is indicated by the SERFOR (Servicio Nacional Forestal y de Fauna Silvestre) of Peru that establishes the guidelines for the scientific investigation of flora and/or wild fauna (Resolution of Executive Direction Nº060-2016 SERFOR-DE).  (Dale, 1970) and in Chile it is reported in hosts of the family Laridae (González-Acuña et al., 2006), but not including L. belcheri. Likewise, Price et al. (2003) and Smith et al. (2020)  men length 1057 (974 -1100), abdomen width 580 (552 -617). Comment: Colpocephalum turbinatum is considered a generalist species since it has been reported parasitizing different orders of birds, such as Columbiformes, Falconiformes, Accipitriformes, Ciconiformes and Galliformes by various authors in different countries (Martín, 2006;Parra-Henao et al., 2011;Adly et al., 2019). This species has been recorded for the first time in Peru in the study of Dale (1970) parasitizing C. livia, this relationship coincides with our study where the association is also observed.

RESULTS
Hohorstiella Eichler, 1940 Hohorstiella lata (Piaget, 1880) ( Fig Comment: The association of Columba livia and Hohorstiella lata found in this study coincides with that reported by Quiguango (2015) in Ecuador, by Cortés et al. (2016) in Colombia and in the same way in Brazil (Amaral et al., 2017). In Peru, H. lata has not been registered in previous works, so this study would be the first to report this ectoparasite within the diversity of chewing lice for the country.  (Ferreira et al., 2013) and in columbiform birds such as the common dove C. livia in Chile by González et al. (2004), in the same way in Ecuador by Quiguango (2015), the same relationship was reported by Dale (1970) for the first time in Peru, thus coinciding with our study. ment) wider and more robust compared to the female that has it in the form of a brush and the vulvar segment of the female in two lobes (Eichler, 1953). Comment: Columbicola columbae is a cosmopolitan ectoparasite common in pigeons, and whose specific association has been reported in Peru (Naupay et al., 2015;Castro et al., 2017), Colombia (Pérez et al., 2015), Brazil (De Oliveira et al., 2000), Chile (González et al., 2004) to name a few, thus coinciding with our results. Mey, 2004 ( Quadraceps Clay & Meinertzhagen, 1939 Quadraceps eugrammicus (Burmeister, 1838) ( Fig. 5A -D) Material studied: MUFV: ZOO-HPIA:162. Host: Larus belcheri, Peru: Lima: Ventanilla, 11°52´15" S, 77°9´30" W, 21-23.ix.2017. Naupay A. Description: Based on 5 individuals (4 males, 1 female). The antennae present in the last two segments a darker coloration than the rest of the segments. The contours of the temples form an acute angle. The edge of the head has dark pigmentation, except for the frontal area. It has a long mushroom that grows from the edge of the temple. Abdominal segments have transverse dark brown spots; Dark coloration that extends to the entire proximal part of the basal plate (Timmermann, 1952 Carriker (1950), finding the congeneric species Quadraceps burhinoides Carriker, 1950 in hosts of the family Charadriidae, from Paramonga and later by Gomez-Puerta & Lujan-Vega (2018) in Surco, Lima. In our study, we reported for the first time on Q. eugrammicus in Peru and L. belcheri as a new host for this species.

Mayriphilopterus ernsti
Saemundssonia Timmermann, 1936 Saemundssonia ( Comment: This species was recorded in Chile in hosts of the family Laridae by González-Acuña et al. (2006). In Peru it has been previously reported in Leucophaeus atricilla, from Atocongo, Lima, and in Larus belcheri from Pisco, Ica (Dale, 1970). Additionally, Gomez-Puerta & Cribillero (2015) reported S. lari in Larus pipixcan in the Province of Huaral, Lima. Therefore, the ectoparasite-host relationship found in this study coincides with what has already been reported.

DISCUSSION
Peru has a great diversity of birds, with approximately 1870 species (Plenge, 2020). However, the number of bird species evaluated for the study of chewing lice is still low (Gomez-Puerta & Cribillero, 2015), despite the importance of these studies because of the effects of parasites like lice in birds. These parasites have direct pathological effects (hyperkeratosis and damage to feathers), and indirect effects such as negative sexual selection for parasitized birds (Lopez et al., 2008;Liebana et al., 2011;Moreno-Rueda & Hoi, 2012).
Among the results of this investigation, we report the species Q. eugrammicus, S. lari and A. transversum parasitizing the Peruvian seagull Larus belcheri (Charadriiformes). These three species of lice have been recorded in birds of the Laridae family in Chile, the Galapagos Islands, and Mexico (Emerson, 1972; González-Acuña et al Palma & Peck, 2013), but only S. lari was previously reported in L. belcheri (Dale, 1970). Birds of the genus Larus are highly prone to the transmission of ectoparasites due to the close relationship between their species, sharing spaces in their habitat, nesting and feeding (Gómez & González, 2010;Lenzi, 2011), which could generate contagion between species.
We also report two taxa of lice in the family Ricinidae, the genera Trochiloecetes and Ricinus, although both genera belong to the same family, they parasitize different orders of birds. In our study we report for the first-time T. illumani parasitizing T. leucurus. In the case of Ricinus frenatus, Valan et al. (2016) reported this species in association with different birds of the order Passerifomes. These results agree with the ones published by Soto-Patiño et al. (2018), who report the Ricinus genus in multiple Passerifomes birds.
Four species of ectoparasites were identified in the common pigeon Columba livia. This host bird has been studied in Brazil by Amaral et al. (2017) who reported the same species of ectoparasites in their study. In Peru, different authors have reported the same association of ectoparasites with the host, found in C. columbae (Naupay et al., 2015;Castro et al., 2017), C. turbiratum and C. compar (Dale, 1970), however, it was not previously reported for H. lata. The diversity of ectoparasites in C. livia could be attributed to the fact that this species has a close interaction with domestic and wild birds, in addition to being located in different parts of the city, which can generate a cross contagion (Begum & Sehrin, 2011).

CONCLUSION
Our results show important contributions to the diversity of chewing lice in birds of Peru, including four new reports of lice for the country. Likewise, new associations were found, expanding the list of hosts for four species of chewing lice. This work highlights the need to investigate parasites in birds that do not present previous studies on ectoparasites since these birds are likely to harbor new species for Peru and science.