**1. Introduction**

Three genera of flies within the order Diptera have larvae that parasitise avian hosts: *Protocalliphora* Hough (Calliphoridae), as well as *Passeromyia* Rodhain & Villeneuve (Muscidae) and *Philornis* Meinert (Muscidae). The adult flies in these genera are free-living and do not parasitise birds, but their larvae develop in the nests of altricial birds, feed on their avian hosts, and exhibit feeding behaviours

from hematophagy to coprophagy [1, 2]. Most larval infestations have been documented in host nests of the order Passeriformes, but larvae have also been found in nests of Accipitriformes, Apodiformes, Strigiformes and other avian taxa (*Protocalliphora*: [3]; *Passeromyia*: [4]; *Philornis*: [5, 6]). The effect of these parasitic fly larvae on host survival can be severe to mild, depending on many factors including host population size, body size, nesting density and the presence of behavioural or immunological defence mechanisms [6–8].

*Protocalliphora* is widely distributed throughout the Holarctic and contains 40+ species with obligate avian parasitic larvae [3]. Within Muscidae, only *Passeromyia* and *Philornis* larvae parasitise birds [4, 9, 10]. Both *Passeromyia* and *Philornis* are members of the subfamily Cyrtoneurininae, however their complete evolutionary relationships have yet to be resolved [11, 12]. Due to the similarities between *Passeromyia* and *Philornis*, many workers regarded the two genera as close relatives, including Skidmore [9], who stated that their similarities could not be based on convergent evolution alone. The five *Passeromyia* species include *P. steini* (Pont), *P. heterochaeta* (Villeneuve), *P. indecora* (Walker), *P. longicornis* (Macquart) and *P. veitchi* (Bezzi), and are distributed throughout Europe, Africa, Asia and Australasia [4, 13]. *Passeromyia* species differ in their larval habits. For example, *P. steini* larvae scavenge nests for organic matter and *P. indecora* larvae consume host resources as subcutaneous parasites. The 52 *Philornis* species are distributed primarily in Neotropical South America and southern North America [1, 2, 10]. *Philornis* species also show a wide range of feeding habits, including free-living coprophagous larvae, free-living semi-hematophagous larvae, and subcutaneous hematophagous larvae (**Table 1**). One species, *P. downsi*, is a recently discovered invasive species on the Galápagos Islands [14, 15]. Its semi-hematophagous larvae cause significant in-nest host mortality in their novel Galápagos land bird hosts [16]. Cladistics and molecular phylogenetic analyses suggest that the parasitic larval habits of *Passeromyia* and *Philornis* evolved independently [10, 12] despite the similarities between both genera including cocoon-wrapped puparia, life history, and clade.

The Galápagos Islands have been listed as a World Heritage site in 1978. Given a suite of threats, including introduced species, the archipelago was added to the 'List of the World Heritage in Danger' in 2007 and then removed from this list in 2010 because of actions by the Government of Ecuador to reduce invasions [17, 18]. Biological invasion is considered the greatest threat to biodiversity in the Galápagos Islands [19]. Currently, 543 terrestrial species have been introduced, of which 55 are considered harmful or potentially harmful to native biodiversity [17].

In this chapter, we consider changes in the development and behaviour of the accidentally introduced fly *P. downsi* Dodge and Aitken (Diptera: Muscidae), that is now considered the biggest threat to the survival of Galápagos land birds [20]. The first *P. downsi* larvae were collected from Galápagos land bird nests on Santa Cruz Island in 1997 [21]. From examination of museum specimens collected in 1899 (during the Stanford University Expedition led by Robert Snodgrass and Edmund Heller), in 1905–1906 and 1932 (during expeditions sponsored by the California Academy of Sciences), and in 1962 (by Robert Bowman) on Floreana Island, there is no current evidence to suggest *P. downsi* was present or abundant on the Galápagos Islands prior to 1964, though this is possible [22, 23]. By collating information from a range of researchers investigating *Philornis* in general and *P. downsi* in particular, we aim to improve our understanding of the ontogeny and behaviour of an invasive *Philornis* species within the larger context of Dipteran parasites of birds. We review *Philornis* systematics and taxonomy, discuss feeding habits across *Philornis* species, report on differences in the ontogeny of wild and captive *P. downsi* larvae, report on adult *P. downsi* behaviour, and describe changes in *P. downsi* behaviour since its discovery on the Galápagos Islands.

**53**

*1*

*2*

*3*

*4*

**Table 1.**

*P. umanani.*

*abdomen and wings [41, 43].*

*P. nielseni proposed synonym of P. seguyi [34].*

*Vespidae) [2, 29].*

**2.** *Philornis* **systematics and taxonomy**

Macquart [24] provided the first description of *Philornis* larvae when he described *Aricia pici*; a subcutaneous larval parasite found on an adult Hispaniolan woodpecker (*Melanerpes striatus;* previously *Picus striatus*) Muller (Piciformes: Picidae). Meinert [25] erected the genus *Philornis* for the single species, *P. molesta*,

*Some P. porteri larvae found in ear canals and nares of nestlings; some later instars found feeding externally on* 

*Only known specimens of P. vespidicola collected from nests of the wasp Paracharitopus frontalis (Hymenoptera:* 

Philornis *species ordered according to taxonomy, from the most basal '*aitkeni*-group' to the most recently evolved '*angustifrons*-group' (groups from [33]). Larval feeding habits are shown where known and abbreviated as follows: free-living coprophagous larvae (FLC), free-living semi-hematophagous larvae (FLSH), subcutaneous hematophagous larvae (SubH). The following nine species are not included in the list as they are currently not assigned to a taxonomic group [33] given insufficient information: P. molesta, P. nielseni, P. blanchardi, P. cinnamomina, P. convexus, P. mima, P. obscurus, P. steini,*

*P. mimicola larvae found in the nasal cavity of owls, mainly subcutaneous on body [40].*

*Taxonomic Shifts in* Philornis *Larval Behaviour and Rapid Changes in* Philornis downsi*…*

*P. amazonensis P. grandis P. porteri*<sup>1</sup>

*P. lopesi P. sabroskyi P. mimicola*<sup>2</sup>

*Falsificus* **group Larval** 

*P. fasciventris* [37] FLC *P. fumicosta P. downsi* [30] FLSH *P. schildi P. univittatus P. niger* [1, 30] SubH

*P. aikteni* [30] FLC *P. falsificus* [1, 30] FLSH *P. sperophilus* [1] SubH *P. zeteki P. carinatus* [47] SubH *P. rufoscutellaris* [36] FLC *P. deceptiva* [48, 49] SubH *P. rettenmeyeri P. trinitensis* [30] SubH *P. setinervis P. glaucinis* [30] SubH

**habits**

*Angustifrons* **group Larval** 

[43] SubH

[40] SubH

*P. pici* [24] SubH

*P. medianus* [33] SubH *P. vulgaris* [1] SubH *P. masoni* SubH *P. diminutus* [1] SubH *P. querulus* [30] SubH

*P. frontalis* [1] SubH *P. gagnei* [33] SubH *P. insularis* [33] SubH

*P. torquans* [1] SubH *P. angustifrons* [30] SubH *P. bellus* [2] SubH *P. sanguinis* [30] SubH

[50, 51] SubH

[2] SubH

*P. vespidicola*<sup>3</sup>

*P. albuquerquei*

*P. obscurinervis P. petersoni*

*P. seguyi*<sup>4</sup>

**habits**

*DOI: http://dx.doi.org/10.5772/intechopen.88854*

**habits**

*Aitkeni* **group Larval** 


*Taxonomic Shifts in* Philornis *Larval Behaviour and Rapid Changes in* Philornis downsi*… DOI: http://dx.doi.org/10.5772/intechopen.88854*

*1 Some P. porteri larvae found in ear canals and nares of nestlings; some later instars found feeding externally on abdomen and wings [41, 43].*

*2 P. mimicola larvae found in the nasal cavity of owls, mainly subcutaneous on body [40].*

*3 Only known specimens of P. vespidicola collected from nests of the wasp Paracharitopus frontalis (Hymenoptera: Vespidae) [2, 29].*

*4 P. nielseni proposed synonym of P. seguyi [34].*

#### **Table 1.**

*Life Cycle and Development of Diptera*

or immunological defence mechanisms [6–8].

from hematophagy to coprophagy [1, 2]. Most larval infestations have been documented in host nests of the order Passeriformes, but larvae have also been found in nests of Accipitriformes, Apodiformes, Strigiformes and other avian taxa (*Protocalliphora*: [3]; *Passeromyia*: [4]; *Philornis*: [5, 6]). The effect of these parasitic fly larvae on host survival can be severe to mild, depending on many factors including host population size, body size, nesting density and the presence of behavioural

genera including cocoon-wrapped puparia, life history, and clade.

considered harmful or potentially harmful to native biodiversity [17].

behaviour since its discovery on the Galápagos Islands.

The Galápagos Islands have been listed as a World Heritage site in 1978. Given a suite of threats, including introduced species, the archipelago was added to the 'List of the World Heritage in Danger' in 2007 and then removed from this list in 2010 because of actions by the Government of Ecuador to reduce invasions [17, 18]. Biological invasion is considered the greatest threat to biodiversity in the Galápagos Islands [19]. Currently, 543 terrestrial species have been introduced, of which 55 are

In this chapter, we consider changes in the development and behaviour of the accidentally introduced fly *P. downsi* Dodge and Aitken (Diptera: Muscidae), that is now considered the biggest threat to the survival of Galápagos land birds [20]. The first *P. downsi* larvae were collected from Galápagos land bird nests on Santa Cruz Island in 1997 [21]. From examination of museum specimens collected in 1899 (during the Stanford University Expedition led by Robert Snodgrass and Edmund Heller), in 1905–1906 and 1932 (during expeditions sponsored by the California Academy of Sciences), and in 1962 (by Robert Bowman) on Floreana Island, there is no current evidence to suggest *P. downsi* was present or abundant on the Galápagos Islands prior to 1964, though this is possible [22, 23]. By collating information from a range of researchers investigating *Philornis* in general and *P. downsi* in particular, we aim to improve our understanding of the ontogeny and behaviour of an invasive *Philornis* species within the larger context of Dipteran parasites of birds. We review *Philornis* systematics and taxonomy, discuss feeding habits across *Philornis* species, report on differences in the ontogeny of wild and captive *P. downsi* larvae, report on adult *P. downsi* behaviour, and describe changes in *P. downsi*

*Protocalliphora* is widely distributed throughout the Holarctic and contains 40+ species with obligate avian parasitic larvae [3]. Within Muscidae, only *Passeromyia* and *Philornis* larvae parasitise birds [4, 9, 10]. Both *Passeromyia* and *Philornis* are members of the subfamily Cyrtoneurininae, however their complete evolutionary relationships have yet to be resolved [11, 12]. Due to the similarities between *Passeromyia* and *Philornis*, many workers regarded the two genera as close relatives, including Skidmore [9], who stated that their similarities could not be based on convergent evolution alone. The five *Passeromyia* species include *P. steini* (Pont), *P. heterochaeta* (Villeneuve), *P. indecora* (Walker), *P. longicornis* (Macquart) and *P. veitchi* (Bezzi), and are distributed throughout Europe, Africa, Asia and Australasia [4, 13]. *Passeromyia* species differ in their larval habits. For example, *P. steini* larvae scavenge nests for organic matter and *P. indecora* larvae consume host resources as subcutaneous parasites. The 52 *Philornis* species are distributed primarily in Neotropical South America and southern North America [1, 2, 10]. *Philornis* species also show a wide range of feeding habits, including free-living coprophagous larvae, free-living semi-hematophagous larvae, and subcutaneous hematophagous larvae (**Table 1**). One species, *P. downsi*, is a recently discovered invasive species on the Galápagos Islands [14, 15]. Its semi-hematophagous larvae cause significant in-nest host mortality in their novel Galápagos land bird hosts [16]. Cladistics and molecular phylogenetic analyses suggest that the parasitic larval habits of *Passeromyia* and *Philornis* evolved independently [10, 12] despite the similarities between both

**52**

Philornis *species ordered according to taxonomy, from the most basal '*aitkeni*-group' to the most recently evolved '*angustifrons*-group' (groups from [33]). Larval feeding habits are shown where known and abbreviated as follows: free-living coprophagous larvae (FLC), free-living semi-hematophagous larvae (FLSH), subcutaneous hematophagous larvae (SubH). The following nine species are not included in the list as they are currently not assigned to a taxonomic group [33] given insufficient information: P. molesta, P. nielseni, P. blanchardi, P. cinnamomina, P. convexus, P. mima, P. obscurus, P. steini, P. umanani.*

#### **2.** *Philornis* **systematics and taxonomy**

Macquart [24] provided the first description of *Philornis* larvae when he described *Aricia pici*; a subcutaneous larval parasite found on an adult Hispaniolan woodpecker (*Melanerpes striatus;* previously *Picus striatus*) Muller (Piciformes: Picidae). Meinert [25] erected the genus *Philornis* for the single species, *P. molesta*,

based on larvae with distinctive posterior spiracles found parasitising nestlings. At this time, *Philornis* was suggested to be a synonym for *Protocalliphora* and assigned to the family Calliphoridae [26]. In 1921, Malloch [27] proposed the genus *Neomusca* based on adult specimens, whereas the genus *Philornis* was based on larval characters. Aldrich [28] revised this group and synonymized *Neomusca* with *Philornis* as independent genera, assigning both within the family Muscidae (Anthomyiidae at the time). This revision was supported by further work on *Philornis* species, as new and previously described species were transferred from other genera including *Hylemyia, Mesembrina, Neomusca* and *Mydaea* [9, 28–31]. *Philornis* adults are distinguished from other muscid genera by the presence of hair on the anepimeron and the postalar wall [1, 32].

Using morphological and ecological data, *Philornis* can be divided into three phylogenetic groups: the '*aitkeni*-group', the '*falsificus-*group' and the '*angustifrons-*group' [33]. Male characters (given few female specimens) generally define the most basal lineage of *Philornis*, the '*aitkeni-*group', including enlarged upper eye facets in holotypic males [29, 33]. The members of this group display adult character states that are considered primitive among muscids (i.e., enlarged upper eye facets and presence of cilia on the surface of the wing vein R4+5) [33]. This group includes *P. aitkeni* (Dodge), *P. rufoscutellaris* (Couri), and *P. fasciventris* (Wulp). The phylogeny of the *aitkeni*-group is not completely resolved because of missing information about life history and morphology, as female and larval specimens are not available for many species. The second group, the *falsificus-*group, is defined primarily by *P. falsificus* (Dodge and Aitken), whose larvae are free-living [9]. Common morphological characters include five scutellar marginal setae that also place *P. fumicosta* (Dodge), *P. univittatus* (Dodge), *P. grandis* (Couri) and *P. sabroskyi* (Albuquerque) within this group [33]; however, data on the ecology of these species are missing. More information on larval life history is necessary to confirm whether species other than *P. falsificus* belong in this lineage. Despite a similar life history to *P. falsificus*, *P. downsi* is not within the *falsificus-*group [1, 9, 33], but forms a sister-group to all species within the *angustifrons*-group for which larval habits have mostly been documented (**Table 1**). The *angustifrons*-group is the most recently evolved and largest of the three *Philornis* lineages and contains species with subcutaneous hematophagous larvae as well as *P. downsi* with semi-hematophagous larvae.

Comparative taxonomic analyses of *Philornis* species have been hampered by a lack of specimens and information [9]. For several species of *Philornis*, their morphological descriptions are based solely on one sex, generally males. In others, the holotype is missing or destroyed, and so other traits and ecological information are missing. *Philornis blanchardi* (Garcia) has been originally identified and described in Argentina from a single female specimen, which has since been lost [34]. This specimen may belong to a previously described species as it has not been captured and identified since, however the original description is considered sufficiently unique that it may be a separate species [34]. The single male holotype used to describe *P. umanani* (Garcia) has also been lost and due to the lack of detail provided in the original description, this species is deemed unrecognisable and is now considered a *nomen dubium* [34]. Evidence of a *Philornis* species complex within specimens of *P. seguyi* (Garcia) and *P. torquans* (Nielsen) in Argentina throws further doubt on the original taxonomic characterisation of many *Philornis* species [35]. These issues highlight the need for more extensive molecular and morphological analysis of currently recognised *Philornis* species to confirm species classifications and their evolutionary relationships.

**55**

*Taxonomic Shifts in* Philornis *Larval Behaviour and Rapid Changes in* Philornis downsi*…*

*Philornis* species differ in their larval feeding habits, which include coprophagous and hematophagous diets (**Table 1**). Larval habits have been documented for 30 out of 52 described species (**Table 1**). The most basal group in the *Philornis* phylogeny (*aikteni*) have free-living coprophagous larvae [33]. These larvae parasitise cavity nesting host species that do not remove waste, such as the rufous-tailed jacamar (*Galbula ruficauda*) Cuvier (Piciformes: Galbulidae) and appear to be specific to this type of nest [2, 5, 30, 36, 37]. Free-living saprophagous larvae in the nest are regarded as the ancestral trait, evolving into coprophagous larvae, semi-hematophagous larvae and then subcutaneous larvae [9, 33]. This transition is also supported in *Passeromyia* where species show a similar order of descent [4, 10, 33]. Two documented species, *P. downsi* (*angustifrons*-group) and *P. falsificus* (*falsificus-*group)*,* have free-living and semi-hematophagous larvae, although other undescribed species within the *falsificus-*group may also have free-living larvae [1, 30, 33]. Most *Philornis* species (83%) have larvae with subcutaneous hematophagous feeding habits, which is also the primary larval strategy in the *angustrifrons*-group. Within this group, only *P. downsi* has non-subcutaneous larvae. The semi-hematophagous *P. downsi* larvae may be similar to *P. falsificus* (*falsificus*-group), which is also suspected of having free-living semi-hematophagous larvae [33]—but not enough is known about the biology of the *falsificus*-group. While *P. falsificus* is considered a free-living ectoparasite [30], this assessment is limited by the observations to date of later instars and puparia [38, 39]. On the other hand, in two species with subcutaneous feeding habits in the *angustifrons-*group, a few *Philornis* larvae have been also observed in avian nares. Specifically, *P. mimicola* larvae have been found in the nares of ferruginous pygmy-owl nestlings (*Glaucidium brasilianum*) Gmelin (Strigiformes: Strigidae), but most larvae occurred subcutaneously [40]. Larvae of *P. porteri* (Dodge) have been found in the nares and ear canals of some nestlings [41, 42], and 3rd instar larvae observed to feed externally on the abdomen and wings of their hosts [41, 43]. In the semi-hematophagous *P. downsi* larvae, 1st instars regularly reside within the avian nares [44–46] and later instars move to the base of the nest where they emerge at dusk and dawn to feed externally on the blood and tissue of the developing birds [45, 46]. Lineages with free-living larvae have been far less studied than lineages with subcutaneous larvae (**Table 1**). Free-living larvae move freely within the host nest, detach from the host at various times and reside in the nest base during the day, making them less conspicuous to human observers [45, 46]. In contrast, subcutaneous larvae reside under the skin of the

*DOI: http://dx.doi.org/10.5772/intechopen.88854*

**3.1** *Philornis* **larval behaviour**

**3. Larval feeding habits across** *Philornis* **species**

host and hence can be detected when nestlings are examined.

**4.1** *Philornis downsi* **larval instars**

**4.** *Philornis downsi* **larval development in the wild and in the laboratory**

*Philornis downsi* larval development is split into three instar development stages. 1st instar larvae generally reside in the naris and ear canals of developing nestlings, but some have also been found moving freely within the nesting material [21, 52, 53]. First instars are commonly collected from 2 to 3 day old nestlings [43]. Late 2nd and 3rd instar larvae are generally free-living, residing within the base of the nest and feeding externally on nestlings at night [14, 45, 46]. These later instar larvae feed
