External and gastrointestinal parasites of the Franklin’s Gull, Leucophaeus pipixcan (Charadriiformes: Laridae), in Talcahuano, central Chile

Parasitas externos e gastrointestinais da gaivota de Franklin Leucophaeus pipixcan (Charadriiformes: Laridae) em Talcahuano, Chile central

Abstract

Parasitological studies of the Franklin's gull, Leucophaeus pipixcan, are scarce, and knowledge about its endoparasites is quite limited. In order to describe its parasitic community, a total of 60 Franklin’s gulls were captured in the coastal area in central Chile, using modified Bal-chatri traps. Ectoparasites were collected from all 60 live individuals through inspection of their plumage, while 30 were examined for endoparasites by standard parasitological necropsy. The prevalence of ectoparasites was 78.3%, including the feather mite Zachvatkinia larica (43.3%) and four species of lice: Actornithophilus piceus lari (15.0%), Austromenopon transversum (6.7%), Quadraceps punctatus (10.0%) and Saemundssonia lari (46.7%). Some 25 of 30 (83.3%) of birds necropsied were parasitized with the following helminths: Aporchis sp. (6.7%), Tetrabothrius cylindraceus (56.7%), Cyclophyllidea gen. sp. (3.3%), Profilicollis altmani (56.7%), Eucoleus contortus (10.0%), Cosmocephalus obvelatus (13.3%), Paracuaria adunca (10.0%), Stegophorus sp. (3.3%) and Tetrameres skrjabini (3.3%). To our knowledge, with the exception of P. altmani, these helminths are reported for first time in the Franklin's gull.

Keywords:  Acari; seabirds; helminths; Phthiraptera; Laridae

Resumo

Existem escassos estudos de parasitismo em gaivota-de-Franklin Leucophaeus pipixcan, e o conhecimento sobre seus endoparasitas é ainda mais limitado. Com o objetivo de descrever sua comunidade parasitaria, um total de 60 gaivotas-de-Franklin foram capturadas usando-se armadilhas Bal-chatri numa zona costeira do centro do Chile. A pesquisa de ectoparasitas foi realizada em todos os indivíduos capturados e, para os endoparasitas, foram examinados 30 deles por necropsias. A prevalência de ectoparasitas foi de 78,3%, incluíndo o ácaro de pena Zachvatkinia larica (43,3%) e outras quatro espécies de piolhos, Actornithophilus piceus lari (15,0%), Austromenopon transversum (6,7%), Quadraceps punctatus (10,0%) e Saemundssonia lari (46,7%). Das aves necropsiadas, 83,3% estavam parasitadas por helmintos, sendo registrados Aporchis sp. (6,7%), Tetrabothrius cylindraceus (56,7%), Cyclophyllidea gen. sp. (3,3%), Profilicollis altmani (56,7%), Eucoleus contortus (10,0%), Cosmocephalus obvelatus (13,3%), Paracuaria adunca (10,0%), Stegophorus sp. (3,3%) e Tetrameres skrjabini (3,3%). Com exceção de P. altmani, este é o primeiro relato desses helmintos parasitando gaivotas-de-Franklin.

Palavras-chave:  Acari; aves marinhas; helmintos; Phthiraptera; Laridae

Introduction

The Franklin’s gull, Leucophaeus pipixcan (Wagler, 1831), is a migratory bird that travels every year from breeding sites in the United States and Southern Canada (Harrison, 1983) to Central and South America; most individuals stay in the southern hemisphere during the austral summer (Marin & Couve, 2001). Its presence on the Chilean coasts is observed from Arica (18°28'S, 70°17'W) to the extreme south of the country, Aysén (45°24'S, 72°42'W), with accidental records in the Magellan and Antarctic Regions (Couve et al., 2016).

Most studies of parasitic fauna in the Franklin's gull concern ectoparasites. To date, four species of lice have been found in the Franklin’s gull: Saemundssonia lari (Fabricius, 1780), Quadraceps punctatus (Burmeister, 1838), Actornithophilus piceus lari (Packard,1870) and Austromenopon transversum (Denny, 1842), recorded in the Neotropical region and Northern hemisphere (Emerson, 1972; Palma, 1995; Hellenthal et al., 2004; González-Acuña et al., 2006, 2011; Galloway et al., 2014; Gomez-Puerta & Cribillero, 2015). In addition, the nasal mite Turbinoptes strandtmanni Boyd, 1949 and feather mites of the genera Alloptes Canestrini, 1879, Zachvatkinia Dubinin, 1949 and Ingrassia Oudemans, 1905 were reported from this host in North America (Galloway et al., 2014; Knee & Galloway, 2016).

Regarding its endoparasites, there are records of the acanthocephalan Profilicollis altmani (Perry, 1942) Van Cleave, 1947 (= P. bullocki), isolated from this host in South America (Peru and Chile) (Tantaleán et al., 2005; Riquelme et al., 2006; Rodríguez et al., 2017), and the filarioid nematode Eulimdana sp. in Canada (Bartlett, 1992). Despite its wide geographical distribution, reports on its parasitic fauna are scarce, and knowledge about its internal parasites is quite limited. This study aims to provide new records of diversity and prevalence of parasites associated with the Franklin's gull.

Materials and Methods

The study was carried out in Talcahuano, a coastal city in central Chile (36º44'10”S, 73º06'17”W) (Figure 1), during January and February 2008 and March 2009. Sixty Franklin’s gulls were captured with modified Bal-chatri traps pre-baited with fish. Captured gulls were visually examined, inspecting their feathers and skin for ectoparasites, which were collected and preserved in 70 GL ethanol. Half of the individuals were released, and the rest were euthanized by cervical dislocation. All procedures were authorized by the Agricultural and Livestock Service (SAG) under the resolutions No 1801 and 811.

Figure 1
Sampling locations of Franklin’s gull in Talcahuano, central Chile.

The 30 dead birds were stored in plastic bags and immediately taken to the laboratory for parasitological necropsy. The extracted feather lice were cleared and mounted in Canada balsam, as described by Palma (1978) and Price et al. (2003). Mites were cleared in Nesbitt's solution for 72 hours and mounted in Berlese's solution, as described by Krantz & Walter (2009). The identification of lice followed the taxonomic keys by Clay (1949, 1959, 1962), Price & Clay (1972), Timmermann (1952), and Ward (1955); for mites, the keys by Gaud & Atyeo (1996), and Mironov (1989) were applied.

Bird dissection and endoparasite collection followed the necropsy technique described by Oyarzún-Ruiz & González-Acuña (2020). Trematodes and cestodes were fixed with 70° ethanol and stained with Alum Carmine stain; and finally, nematodes and acanthocephalan were fixed in ethanol 70° and later cleared in lactophenol. For the identification of helminths, the keys proposed by Anderson et al. (2009), Khalil et al. (1994), Yamaguti (1958, 1959, 1961, 1963) and Baruš et al. (1978) were followed. Parasitological descriptors such prevalence, mean intensity, range and mean abundance were calculated according to Bush et al. (1997).

Results and Discussion

Phthiraptera

Lice were recorded on 53.3% (32/60) of gulls, corresponding to four species (Figure 2222d): Actornithophilus piceus lari (Amblycera: Menoponidae) was collected from the wings of 15% (9/60) of the individuals, with a total of 17 specimens (Table 1). The genus Actornithophilus is exclusive to the order Charadriiformes (Clay, 1962; Price et al. 2003), while the cosmopolitan subspecies A. piceus lari is restricted to the family Laridae, being reported from the genera Larus, Pagophila, Rhodostethia, Rissa, Xema and Leucophaeus (Emerson, 1972; Price et al. 2003). This report adds A. piceus lari to the list of parasites of L. pipixcan.

Figure 2
Ectoparasites recorded on Franklin’s gull from Talcahuano, Chile. Lice (a-d). (a) Actornithophilus piceus lari. Scale bars= 1 mm; (b) Austromenopon transversus. Scale bars= 500 µm; (c) Quadraceps punctatus. Scale bars= 500 µm; (d) Saemundsonia lari. Scale bars= 500 µm. Mites (e-f); (e) Zachvatkinia larica female, dorsal view (left), ventral view (right). Scale bar= 200 µm; (f) Z. larica male, dorsal view (left), ventral view (right). Scale bar= 200 µm.

Table 1
Summary of external parasites found in 60 Franklin’s gulls (Leucophaeus pipixcan) from Talcahuano, central Chile.

Species	Location (feathers)	Prevalence (%)	Range	Mean intensity	Mean abundance	Total parasites
Phthiraptera
Actornithophilus piceus lari	Wings	15.0	1-4	1.9	0.3	17
Austromenopon transversum	Body	6.7	1-3	2	0.13	6
Quadraceps punctatus	Wings	10.0	1-3	1	0.10	8
Saemundssonia lari	Head/neck	46.7	1-17	3.8	46.7	106
Acari
Zachvatkinia larica	Primaries	43.3	2-969	156.9	43.3	4080

Austromenopon transversum (Amblycera: Menoponidae) was collected with a prevalence of 6.7% (4/60), the lowest among lice detected (Table 1). These parasites were isolated from the chest and belly of the individuals, with a total of six specimens. Lice of the genus Austromenopon have been reported as parasites of, Charadriiformes, Pelecaniformes and Procellariiformes (Clay, 1959; Price & Clay, 1972; Pilgrim & Palma, 1982). Austromenopon transversum has been mainly isolated from gulls of the genus Larus (Price et al., 2003). This finding adds to the reports of parasitism of A. transversum on Franklin's gull, recorded in Europe (Belgium) (Hellenthal et al., 2004), North America (Emerson, 1972; Galloway et al., 2014) and South America (Chile) (González-Acuña et al., 2011).

Quadraceps punctatus (Ischnocera: Philopteridae) was collected from the wings with 10.0% (6/60) of prevalence, presenting the lowest mean intensity and mean abundance of lice (Table 1). The cosmopolitan genus Quadraceps is composed of a wide variety of species and subspecies that parasitize birds of the order Charadriiformes (Price et al., 2003). Quadraceps punctatus has been frequently recorded on birds of the family Laridae, mainly in those of the genus Larus, with records from the Palearctic, Nearctic and Neotropical regions, also Australasia (Timmermann, 1952; Price et al., 2003). Quadraceps punctatus is one of the four lice species identified as parasites in L. pipixcan, being previously reported in Canada (Galloway et al., 2014), Belgium (Hellenthal et al., 2004), Galapagos (Palma, 1995), and Chile (González-Acuña et al., 2011). In Chile, this louse has also been isolated from the gulls Larus dominicanus and L. modestus (González-Acuña et al., 2011).

Saemundssonia lari (Ischnocera: Philopteridae) was collected from the head and chin regions with 46.7% (28/60) of prevalence, and a total of 106 specimens (Table 1). Lice of the genus Saemundssonia inhabit preferentially the head of their hosts (Johnson et al., 2012; Yamagishi et al., 2014). Morphologically, it has a triangular anterior margin with a rostral groove, the common characteristic of head lice, that helps them hold on feathers and resist against scratches (Price et al., 2003; Johnson et al., 2012). Saemundssonia lari was the most prevalent parasite in this study, with the highest mean abundance, that presumably related to its capability ecological niche occupied to resist to grooming (Johnson et al., 2012). This cosmopolitan species parasitizes birds of the family Laridae, with reports in those of the genera Gabianus, Larus, Pagophila, Rissa and Xema (Price et al., 2003; Vas et al., 2012), and has been previously recorded from L. pipixcan in Belgium (Hellenthal et al., 2004), Canada (Galloway et al., 2014), Peru (Gomez-Puerta & Cribillero, 2015), and Chile (González-Acuña et al., 2006, 2011).

Acari

The feather mite Zachvatkinia larica Mironov, 1989 (Acari: Avenzoariidae) was found on 43.3% (26/60) of the gulls examined (Figure 22f). This mite had the highest mean intensity among other ectoparasites (Table 1), with 4080 specimens collected from vanes of primaries, secondaries, and rectrices. The predilection for these microhabitats in the plumage has been previously documented for mites of the genus Zachvatkinia Dubinin, 1949 (Mironov, 1989; Dabert & Mironov, 1999; Bridge, 2003; Dabert et al., 2015), assuming that their location in relatively exposed areas could facilitate transmission of mite individuals between host individuals (Dabert et al., 2015). This feather mite genus, which is specifically associated with gulls, terns (Charadriiformes: Laridae), crab plovers (Charadriiformes: Dromadidae), and with Procellariiformes (Mironov, 1989; Gaud & Atyeo, 1996; Negm et al., 2013), is usually very abundant on their hosts (Mironov & Stefan, 2013), as well as in this report. Zachvatkinia larica has been isolated from various gull genera (Larinae) in Russia (Mironov, 1989), Netherlands (Siepel et al., 2016), North America (Galloway et al., 2014; Beltrán-Ontiveros & Vergara-Pineda, 2016), Colombia (Barreto et al., 2012) and Korea (Han et al., 2016). In addition, this mite was reported for the first time as a parasite in L. pipixcan by González-Acuña et al. (2011) in the same locality of the present study.

Trematodes

Aporchis sp. (Digenea: Echinostomatidae) was collected from the small intestine of two individuals with a prevalence of 6.7% (Table 2, Figure 3a). The genus Aporchis (Stossich, 1905) has a wide geographical distribution being associated with seabirds, and was previously registered in the Palearctic (Bosch et al., 2000; Roca et al., 2001; Santoro et al., 2011; Radwan, 2014), Nearctic (McCauley & Pratt, 1960; Hoberg, 1981) and Neotropical regions (González-Acuña et al., 2009). In Chile, this genus was found in the Kelp gull, L. dominicanus, by González-Acuña et al. (2009), with which the Franklin's gull shares habitats during the southern summer, and it is still unknown what other gull species could act as a host in the area. The specific identification could not be achieved because the peristomic disc of specimens lack of their spines which are required for its diagnosis (Yamaguti, 1958). Aporchis sp. in toto is shown in Figure 3a. Its narrower forebody is indicated by the right arrowhead; at the anterior end, the peristomic disc is indicated by an asterisk and the left arrowhead shows the acetabulum. The present study represents the first report of the genus Aporchis in L. pipixcan, expanding its host range.

Table 2
Summary of endoparasites found in 30 Franklin’s gulls (Leucophaeus pipixcan) from Talcahuano, central Chile.

Species	Location	Prevalence (%)	Range	Mean intensity	Mean abundance	Total parasites
Trematoda
Aporchis sp.	Small intestine	6.7	4-6	5	0.3	10
Cestoda
Tetrabothrius cylindraceus	Small intestine	56.7	1-7	1.8	1	30
Cyclophyllidea gen. sp.	Small intestine	3.3	2	2	0.1	2
Acanthocephala
Profilicollis altmani	Small intestine	56.7	1-34	10.1	5.7	171
Nematoda
Eucoleus contortus	Esophagus	10	1-2	1.7	0.2	5
Cosmocephalus obvelatus	Esophagus/ proventriculus	13.3	1-5	1.7	0.2	7
Paracuaria adunca	Proventriculus/gizzard	10	1-3	1.7	0.2	5
Stegophorus sp.	Gizzard	3.3	1	1	0.03	1
Acuariidae gen. sp. (larva)	Gizzard	3.3	1	1	0.03	1
Tetrameres skrjabini	Esophagus/ proventriculus	3.3	-	7	0.2	7

Figure 3
(a) Aporchis sp., in toto. Right, scale bar= 2 mm. Upper left side, scale bar= 500 µm. Egg with its unique polar filament. Bottom left side, scale bar= 125 µm; (b) Tetrabothrius cylindraceus. Scale bar= 250 µm; (c) Profilicollis altmani, worm in toto. Right, scale bar= 5 mm. Upper left side, scale bar= 250 µm. Elongated eggs. Bottom left side, scale bar= 125 µm; (d) Cosmocephalus obvelatus. Scale bar= 250 µm. Upper left side, scale bar= 125 µm; (e) Paracuaria adunca. Central image, scale bar= 125 µm. Left, scale bar= 30 µm. Upper right side, scale bar= 250 µm. Bottom right side, scale bar= 30 µm; (f) Stegophorus sp. Left, scale bar= 60 µm. Upper right side, scale bar= 30 µm. Bottom right side, scale bar= 30 µm.

Cestodes

The species Tetrabothrius cylindraceus (Rudolphi, 1819) (Tetrabothriidea: Tetrabothriidae) was isolated from the small intestine of 17 birds, with a prevalence of 56.7% (Table 2; Figure 3b). The genus Tetrabothrius includes more than 50 species parasitizing seabirds and marine mammals. Both groups act as definitive hosts, while crustaceans, fishes, and cephalopods are intermediate hosts (Hoberg, 1989). This parasite has been recorded in various birds of the order Charadriiformes (Alcidae, Stercorariidae, Laridae) from Europe (Roca et al., 2001; Santoro et al., 2011; Haukisalmi, 2015; Parejo et al., 2015), Asia (Uchida et al., 2005; Kuklin, 2011), North America (Threlfall, 1968; Muzaffar, 2009), South America (Argentina and Chile) (González-Acuña et al., 2009; Diaz et al., 2011), and Antarctica (Barbosa & Palacios, 2009; Rocka, 2019). In Latin America, it has been isolated from the gull L. dominicanus in Chile (Torres et al., 1991, 1992, 1993; González-Acuña et al., 2009) and later from the same host in Argentina (Diaz et al., 2011). Despite being a common parasite in seagulls, this study presents the first record of T. cylindraceus in L. pipixcan worldwide.

A few cyclophyllidean tapeworms were isolated from the small intestine of gulls with a prevalence of 3.3% (1/30) (Table 2). However, its specific identification could not be achieved because the poor preservation of proglottids and loss of rostellar hooks. The scolex is shown in Figure 3b, where the arrowhead indicates its four semi-circular suckers.

To our knowledge, the only record of a cyclophyllidean tapeworm in the Franklin’s gull corresponds to Retinometra caballeroi (Flores-Barroeta, 1953) (syn. Aploparaksis caballeroi) (Hymenolepididae), which was reported by first time in Panama (Bondarenko & Kontrimavichus, 2018). Furthermore, other genera of family Dilepididae (e.g. Alcataenia and Anomotaenia) have been recorded in other gulls such L. dominicanus and brown-hooded gull Chroicocephalus maculipennis from Chile (Torres et al., 1991, 1992, 1993; González-Acuña et al., 2009) and other South American (Diaz et al., 2011) and European countries (Sanmartín et al., 2005; Álvarez et al., 2006; Sagerup et al., 2009; Santoro et al., 2011). Also, other cyclophyllidean genera such Aploparaksis (Aploparaksidae), Nadejdolepis, Microsomacanthus and Wardium (Hymenolepididae) have been recorded in gulls around the world (Khalil et al., 1994; González-Acuña et al., 2009; Sagerup et al., 2009; Bondarenko & Kontrimavichus, 2018). Additional surveys are required to establish the identity of these tapeworms.

Acanthocephala

Profilicollis altmani (Polymorphida: Polymorphidae) was the only acanthocephalan found in this study, collected from the small intestine of 56.7% (17/30) of gulls (Table 2; Figure 3c). Figure 3c shows an individual of P. altmani with its spherical proboscis (right) and in detail (upper left side) the rows of small hooks present on the surface of this structure (indicated by asterisks).

This parasite has an indirect life cycle with decapod crustaceans as intermediate hosts; Emerita analoga (Stimpson, 1857) and Hemigrapsus crenulatus (Milne-Edwards, 1837) (Balboa et al., 2009; González-Acuña et al., 2009), both widely distributed along the coast of Chile (Retamal, 1981). Profilicollis altmani has been reported in Charadriiformes from the Neotropical region (Tantaleán et al., 2005; Riquelme et al., 2006; Gonzáles-Viera et al., 2009; González-Acuña et al., 2017; Rodríguez et al., 2017; Gomez-Puerta & Naupay, 2019), being previously isolated from Franklin's gulls in northern and central Chile and Peru (Tantaleán et al., 2005; Riquelme et al., 2006; Rodríguez et al., 2017), areas where it has also been recorded on its intermediate hosts and sympatric birds (Riquelme et al., 2006; Iannacone et al., 2007; Balboa et al., 2009). The present study provides a new report of this parasite-host association in central coasts of Chile, where L. pipixcan has been shown to be a better host that increases the abundance of P. altmani when it arrives to this area (Riquelme et al., 2006).

Nematodes

Eucoleus contortus (Creplin, 1839) (Enoplida: Capillariidae) was collected from the esophagus of three individuals, with 10% (3/30) prevalence (Table 2). This nematode is frequently found in the esophagus of a wide variety of aquatic birds such as gulls, grebes, cormorants and ducks in Europe (Bosch et al., 2000; Sanmartín et al., 2005; Álvarez et al., 2006; Santoro et al., 2011), North America (Fedynich et al., 1997; Threlfall et al., 1982), Asia (Yoshino et al., 2009), and South America (Brazil and Chile) (Monteiro et al., 2011; González-Acuña et al., 2017; Carvalho et al., 2019). Eucoleus contortus was reported for the first time in Chile parasitizing Podiceps occipitalis (Podicipedidae) (González-Acuña et al., 2017); it is suspected that it could be an accidental infestation because of sharing the habitat with potential hosts. This study provides the first record of E. contortus in L. pipixcan globally, expanding its host range.

Cosmocephalus obvelatus (syn: C. firlotlei) (Creplin, 1825) (Spirurida; Acuariidae) was collected from the esophagus and proventriculus of 13.3% (4/30) of the individuals (Table 2, Figure 3d), the usual location, since larvae initially invade the proventriculus and later settle in the esophagus (Wong & Anderson, 1982a). Figure 3d shows the anterior end of an individual of C. obvelatus, the arrowhead indicates the cephalic cordons. On the upper left side is shown the posterior end of a male worm. The asterisks are indicating the pre-anal and post-anal papillae, on the ventral surface, and the arrowhead indicates the left spicule, which is triangular at its distal border.

The life cycle of this species includes amphipod crustaceans and fishes as intermediate and paratenic hosts, respectively (Wong & Anderson, 1982a; Anderson, 2000). This nematode has been reported in a wide variety of piscivorous birds (Sphenisciformes, Charadriiformes, Anseriformes, Pelecaniformes, Procellariiformes, Podicipediformes, Gaviiformes, and Ciconiiformes) from all continents except Antarctica (Anderson & Wong, 1981; Sanmartín et al., 2005; Álvarez et al., 2006; Mutafchiev et al., 2010; Santoro et al., 2011). In the southern cone of Latin America, it has been isolated from the penguins Spheniscus humboldti (Spheniscidae) (Fernández et al., 2019), Spheniscus magellanicus (Spheniscidae) (Diaz et al., 2001, 2010), the generalist raptor Milvago chimango (Falconidae) (Oyarzún-Ruiz et al., 2016) and L. dominicanus (Gonzalez-Acuña et al., 2009; Diaz et al., 2011). Cosmocephalus obvelatus has been described in the American continent from larids sympatric to the Franklin's gull, including Rissa tridactyla, Larus californicus, Larus delawarensis, Larus hyperboreus, Larus marinus, and L. dominicanus (Rodrigues de Olivera & Vicente, 1963; Threlfall, 1968; Anderson & Wong, 1981; Gonzalez-Acuña et al., 2009; Diaz et al., 2011; Hannon et al., 2016). This is the first report worldwide of this nematode parasitizing L. pipixcan.

Paracuaria adunca (Creplin, 1846) (Spirurida; Acuariidae) was isolated in the 10% (3/30) of birds (Table 2; Figure 3e). These nematodes were collected from the proventriculus and under the koilin layer of gizzard, which is in agreement with Anderson & Wong (1982) and Wong & Anderson (1982b). Figure 3e shows an individual of this species. In the center of the figure, is shown the anterior part of the worm with its two pseudolabia and striated cuticle. The position of the deirid is posterior to the nerve ring (white asterisk) and its tridentate shape is shown in detail on the left picture. The posterior end of male worm (upper right side) has 2 dissimilar spicules; right spicule is short and stout, rounded at its basis (arrow), and left spicule is long, slender (arrowhead) and presents a triangular and serrated distal tip, shown in detail on the bottom right side.

Through experimental studies, Anderson & Wong (1982) showed that amphipod crustaceans and fishes act as a source of transmission for P. adunca, with the latter group as the main source of infection in seagulls. Due to the above, this nematode mainly parasitizes piscivorous birds as has been reported in Europe, Asia, North America, South America and Cuba (Baruš et al., 1978; Wong & Anderson, 1982b; Diaz et al., 2004, 2011; Sanmartín et al., 2005; Álvarez et al., 2006; Santoro et al., 2011; Hannon et al., 2016). In Chile, it has been documented for the first time in the raptor M. chimango that is attributable to its piscivorous food habits (Oyarzún-Ruiz et al., 2016), and in the Kelp gull, L. dominicanus, (González-Acuña et al., 2009), a host species for which exists other records in Latin America (Diaz et al., 2004, 2011). To our knowledge, this is the first report of the Franklin's gull as a host of this nematode.

Stegophorus sp. (Spirurida: Acuariidae) and other unidentified acuariid larva were isolated under the koilin layer of the gizzard from two different gulls, both with a prevalence of 3.3% (1/30) (Table 2; Figure 3f). The specific diagnosis for Stegophorus could not be achieved because the isolated specimen corresponded to an immature female worm (Anderson et al., 2009). Figure 3f shows the only specimen of Stegophorus sp. isolated. On the left is shown the anterior end with two pseudolabia covered at its posterior border by teeth (asterisks). The position of the deirid is over the union between the buccal capsule and muscular esophagus (arrowhead), it has a rounded tridentate shape shown bordered by asterisks on the right side. Detail of pseudolabia, which appears as a collarette with several teeth, are indicated on the bottom right side by arrowheads.

This genus has been reported previously in several piscivorous birds such orders Procellariformes, Sphenisciformes and Charadriiformes (Baruš et al., 1978; Mutafchiev et al., 2014). Those species reported parasitizing charadriiform birds (e.g. the genera Larus and Stercorarius) are the following: Stegophorus arctowskii Zdzitowiecki & Dróżdż, 1980, Stegophorus macronectes (Johnston & Mawson, 1942), Stegophorus stellaepolaris (Parona, 1901) and Stegophorus stercorarii Leonov, Sergeeva & Tsimbalyuk, 1966 (Sagerup et al., 2009; Mutafchiev et al., 2014). These parasites, like other acuariid nematodes, are probably transmitted mostly by consumption of fishes which could act as paratenic hosts (Anderson & Wong, 1982; Wong & Anderson, 1982a; Anderson, 2000). To our knowledge, the present record of the genus Stegophorus is the first for the Franklin’s gull.

Tetrameres skrjabini (Panova, 1962) (Spirurida: Tetrameriidae) was isolated from a single gull with a prevalence of 3.3% (1/30) (Table 2). One male specimen was found in the esophagus lumen, and seven females were found into the proventriculus glands, location typically adopted by this genus in the case of females, but not males, who are usually found on the lumen or mucosa of the proventriculus (Kinsella & Forrester, 2008). This genus has an indirect life cycle, with crustaceans acting as intermediate hosts in aquatic environments (Anderson, 2000; Kinsella & Forrester, 2008), while birds of the orders Anseriformes, Ardeiformes, Gruiformes and Charadriiformes act as definitive hosts (Mollhagen, 1976; Kinsella & Forrester, 2008). In spite of the above, T. skrjabini has been reported more frequently in birds of the subfamilies Sterninae and Larinae (Mollhagen, 1976), with reports in Europe (Sanmartín et al., 2005; Álvarez et al., 2006; Kavetska et al., 2012; Parejo et al., 2015), Asia, North America (Mollhagen, 1976) and South America (González-Acuña et al., 2009). In the Neotropical region, it has only been isolated from L. dominicanus in south-central Chile (González-Acuña et al., 2009). The latter locality is close to that of the present study, where it lives in sympatry with L. pipixcan (González-Acuña et al., 2011). This is the first report of this nematode as a parasite of L. pipixcan worldwide.

Conclusion

The present study contributes to the current knowledge on the diversity of parasites associated with Franklin's gulls, reporting for this host five ectoparasites (feather mites and chewing lice) and nine gastrointestinal parasites. New host-parasite associations are reported, including the following helminths: Cyclophyllidea gen. sp., Aporchis sp., Eucoleus contortus, Cosmocephalus obvelatus, Paracuaria adunca, Stegophorus sp., and Tetrameres skrjabini as endoparasites of L. pipixcan.

Acknowledgements

We thank the students who collaborated during fieldwork and laboratory activities related to this study. Also, to Julia Diaz who provide us with publications. The fieldwork carried out during this research work was funded by the FONDECYT, project number 1170972. Authors would like to thank Diane Haughney for the correction of the English text and Juliana Vianna for correction of the Portuguese text.

• How to cite: González-Acuña D, Veloso-Frías J, Missene C, Oyarzún-Ruiz P, Fuentes-Castillo D, Kinsella JM, et al. External and gastrointestinal parasites of the Franklin's Gull, Leucophaeus pipixcan (Charadriiformes: Laridae), in Talcahuano, central Chile. Braz J Vet Parasitol 2020; 29(4): e016420. https://doi.org/10.1590/S1984-29612020091

References

• Álvarez MF, Cordeiro JA, Leiro JM, Sanmartín ML. Influence of host age and sex on the helminth fauna of the yellow-legged gull (Larus michahellis) in Galicia (Northwestern Spain). J Parasitol 2006; 92(3): 454-458. http://dx.doi.org/10.1645/GE-3546.1 PMid:16883985.
  » http://dx.doi.org/10.1645/GE-3546.1
• Anderson RC, Chabaud AG, Willmott S. Keys to the nematode parasites of vertebrates: archival volume Wallingford: CAB International; 2009. http://dx.doi.org/10.1079/9781845935726.0000
  » http://dx.doi.org/10.1079/9781845935726.0000
• Anderson RC, Wong PL. Redescription of Cosmocephalus obvelatus (Creplin, 1825) (Nematoda: Acuarioidea) from Larus delawarensis Ord (Laridae). Can J Zool 1981; 59(10): 1897-1902. http://dx.doi.org/10.1139/z81-258
  » http://dx.doi.org/10.1139/z81-258
• Anderson RC, Wong PL. The transmission and development of Paracuaria adunca (Creplin, 1846) (Nematoda: Acuarioidea) of gulls (Laridae). Can J Zool 1982; 60(12): 3092-3104. http://dx.doi.org/10.1139/z82-393
  » http://dx.doi.org/10.1139/z82-393
• Anderson RC. Nematode parasites of vertebrates: their development and transmission 2nd ed. Wallingford: CABI Publishing; 2000. http://dx.doi.org/10.1079/9780851994215.0000
  » http://dx.doi.org/10.1079/9780851994215.0000
• Balboa L, Hinojosa A, Riquelme C, Rodríguez S, Bustos J, George-Nascimento M. Alloxenic distribution of cystacanths of two Profilicollis species in sympatric crustacean hosts in Chile. J Parasitol 2009; 95(5): 1205-1208. http://dx.doi.org/10.1645/GE-1965.1 PMid:19374470.
  » http://dx.doi.org/10.1645/GE-1965.1
• Barbosa A, Palacios MJ. Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 2009; 32(8): 1095-1115. http://dx.doi.org/10.1007/s00300-009-0640-3 PMid:32214635.
  » http://dx.doi.org/10.1007/s00300-009-0640-3
• Barreto M, Burbano ME, Proctor HC, Mironov SV, Wauthy G. Feather mites (Acariformes: Psoroptidia) from Colombia: Preliminary list with new records. Zootaxa 2012; 3516(1): 1-68. http://dx.doi.org/10.11646/zootaxa.3516.1.1
  » http://dx.doi.org/10.11646/zootaxa.3516.1.1
• Bartlett CM. New, known and unidentified species of Eulimdana (Nematoda): additional information on biologically unusual filarioids of charadriiform birds. Syst Parasitol 1992; 23(3): 209-230. http://dx.doi.org/10.1007/BF00010874
  » http://dx.doi.org/10.1007/BF00010874
• Baruš V, Sergeeva TP, Sonin MD, Ryzhikov KM. Helminths of fish-eating birds of the Palearctic Region I Prague: Springer Science+Business Media Dordrecht; 1978. http://dx.doi.org/10.1007/978-94-009-9972-5
  » http://dx.doi.org/10.1007/978-94-009-9972-5
• Beltrán-Ontiveros D, Vergara-Pineda S. Ácaros asociados a Larus occidentalis Audubon, 1839 (Charadriiformes: Laridae) en tres islas del pacífico de Baja California. Folia Entomol Mex 2016; 3: 96-102.
• Bondarenko S, Kontrimavichus V. Revision of Aploparaksis Clerc, 1903 (Cestoda: Cyclophyllidea, Aploparaksidae), with keys to the species of the genus. Biologija (Vilnius) 2018; 64(1): 1-64. http://dx.doi.org/10.6001/biologija.v64i1.3659
  » http://dx.doi.org/10.6001/biologija.v64i1.3659
• Bosch M, Torres J, Figuerola J. A helminth community in breeding Yellow-legged gulls (Larus cachinnans): pattern of association and its effect on host fitness. Can J Zool 2000; 78(5): 777-786. http://dx.doi.org/10.1139/z99-252
  » http://dx.doi.org/10.1139/z99-252
• Bridge ES. Densities and distributions of commensal feather mites (Zachvatkinia caspica) among the primaries of Caspian terns. Int J Acarol 2003; 29(4): 389-398. http://dx.doi.org/10.1080/01647950308684356
  » http://dx.doi.org/10.1080/01647950308684356
• Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227 PMid:9267395.
  » http://dx.doi.org/10.2307/3284227
• Carvalho EL, Santana RLS, Pinheiro RH, Giese EG. Eucoleus contortus (Nematoda: Capillariidae), a parasite of Cairina moschata domestica (Anseriformes: Anatidae) on Marajó Island, Pará State, in Brazilian Amazon. Rev Bras Parasitol Vet 2019; 28(4): 692-699. http://dx.doi.org/10.1590/s1984-29612019097 PMid:31800883.
  » http://dx.doi.org/10.1590/s1984-29612019097
• Clay T. A key to the species of Actornithophilus Ferris with notes and descriptions of new species. Bull Br Mus (Natural History) Entomol 1962; 2(5): 190-244.
• Clay T. Key to the species of Austromenopon Bedford (Mallophaga) parasitic on the Charadriiformes. Proc R Entomol Soc Lond 1959; 28(11-12): 157-168. http://dx.doi.org/10.1111/j.1365-3113.1959.tb00122.x
  » http://dx.doi.org/10.1111/j.1365-3113.1959.tb00122.x
• Clay T. Species of the genus Saemundssonia (Mallophaga) from the Sterninae. Am Mus Novit 1949;(1409): 1-25.
• Couve E, Vidal CF, Ruiz J. Aves de Chile, sus Islas Oceánicas y Península Antártica Punta Arenas: FS Editorial; 2016.
• Dabert J, Mironov SV. Origin and evolution of feather mites (Astigmata). Exp Appl Acarol 1999; 23(6): 437-454. http://dx.doi.org/10.1023/A:1006180705101
  » http://dx.doi.org/10.1023/A:1006180705101
• Dabert M, Coulson SJ, Gwiazdowicz DJ, Moe B, Hanssen SA, Biersma EM, et al. Differences in speciation progress in feather mites (Analgoidea) inhabiting the same host: the case of Zachvatkinia and Alloptes living on arctic and long-tailed skuas. Exp Appl Acarol 2015; 65(2): 163-179. http://dx.doi.org/10.1007/s10493-014-9856-1 PMid:25342243.
  » http://dx.doi.org/10.1007/s10493-014-9856-1
• Diaz JI, Cremonte F, Navone GT. First Record of the Acuarioid Nematode Paracuaria adunca from South America, with new morphological details and discussion of cordons. Comp Parasitol 2004; 71(2): 238-242. http://dx.doi.org/10.1654/4110
  » http://dx.doi.org/10.1654/4110
• Diaz JI, Cremonte F, Navone GT. Helminths of the kelp gull, Larus dominicanus, from the northern Patagonian coast. Parasitol Res 2011; 109(6): 1555-1562. http://dx.doi.org/10.1007/s00436-011-2396-2 PMid:21556688.
  » http://dx.doi.org/10.1007/s00436-011-2396-2
• Diaz JI, Cremonte F, Navone GT. Helminths of the Magellanic Penguin, Spheniscus magellanicus (Sphenisciformes), during the breeding season in Patagonian coast, Chubut, Argentina. Comp Parasitol 2010; 77(2): 172-177. http://dx.doi.org/10.1654/4441.1
  » http://dx.doi.org/10.1654/4441.1
• Diaz JI, Navone GT, Cremonte F. New Host and Distribution Records of Cosmocephalus obvelatus (Creplin, 1825) (Nematoda: Acuariidae), with Morphometric Comparisons. Comp Parasitol 2001; 68(2): 277-282.
• Emerson KC. Checklist of the Mallophaga of North America (North of Mexico) Part II. Sub-order Amblycera Utah: Deseret Test Center; 1972.
• Fedynich AM, Pence DB, Bergan JF. Helminth community structure and pattern in sympatric populations of double-crested and Neotropic cormorants. J Helminthol Soc Wash 1997; 64(2): 176-182.
• Fernández Í, Moraga R, Yáñez F, Mansilla M, Smith C, Campos V. Gastrointestinal helminths of wild Humboldt penguins Spheniscus humboldti (Meyen, 1834) from the south-central coast of Chile. Lat Am J Aquat Res 2019; 47(1): 206-211. http://dx.doi.org/10.3856/vol47-issue1-fulltext-25
  » http://dx.doi.org/10.3856/vol47-issue1-fulltext-25
• Galloway TD, Proctor HC, Mironov SV. Chewing lice (Insecta: Phthiraptera: Amblycera, Ischnocera) and feather mites (Acari: Astigmatina: Analgoidea, Pterolichoidea): Ectosymbionts of Grassland Birds in Canada. In: Cárcamo HA, Giberson DJ. Arthropods of Canadian Grasslands Ottawa: Biological Survey of Canada; 2014. p. 138-188. (Biodiversity and Systematics Part 1, vol. 3). http://dx.doi.org/10.3752/9780968932162.ch5
  » http://dx.doi.org/10.3752/9780968932162.ch5
• Gaud J, Atyeo WT. Feather mites of the world (Acarina, Astigmata): the supraspecific taxa Tervuren: Koninklijk museum voor Midden-Afrika; 1996.
• Gomez-Puerta LA, Cribillero NG. Contribución al conocimiento de los malófagos (Phthiraptera, Amblycera, Ischnocera) de aves peruanas. Parte 1. Rev Peru Biol 2015; 22(3): 341-346. http://dx.doi.org/10.15381/rpb.v22i3.11441
  » http://dx.doi.org/10.15381/rpb.v22i3.11441
• Gomez-Puerta LA, Naupay A. Algunos helmintos parásitos de la gaviota peruana (Larus belcheri). Rev Peru Biol 2019; 26(1): 149-156. http://dx.doi.org/10.15381/rpb.v26i1.15919
  » http://dx.doi.org/10.15381/rpb.v26i1.15919
• Gonzáles-Viera O, Luján-Vega C, Chavera–Castillo A, Cárdenas-Callirgos J, Tantaleán VM. Pathological lesions caused by Profilicollis altmani (Perry, 1942) Van Cleave, 1947 (Acanthocephala) in a Gray gull (Leucophaeus modestus) (Tschudi, 1843) from the Peruvian coast. Neotrop Helminthol 2009; 3(2): 115-120.
• González-Acuña D, Cerda F, López J, Ortega R, Mathieu C, Kinsella M. Checklist of the helminths of the kelp gull, Larus dominicanus (Aves: Laridae), with new records from Chile. Zootaxa 2009; 2297(1): 27-43. http://dx.doi.org/10.11646/zootaxa.2297.1.3
  » http://dx.doi.org/10.11646/zootaxa.2297.1.3
• González-Acuña D, Corvalán F, Barrientos C, Doussang D, Mathieu C, Nilsson L, et al. Community structure of lice (Insecta: Phthiraptera) from two sympatric gull species: Kelp gull (Larus dominicanus) and Franklin’s gull (Larus pipixcan) in Talcahuano, Chile. Neotrop Entomol 2011; 40(3): 300-304. http://dx.doi.org/10.1590/S1519-566X2011000300002 PMid:21710024.
  » http://dx.doi.org/10.1590/S1519-566X2011000300002
• González-Acuña D, Fischer C, Palma R, Moreno L, Barrientos C, Muñoz L, et al. Piojos (Phthiraptera: Insecta) de aves de la familia Laridae (Aves: Charadriiformes) en Chile. Parasitol Latinoam 2006; 61(3-4): 188-191. http://dx.doi.org/10.4067/S0717-77122006000200017
  » http://dx.doi.org/10.4067/S0717-77122006000200017
• González-Acuña D, Llanos-Soto S, Landaeta-Aqueveque C, González F, Kinsella JM, Mironov S, et al. Parasites of the Southern silvery grebe Podiceps occipitalis (Aves, Podicipedidae) in Chile. Rev Bras Parasitol Vet 2017; 26(3): 378-382. http://dx.doi.org/10.1590/s1984-29612017015 PMid:28977250.
  » http://dx.doi.org/10.1590/s1984-29612017015
• Han Y-D, Song J-H, Min G-S. Han Y-D, Song J-H, Min G-S. New record of two feather mites (Acari: Sarcoptiformes: Astigmata) from Korea. J Species Res 2016; 5(3): 324-332. http://dx.doi.org/10.12651/JSR.2016.5.3.324
  » http://dx.doi.org/10.12651/JSR.2016.5.3.324
• Hannon ER, Kinsella JM, Calhoun DM, Joseph MB, Johnson PTJ. Endohelminths in bird hosts from Northern California and an analysis of the role of life history traits on parasite richness. J Parasitol 2016; 102(2): 199-207. http://dx.doi.org/10.1645/15-867 PMid:26579621.
  » http://dx.doi.org/10.1645/15-867
• Harrison P. Seabirds, an identification guide Boston: Houghton Mifflin Co; 1983.
• Haukisalmi V. Checklist of tapeworms (Platyhelminthes, Cestoda) of vertebrates in Finland. ZooKeys 2015; 533(533): 1-61. http://dx.doi.org/10.3897/zookeys.533.6538 PMid:26668540.
  » http://dx.doi.org/10.3897/zookeys.533.6538
• Hellenthal RA, Dame N, Price RD, Smith F, Palma RL. Chewing Lice of Belgium [online]. 2004 [cited 2020 Apr 10]. Available from: http://bch-cbd.naturalsciences.be/belgium/biodiversity/faunaflorahabitats/belchewinglice.pdf
  » http://bch-cbd.naturalsciences.be/belgium/biodiversity/faunaflorahabitats/belchewinglice.pdf
• Hoberg EP. A redescription of Aporchis continuus McCauley and Pratt 1960 (Trematoda: Echinostomatidae) with new host and geographic records. Can J Zool 1981; 59(1): 19-21. http://dx.doi.org/10.1139/z81-004
  » http://dx.doi.org/10.1139/z81-004
• Hoberg EP. Phylogenetic relationships among genera of the Tetrabothriidae (Eucestoda). J Parasitol 1989; 75(4): 617-626. http://dx.doi.org/10.2307/3282914 PMid:2760773.
  » http://dx.doi.org/10.2307/3282914
• Iannacone J, Alvariño L, Bolognesi B. Quantitative aspects of metazoan parasites of mole crab Emerita analoga (Stimpson) (Decapoda, Hippidae) from Chorrillos, Lima, Peru. Neotrop Helminthol 2007; 1(2): 59-67.
• Johnson KP, Shreve SM, Smith VS. Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biol 2012; 10(1): 52. http://dx.doi.org/10.1186/1741-7007-10-52 PMid:22717002.
  » http://dx.doi.org/10.1186/1741-7007-10-52
• Kavetska KM, Pilarczyk B, Królaczyk K. Stomach nematodes of wild ducks (subfamily Anatinae) wintering in the North-Western Poland. Bull Vet Inst Pulawy 2012; 56(1): 27-31. http://dx.doi.org/10.2478/v10213-012-0005-5
  » http://dx.doi.org/10.2478/v10213-012-0005-5
• Khalil LF, Jones A, Bray RA. Keys to the cestode parasites of vertebrates Wallingford: CAB International; 1994.
• Kinsella JM, Forrester DJ. Tetrameridosis. In: Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds Iowa: Wiley-Blackwell; 2008. p. 376-383.
• Knee W, Galloway TD. New host and locality records for endoparasitic nasal mites (Acari: Rhinonyssidae, Turbinoptidae, and Ereynetidae) infesting birds in Manitoba, Canada. Can Entomol 2016; 149(1): 89-103. http://dx.doi.org/10.4039/tce.2016.47
  » http://dx.doi.org/10.4039/tce.2016.47
• Krantz GW, Walter DE. A manual of acarology Lubbock: Texas Tech University Press; 2009.
• Kuklin VV. The peculiarities of the helminth fauna of herring gulls of the synanthropic Murmansk population. Dokl Biol Sci 2011; 440(1): 309-312. http://dx.doi.org/10.1134/S0012496611050115 PMid:22134819.
  » http://dx.doi.org/10.1134/S0012496611050115
• Marin M, Couve E. La gaviota de Franklin, Larus pipixcan Wagler (Laridae), al sur de latitud 41ºS, con nuevos registros de distribución. Anal Inst Patag Ser Cienc Nat 2001; 29: 161-163.
• McCauley JE, Pratt I. Aporchis continuus n. sp. (Trematoda: echinostomatidae). J Parasitol 1960; 46(5): 642-644. http://dx.doi.org/10.2307/3274952 PMid:13773781.
  » http://dx.doi.org/10.2307/3274952
• Mironov SV, Stefan LM. Redescription of the feather mite species, Zachvatkinia puffini (Buchholz, 1869) (Acariformes: Avenzoariidae), from its type host, the grey petrel Procellaria cinerea (Procellariiformes: Procellariidae). Acarina (Mosc) 2013; 21(1): 27-37.
• Mironov SV. A brief review of the feather mites of the genus Zachvatkinia in the USSR (Analgoidea, Avenzoariidae). Parazitologicheskii Sbornik Zoologicheskii Institut AN SSSR 1989; 36: 91-115.
• Mollhagen TR. A study of the systematics and hosts of the parasitic nematode genus Tetrameres (Habronematoidea: Tetrameridae) [PhD thesis]. Lubbock: Texas Tech University; 1976.
• Monteiro CM, Amato JFR, Amato SB. Helminth parasitism in the Neotropical cormorant, Phalacrocorax brasilianus, in Southern Brazil: effect of host size, weight, sex, and maturity state. Parasitol Res 2011; 109(3): 849-855. http://dx.doi.org/10.1007/s00436-011-2311-x PMid:21431903.
  » http://dx.doi.org/10.1007/s00436-011-2311-x
• Mutafchiev Y, Halajian A, Georgiev BB. Two new nematode species of the genus Cosmocephalus Molin, 1858 (Spirurida: Acuariidae), with an amended generic diagnosis and an identification key to Cosmocephalus spp. Zootaxa 2010; 2349(1): 1-20. http://dx.doi.org/10.11646/zootaxa.2349.1.1
  » http://dx.doi.org/10.11646/zootaxa.2349.1.1
• Mutafchiev Y, Mariaux J, Georgiev BB. Description of Proyseria petterae n. sp., with an amended generic diagnosis and a review of the species of Proyseria Petter, 1959 and Stegophorus Wehr, 1934 (Nematoda: acuariidae). Syst Parasitol 2014; 89(1): 3-14. http://dx.doi.org/10.1007/s11230-014-9507-2 PMid:25079811.
  » http://dx.doi.org/10.1007/s11230-014-9507-2
• Muzaffar SB. Helminths of murres (Alcidae: Uria spp.): Markers of ecological change in the marine environment. J Wildl Dis 2009; 45(3): 672-683. http://dx.doi.org/10.7589/0090-3558-45.3.672 PMid:19617477.
  » http://dx.doi.org/10.7589/0090-3558-45.3.672
• Negm MW, Nasser MG-D, Alatawi FJ, Ahmad AMA, Shobrak M. Feather mites of the genus Zachvatkinia Dubinin, 1949 (Astigmata: Analgoidea: Avenzoariidae) from Saudi Arabia: a new species and two new records. Zootaxa 2013; 3710(1): 61-71. http://dx.doi.org/10.11646/zootaxa.3710.1.4 PMid:26106674.
  » http://dx.doi.org/10.11646/zootaxa.3710.1.4
• Oyarzún-Ruiz P, González-Acuña D. Colecta, preparación e identificación de parásitos. Parasitol Latinoam 2020; 69(1): 12-29.
• Oyarzún-Ruiz P, Muñoz-Alvarado P, Raffo E. Helminths of Milvago chimango temucoensis (Aves: Falconiformes) from Los Ríos region, Chile: new records for Neotropical raptors. Helminthol 2016; 53(4): 336-353. http://dx.doi.org/10.1515/helmin-2016-0037
  » http://dx.doi.org/10.1515/helmin-2016-0037
• Palma R. Slide-mounting of lice: a detailed description of the Canada balsam technique. N Z Entomol 1978; 6(4): 432-436. http://dx.doi.org/10.1080/00779962.1978.9722313
  » http://dx.doi.org/10.1080/00779962.1978.9722313
• Palma RL. A new synonymy and new records of Quadraceps (Insecta: Phthiraptera: Philopteridae) from the Galápagos Islands. N Z J Zool 1995; 22(2): 217-222. http://dx.doi.org/10.1080/03014223.1995.9518037
  » http://dx.doi.org/10.1080/03014223.1995.9518037
• Parejo SH, Martínez-Carrasco C, Diaz JI, Chitimia L, Ortiz J, Mayo E, et al. Parasitic fauna of a yellow-legged gull colony in the island of Escombreras (South-eastern Mediterranean) in close proximity to a landfill site: potential effects on cohabiting species. Acta Parasitol 2015; 60(2): 290-297. http://dx.doi.org/10.1515/ap-2015-0041 PMid:26203998.
  » http://dx.doi.org/10.1515/ap-2015-0041
• Pilgrim R, Palma R. A list of the Chewing Lice (Insecta: Mallophaga) from birds in New Zealand. Notornis 1982; 29: 1-32.
• Price RD, Clay T. A Review of the Genus Austromenopon (Mallophaga: Menoponidae) from the Procellariiformes. Ann Entomol Soc Am 1972; 65(2): 487-504. http://dx.doi.org/10.1093/aesa/65.2.487
  » http://dx.doi.org/10.1093/aesa/65.2.487
• Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH. The chewing lice: world checklist and biological overview Springfield: Illinois Natural History Survey Special Publication; 2003.
• Radwan NA. Aporchis massiliensis (Digenea: Echinostomatidae) from Larus leucophthalmus (Aves: Laridae) from the Red Sea, Egypt, with Scanning Electron Microscopy of the Tegumental Surface. Glob Vet 2014; 12(6): 760-767. http://dx.doi.org/10.5829/idosi.gv.2014.12.06.83256
  » http://dx.doi.org/10.5829/idosi.gv.2014.12.06.83256
• Retamal MA. Catálogo ilustrado de los Crustáceos Decápodos de Chile. Gayana Zool 1981; 44: 1-110.
• Riquelme C, George-Nascimento M, Balboa L. Morfometría y fecundidad de Profilicollis bullocki Mateo, Córdova & Guzmán 1982 (Acanthocephala: Polymorphidae) en especies simpátricas de aves costeras de Chile. Rev Chil Hist Nat 2006; 79(4): 465-474. http://dx.doi.org/10.4067/S0716-078X2006000400005
  » http://dx.doi.org/10.4067/S0716-078X2006000400005
• Roca V, Lafuente M, Carbonell E. Estudio de los ectoparásitos y helmintos de la gaviota de audouin (Larus audouinii) en las Islas Chafarinas. Ecología (Madr) 2001; 15: 233-241.
• Rocka A. Cestodes of the genus Tetrabothrius (Tetrabothridea: Tetrabothriidae) from Antarctic flying seabirds. Ann Parasitol 2019; 65(4): 423-426. http://dx.doi.org/10.17420/ap6504.230 PMid:32191991.
  » http://dx.doi.org/10.17420/ap6504.230
• Rodrigues de Olivera H, Vicente JJ. Nova espécie do gënero Cosmocephalus Molin, 1858 (Nematoda, Spiruroidea). Rev Bras Biol 1963; 23: 389-392.
• Rodríguez SM, D’Elía G, Valdivia N. The phylogeny and life cycle of two species of Profilicollis (Acanthocephala: Polymorphidae) in marine hosts off the Pacific coast of Chile. J Helminthol 2017; 91(5): 589-596. http://dx.doi.org/10.1017/S0022149X16000638 PMid:27667136.
  » http://dx.doi.org/10.1017/S0022149X16000638
• Sagerup K, Savinov V, Savinova T, Kuklin V, Muir DC, Gabrielsen GW. Persistent organic pollutants, heavy metals and parasites in the glaucous gull (Larus hyperboreus) on Spitsbergen. Environ Pollut 2009; 157(8-9): 2282-2290. http://dx.doi.org/10.1016/j.envpol.2009.03.031 PMid:19364623.
  » http://dx.doi.org/10.1016/j.envpol.2009.03.031
• Sanmartín ML, Cordeiro JA, Álvarez MF, Leiro J. Helminth fauna of the yellow-legged gull Larus cachinnans in Galicia, north-west Spain. J Helminthol 2005; 79(4): 361-371. http://dx.doi.org/10.1079/JOH2005309 PMid:16336721.
  » http://dx.doi.org/10.1079/JOH2005309
• Santoro M, Mattiucci S, Kinsella JM, Aznar FJ, Giordano D, Castagna F, et al. Helminth Community Structure of the Mediterranean Gull (Ichthyaetus melanocephalus) in Southern Italy. J Parasitol 2011; 97(2): 364-366. http://dx.doi.org/10.1645/GE-2602.1 PMid:21506790.
  » http://dx.doi.org/10.1645/GE-2602.1
• Siepel H, Cremers H, Vierbergen B. Provisional checklist of the astigmatic mites of the Netherlands (Acari: Oribatida: Astigmatina). Nederl Faun Med 2016; 47: 49-88.
• Tantaleán M, Sánchez L, Gómez L, Huiza A. Acantocéfalos del Perú. Rev Peru Biol 2005; 12(1): 83-92. http://dx.doi.org/10.15381/rpb.v12i1.2361
  » http://dx.doi.org/10.15381/rpb.v12i1.2361
• Threlfall W, Usnm M, Coll H. Endoparasites of the Double-crested Cormorant (Phalacrocorax auritus) in Florida. Proc Helminthol Soc Wash 1982; 49(1): 103-108.
• Threlfall W. The helminth parasites of three species of gulls in Newfoundland. Can J Zool 1968; 46(5): 827-830. http://dx.doi.org/10.1139/z68-117 PMid:5749648.
  » http://dx.doi.org/10.1139/z68-117
• Timmermann G. LXIV - The species of the genus Quadraceps (Mallophaga) from the Larinae, with some remarks on the systematics and the phylogeny of the gulls. Part II. Ann Mag Nat Hist 1952; 5(54): 595-600. http://dx.doi.org/10.1080/00222935208654329
  » http://dx.doi.org/10.1080/00222935208654329
• Torres P, Contreras A, Cubillos V, Gesche W, Montefusco A, Rebolledo C, et al. Parasitismo en peces, aves piscívoras y comunidades humanas ribereñas de los lagos Yelcho y Tagua Tagua, X región de Chile. Arch Med Vet 1992; 24(1): 76-92.
• Torres P, Ruíz E, Gesche W, Montefusco A. Gastrointestinal helminths of fish-eating birds from Chiloe Island, Chile. J Wildl Dis 1991; 27(1): 178-179. http://dx.doi.org/10.7589/0090-3558-27.1.178 PMid:2023322.
  » http://dx.doi.org/10.7589/0090-3558-27.1.178
• Torres P, Schlatter R, Montefusco A, Gesche W, Ruiz E, Contreras A. Helminths parasites of piscivorous birds from lakes in the South of Chile. Mem Inst Oswaldo Cruz 1993; 88(2): 341-343. http://dx.doi.org/10.1590/S0074-02761993000200028 PMid:8107596.
  » http://dx.doi.org/10.1590/S0074-02761993000200028
• Uchida A, Uchida K, Kawakami Y, Nagatomo M, Minghao S. A helminthological survey of parasites in the waterfowl of Kanagawa Prefecture, Japan. Nippon Juishikai Zasshi 2005; 58(2): 127-131. http://dx.doi.org/10.12935/jvma1951.58.127
  » http://dx.doi.org/10.12935/jvma1951.58.127
• Vas Z, Rekasi J, Rozsa L. A checklist of lice of Hungary (Insecta: Phthiraptera). Annls Hist-nat Mus Natn Hung 2012; 104: 5-109.
• Ward RA. Biting lice of the genus Saemundssonia (Mallophaga: Philopteridae) occuring on terns. Proc U S Natl Mus 1955; 105(3353): 83-100. http://dx.doi.org/10.5479/si.00963801.105-3353.83
  » http://dx.doi.org/10.5479/si.00963801.105-3353.83
• Wong PL, Anderson RC. The transmission and development of Cosmocephalus obvelatus (Nematoda: Acuarioidea) of gulls (Laridae). Can J Zool 1982a; 60(6): 1426-1440. http://dx.doi.org/10.1139/z82-192
  » http://dx.doi.org/10.1139/z82-192
• Wong PL, Anderson RC. Redescription of Paracuaria adunca (Creplin, 1846) (Nematoda: Acuarioidea) from Larus delawarensis Ord (Laridae). Can J Zool 1982b; 60(2): 175-179. http://dx.doi.org/10.1139/z82-023
  » http://dx.doi.org/10.1139/z82-023
• Yamagishi A, Yao I, Johnson KP, Yoshizawa K. Comparisons of host specificity in feather louse genera (Insecta: Phthiraptera: Philopteridae) parasitizing gulls (Aves: Laridae: Larus). Zool Sci 2014; 31(6): 383-389. http://dx.doi.org/10.2108/zs130263 PMid:24882099.
  » http://dx.doi.org/10.2108/zs130263
• Yamaguti S. Systema helminthum New York: Interscience Publishers; 1958. (The digenetic trematodes of vertebrates – Part 1; vol. 1).
• Yamaguti S. Systema helminthum New York: Interscience Publishers; 1959. (The cestodes of vertebrates; vol. 2).
• Yamaguti S. Systema helminthum New York: Interscience Publishers; 1961. (The nematodes of vertebrates - Part 1; vol. 3).
• Yamaguti S. Systema helminthum New York: Interscience Publishers; 1963. (Acanthocephala; vol. 5).
• Yoshino T, Uemura J, Endoh D, Kaneko M, Osa Y, Asakawa M. Parasitic nematodes of Anseriform birds in Hokkaido, Japan. Helminthologia 2009; 46(2): 117-122. http://dx.doi.org/10.2478/s11687-009-0023-x
  » http://dx.doi.org/10.2478/s11687-009-0023-x

Publication Dates

• Publication in this collection
  04 Dec 2020
• Date of issue
  2020

History

• Received
  13 July 2020
• Accepted
  03 Sept 2020