Parasitological survey of coastal birds from the Magellanic coast, Southwestern Atlantic Ocean

Abstract

Ecto and endoparasites of four species of coastal birds, Haematopus ater, Larus dominicanus, Leucophaeus scoresbii (Charadriiformes), and Lophonetta specularioides (Anseriformes), are reported from Puerto Deseado on the Patagonian coast, Argentina. Only H. ater was infested with lice (Phthiraptera), belonging to 2 species (Ischnocera, Amblycera). A total of 19 helminth species were found parasitizing the coastal birds studied: 4 cestodes (1 Tetrabothriidae, 3 Cyclophyllidea); 11 trematodes (2 Gymnophallidae, 3 Microphallidae, 2 Notocotylidae, 1 Philophthalmidae, 2 Renicolidae, 1 Schistosomatidae); 3 nematodes (1 Anisakidae, 2 Acuariidae); and 1 acanthocephalan (Polymorphidae). Although some isolated records have been previously reported for these birds, the present work provides a parasitofauna study for H. ater, L. scoresbii, and L. specularioides for the first time. Endoparasites reflected the feeding habits of the birds; the parasite assemblage of L. dominicanus was the richest, indicating their wide prey spectrum and the diversity of the habitats frequented. A great species richness of trematodes, whose life cycles are partially known, suggests that L. specularioides feeds upon crustaceans and small bivalves. The blackish oystercatcher H. ater preys upon the limpet Nacella magellanica which hosts two larval trematodes corresponding to the adults found parasitizing it.

Key words
lice; helminthes; Kelp gull; Dolphin gull; Crested duck; Blackish oystercatcher

INTRODUCTION

The shoreline of the Argentine Patagonian coast is an important feeding and breeding area for several coastal birds (Favero & Silva Rodríguez 2005) where 17 species, including penguins, shags, gulls, terns, ducks, oystercatchers, skuas, and petrels, breed (Yorio et al. 2005) and prey over the abundant diversity of invertebrates and vertebrate inhabiting the marine littoral and sublittoral zones (Diaz et al. 2011). In the marine ecosystems, the helminths assemblage of coastal birds (definitive hosts) reflects the presence of fish and invertebrates that are involved in their life cycle, which act as intermediate hosts and are mostly transmitted through trophic interactions, making parasites natural markers of changes in biodiversity (Marcogliese 2005).

In contrast with birds in general, studies concerning parasitic lice on aquatic birds in South America are scarce. In Argentina, Daciuk et al. (1981) presented some records of ectoparasites in birds from Península Valdés, providing the first record for lice in the Kelp Gull Larus dominicanus Lichtenstein (Laridae). Recently, Leonardi & Quintana (2017) and Leonardi et al. (2018) reported parasitological data for lice from the Imperial Shag Leucocarbo atriceps (King) (Phalacrocoracidae). However, there is no information available for the majority of marine and shorebird lice.

On the other hand, the birds´ helminth communities and the factors which structured them are still poorly known in South America. One of the most studied host-parasite-environment models in the Patagonian coast is that of L. dominicanus, one of the most abundant coastal bird species found throughout the Argentinean coast (Bertellotti & Yorio 1999, Yorio et al. 2005) which is characterized by a great parasitic richness because of its generalist and opportunistic habits (Diaz et al. 2011). Thirteen (13) adult helminths taxa were recognized parasitizing the L. dominicanus population from Península Valdés, including cestodes, trematodes, nematodes, and acanthocephalans (Cremonte 2001, 2004, Diaz & Cremonte 2004, 2010, Diaz et al. 2001, 2004, 2011, 2012). Besides, there are several isolated reports of parasites in different coastal birds, like nematodes from the Steamer Duck, Tachyeres leucocephalus Humphrey & Thompson, the Crested Duck, Lophonetta specularioides (King), the Black-necked Swan, Cygnus melancoryphus (Molina) (Anatidae) (Agüero & Diaz 2013, Agüero et al. 2015) and from the Imperial Shag P. atriceps and the Red-legged Shag Phalacrocorax gaimardii (Lesson & Garnot) (Phalacrocoracidae) (Garbin et al. 2008, 2014). Also, trematodes like Bartolius pierrei Cremonte, 2001 were recorded in the Red Knot Calidris canutus rufa Linnaeus (Cremonte 2004), and Maritrema formicae Diaz, Gilardoni & Cremonte 2012, Levinseniella cruzi Travassos 1921, and Odhneria odhneri Travassos, 1921 parasitizing the Baird’s Sandpiper Calidris bairdii Coues (Scolopacidae) (Capasso et al. 2019). Odhneria odhneri was also recorded in the Two-banded Plover Charadrius falklandicus Latham (Scolopacidae) (Capasso et al. 2017). Finally, two species of Acanthocephala, Arhythmorhynchus comptus Van Cleave & Rausch, 1950 and immature Profilicollis sp., were reported in C. bairdii and the White-rumped Sandpiper Calidris fuscicollis (Vieillot) (Scolopacidae) (Capasso & Diaz 2016).

Knowledge on richness and diversity of bird parasites in littoral areas may provide important information about interactions, trophic webs, and compound community structure, mainly in those regions where the coastal birds abundance (mostly gulls) is increasing as a result of human activities such as fishing (Galaktionov & Skirnisson 2000, Diaz et al. 2011). Therefore, baseline information on the parasitofauna is very important to understand possible modifications in a changing world. The aim of the present work is to report both ecto and endoparasites for some of the most abundant coastal bird species from the Patagonian coast.

MATERIALS AND METHODS

Ten coastal birds, 2 Blackish Oystercatcher Haematopus ater Vieillot & Oudart (Charadriidae), 4 Kelp Gulls Larus dominicanus, 2 Dolphin Gulls Leucophaeus scoresbii Traill (Laridae), and 2 Crested Duck Lophonetta specularioides (Anatidae) were captured and collected from the rocky littoral near the estuary of the Deseado River, in Puerto Deseado, Santa Cruz Province, Argentina (47° 45’ S, 65° 55’ W) during May 2016. Birds were captured with an airsoft gun under permits provided by the Wildlife Secretary of the Santa Cruz province (Resolution Number 861/08); then they were euthanized with carbon dioxide and inspected for ectoparasites by observing all the surface of the body underneath the feathers. Lice were collected using forceps and fixed in 96% ethanol. Finally, they were dissected and searched for endoparasites under a stereomicroscope. The gastrointestinal tract was separated into esophagus, stomach, and intestine; this last organ was divided into three equal sections. The body cavity, liver, pancreas, biliary vesicle, gall bladder, gonads, lungs, heart, bursa of Fabricius, cloaca, and kidneys were also examined for parasites. Helminths recovered from each section were counted, fixed in 5% hot formalin, and preserved in 70% ethanol. Cestodes were stained in Harris hematoxylin, and digeneans with Semichon’s carmine or Gomori´s trichrome, dehydrated in a graded ethanol series, cleared in methyl salicylate, and mounted in Canada balsam. Nematodes and acanthocephalans were cleared in lactophenol or in 25% glycerine-ethanol. All species were studied using a light microscope and identified at the most precise taxonomic level possible (Odhner 1910, Price 1929, Wright 1956, Clay 1962, 1981, Johri 1963, Szidat 1964, Graefe 1968, Odening 1982, Bona 1994, Czsplinski & Vaucher 1994, Hoberg 1994, Khalil 1994, Navone et al. 1998, Diaz et al. 2004, Nikolov et al. 2005, Diaz & Cremonte 2010, Diaz et al. 2011, Fernandes et al. 2015, Diaz et al. 2020, Gilardoni et al. 2020). The number of parasitized hosts and the intensity of infection (number of parasites divided by number of parasitized hosts) were determined. Specimens were deposited at the Parasitological Collection of the Instituto de Biología de Organismos Marinos (CNP-Par), Puerto Madryn, Argentina.

RESULTS

A total of 21 parasite taxa, 2 ectoparasites (lice) and 19 endoparasites (helminthes) were found parasitizing the 4 coastal bird species studied (Table I). Only Haematopus ater was infested with ectoparasites, finding 2 Phthiraptera species, Quadraceps ridqwayi Kellogg, 1906 (Ischnocera, Philopteridae) and Actornithophilus grandiceps Piaget, 1880 (Amblycera, Menoponidae). Among the helminthes, 4 Cestoda, 11 Digenea, 3 Nematoda, and 1 Acanthocephala were recorded.

Table I
Ecto and endo parasites species recorded in the studied coastal birds from Puerto Deseado, Patagonian coast, Argentina. Mean intensity of infection is given followed by the range in parenthesis.

Coastal bird host	Parasite species	Infection site	Nº parasitized host		Intensity of infection	Deposited specimens
Haematopus ater (n = 2)	Phthiraptera
	Ischnocera
	Quadraceps ridgwayi Amblycera	Feathers	2		3 (1-4)	CNP-Par 179
	Actornithophilus grandiceps	Feathers	1		4	CNP-Par 180
	CestodaProgynotaenia sp. Digenea Gymnophalloides nacellae Gymnophallus australis Paramonostomum sp.	Intestine (first section) Intestine, caeca, cloaca Intestine, caeca, cloaca Intestine, caeca, cloaca	1 1 1 2		7 339 100 505 (11-1000)	CNP-Par 154 CNP-Par 171 CNP-Par 172 CNP-Par 168
Larus dominicanus (n = 4)	CestodaTetrabothrius sp. Dilepididae gen. et sp. Digenea Gymnophallus australis Maritrema madrynense Parorchis sp. Renicola sp. 1 Schistosomatidae gen.et sp. Nematoda Anisakidae gen. et sp. (larvae) Paracuaria adunca Cosmocephallus obvelatus Acantocephala Profilicollis chasmagnathi	Intestine (first and second section) Intestine (first and second section) Intestine (third section) Intestine (third section) Cloaca Kidney Intestine mesenteric vessels Proventriculus, intestine Gizzard Esophagus Intestine (third section)	2 2 2 1 1 2 1 2 1 2 1		2* 4* 27 (4-50) 5 8 3 (1-6) 17 1 (1-2) 12 5 (2-9) 2	CNP-Par 151 CNP-Par 181 CNP-Par 166 CNP-Par 182 CNP-Par 183 CNP-Par 184 CNP-Par 185 CNP-Par 186 CNP-Par 187 CNP-Par 188 CNP-Par 189
Leucophaeus scoresbii (n = 2)	Cestoda Dilepididae gen. et sp. Digenea Gymnophallus australis Parorchis sp.	Intestine (first and second section) Intestine (third section) Cloaca	2 1 1	4 (1-7) 30 1 (1-1)		CNP-Par 152 CNP-Par 190 CNP-Par 191
Lophonetta specularoides (n = 2)	Cestoda Hymenolepididae gen. et sp. Digenea Levinseniella sp. Odhneria odhneri Notocotylus primulus Renicola sp. 2	Intestine (first section) Intestinal caeca Intestinal caeca Intestinal caeca Kidney	1 2 1 2 1	3 118 (86-150) 20 10 (1-20) 16		CNP-Par 153 CNP-Par 170 CNP-Par 169 CNP-Par 173 CNP-Par 192

• * Total number of cestodes from one kelp gull cannot be determined because the scolices were not found.

A taxonomic summary is exposed in Table I hereas remarks of each one are presented below.

ECTOPARASITES

Phthiraptera

Ischnocera Kellog, 1896

Philopteridae Eichler, 1959

Quadraceps Clay & Meinertzhagen, 1939

Quadraceps ridgwayi Kellogg, 1906 (Figure 1)

The morphological diagnosis agrees with the species recorded by Clay (1981). The genus Quadraceps is composed of more than 100 species parasitizing mainly Charadriiformes (Palma 1995); among them Q. ridgwayi was described from the American Oystercatcher Haematopus palliatus galapagensis Ridgway from Galapagos Island. In her study about lice from Oystercatcher, Clay (1981) reported H. ater for the first time as host of Q. ridgwayi, from samples deposited in the Natural History Museum. However, the author of this record was not mentioned in the study. In the NHM Collection, there are two slides from H. ater collected by A.J. Baker in “Punta Clara, Chubut”. However, this does not correspond to a real geographic location, therefore it is not clear where these samples were really collected.

Figures 1-10.
Ecto and endoparasites of coastal birds from Puerto Deseado, Patagonian coast, Argentina. 1) Quadraceps ridgwayi (Ischnocera) from Haematopus ater, 2) Actornithophilus grandiceps (Ambycera) from H. ater, 3) Progynotaenia sp. (Cestoda) from H. ater, in toto 4) Dilepididae gen. et sp. (Cestoda) from Larus dominicanus and Leucophaeus scoresbii, in toto 5) Hymenolepididae gen. et sp. (Cestoda) from Lophonetta specularoides, in toto, 6) Levinseniella sp. (Digenea) from L. specularoides, in toto, 7) Odhneria odhneri (Digenea) from L. specularoides, in toto, 8) Paramonostomum sp. (Digenea) from H. ater, in toto, 9) Renicola sp. (Digenea) from L. dominucanus, in toto, 10) Schistosomatidae gen. et sp. (Digenea) from L. dominucanus, in toto. Scales: 1-2 (500 µm) 3-8 (100 µm) 9 (200 µm) 10 (1000 µm).

Amblycera Kellogg, 1896

Menoponidae Nitzsch, 1818

Actornithophilus Ferris, 1916

Actornithophilus grandiceps Piaget, 1880 (Figure 2)

The morphological diagnosis agrees with the species recorded by Clay (1962). The genus Actornithophilus was erected by Ferris (1916), and currently, it includes 36 species parasitizing Charadriiformes (Clay 1962). In her key to the species of Actornithophilus, Clay (1962) analyzed samples from H. ater from different locations along the South American coast, but there is not information from continental Argentina. Actornithophilus grandiceps was described by Piaget (1880) from the Eurasian oystercatcher, Haematopus ostralegus Linnaeus. Later, this species was reported in 7 out of the 12 oystercatcher species (Price et al. 2003). According to Price et al. (2003), H. ater is infested by A. grandiceps, but there are no bibliographic references for this record. As far as we know, only 2 slides of this species from Chile are deposited at the Price Institute of Parasite Research (PIPeR, Salt Lake City).

ENDOPARASITES

Cestoda

Tetrabothriidea Baer 1954; Tetrabothriidae Linton, 1891

Tetrabothrius Rudolphi, 1819

Tetrabothrius sp.

The morphological diagnosis agrees with species of the genus Tethrabothrius (Hoberg 1994). This genus is widely distributed among marine mammals and birds, including more than 40 species parasitizing seabirds (Hoberg 1994, Schmidt 1986). There are two previous records for the genus from birds on the Patagonian coast. One of these is Tetrabothrius cylindraceus (Rudolphi) reported in L. dominicanus, the other one is Tetrabothrius lutzi Parona, parasitizing the Magellanic Penguin, Spheniscus magellanicus Foster (Spheniscidae) (Diaz et al. 2010, 2011). In this study, specimens of Tetrabothrius were found in L. dominicanus, and because of the lack of mature proglottids, we could not determine them at species level.

Cyclophyllidea van Benedenin Braun, 1900

Progynotaeniidae Fuhmann, 1936; Progynotaeniinae Furhmann, 1936

Progynotaenia Fuhrman, 1909

Progynotaenia sp. (Figure 3)

The morphological diagnosis agrees with species of the genus Progynotaenia (Johri 1963, Khalil 1994, Nikolov et al. 2005). The family Progynotaeniidae mostly parasites charadriiform birds and has been reported in different regions of the world (Johri 1963). In America, a single undescribed species of the genus Proterogynotaenia was reported in the American Oystercatcher Haematopus palliatus Temminck in Chile (Mariaux et al. 2017). There are disagreements about the location of many species into this genus or into Paraprogynotaenia (Nikolov et al. 2005). Following Khalil (1994), specimens collected in the present study in H. ater belong to Progynotaenia, being the first record of the family Progynotaeniidae in Argentina.

Hymenolepididae Ariola, 1899

Hymenolepididae gen. et sp. indet. (Figure 4)

The morphological diagnosis agrees with species of the family Hymenolepididae (Czsplinski & Vaucher 1994). Among cestodes, Hymenolepididae is the family that includes the highest number of species. Few species from this family were reported in gulls from Argentina. Szidat (1964) reported Hymenolepis semiductilis Szidat, 1964 parasitizing L. dominicanus and Larus maculipennis (Lichtenstein) (Laridae) from the Paraná River, Santa Fé province, and Labriola & Suriano (2001) registered Wardium paucispinosum (Sandground 1928) and Microsomacantus shetlandicus Szidat, 1964 in some gulls from the Mar del Plata coast, Buenos Aires province. The specimens found in L. specularioides are small and delicate, so they are easily fragmented, showing great variability in many of the morphological characteristics. The present finding represents the first record of this family in L. specularioides from Argentina.

Dilepididae Raillet and Henry, 1909

Dilepididae gen. et sp. indet. (Figure 5)

The morphological diagnosis agrees with species of the family Dilepididae (Bona 1994). Dilepidid cestodes are very common birds parasites including more than 100 genera that exhibit host specificity at the order level of the host (Schmidt 1986, Bona 1994). The specimens here found in L. scoresbii and L. dominicanus resembles Anomotaenia dominicana (Railliet & Henry 1912), which were recorded in L. dominicanus from Península Valdés (Diaz et al. 2011). The specimens found in the present study constitute the first record of this family in L. scoresbii.

Digenea

Gymnophallidae Odhner, 1905; Gymnophallinae Odhner, 1905

Gymnophallus australis Szidat, 1962

The morphological diagnosis agrees with the species recorded in L. dominicanus from northern Patagonia, Argentina (Diaz et al. 2011). The species was originally described as Gymnophallus australis (metacercariae parasitizing the mussel Mytilus edulis Linnaeus (Mytilidae) and then reassigned by the same author to the genus Parvatrema (Szidat 1965). Cremonte et al. (2008) re-described the species from cultured metacercariae and adults obtained in the laboratory from intertidal mussels and reassigned again to the genus Gymnophallus.

Gymnophalloides nacellae Cremonte, Pina, Gilardoni, Rodrigues, Chai & Ituarte, 2013

The study of the specimens collected in this study allowed the description of the adult form of Gymnophalloides nacellae (Gilardoni et al. 2020). The metacercaria was described by Cremonte et al. (2013) from specimens parasitizing the limpet Nacella magellanica (Gmelin) (Nacellidae) which acts as a second intermediate host. The sporocysts with cercariae were described by Gilardoni et al. (2020) from specimens parasitizing the bivalve Gaimardia trapesina (Lamarck) (Gaimardiidae). Due to the restricted geographic distribution of their first intermediate host, G. trapesina (Gilardoni et al. 2020), the geographic distribution is limited to the Magellanic region on the Patagonian coast due to the restricted geographic distribution of their first intermediate host, G. trapesina (Gilardoni et al. 2020).

Microphallidae Travassos, 1920

Levinseniella sp. Stiles & Hassall, 1901 (Figure 6)

The morphological diagnosis agrees with species of the genus Levinseniella (Szidat 1964). Several bird species were recorded as host of this trematode in different areas of Argentina (Szidat 1964, Lunaschi & Drago 2007). In Patagonia, L. cruzi was reported in L. dominicanus and L. maculipennis from lakes of the Río Negro and Neuquén provinces (Szidat 1964). In marine areas, this species was recorded in C. bairdii from the Chubut province (Capasso et al. 2019). The present finding represents the southernmost record of this genus. It is necessary to study the specimens to know whether they belong to an already described species or an undescribed one.

Maritrema madrynense Diaz & Cremonte, 2010

The morphological diagnosis agrees with the species described in L. dominicanus from northern Patagonia, Argentina (Diaz & Cremonte 2010). Other four species of this genus had been previously reported in Argentinean waters: Maritrema formicae Diaz, Gilardoni & Cremonte, 2012 from L. dominicanus and C. bairdii; Maritrema bonaerensis Etchegoin & Martorelli 1997 from L. dominicanus, L. atlanticus, and L. maculipennis (Etchegoin & Martorelli 1997, La Sala et al. 2009, Diaz et al. 2012); Maritrema orensensis Cremonte & Martorelli 1998 from L. dominicanus and L. atlanticus (Cremonte & Martorelli 1998, La Sala et al. 2009); and Maritrema pichi Capasso, Diaz and D’Amico, 2019 parasitizing C. bairdii from Chubut Province (Capasso et al. 2019). The pulmonate limpet Siphonaria lessonii Blainville (Siphonariidae) acts as the first and second intermediate host of M. madrynense, harboring sporocysts with cercariae and/or metacercariae (Alda & Martorelli 2009, Gilardoni et al. 2011); besides, the crab Cyrtograpsus altimanus Rathbun (Varunidae) and the isopod Idotea baltica (Pallas) (Idoteidae) were recorded as the second intermediate hosts (Diaz & Cremonte 2010, Bagnato et al. 2015).

Odhneria Travassos, 1921

Odhneria odhneri Travassos, 1921 (Figure 7)

The morphological diagnosis agrees with Odhneria odhneri Travassos, 1921, which is the only species of the genus and it was widely recorded in the western hemisphere parasitizing birds belonging to several families: Anatidae, Ardeidae, Charadriidae, Laridae, Scolopacidae, and Phalacrocoracidae (Fernandes et al. 2015). In Argentina, it was reported from Calidris fuscicollis, C. bairdii (Scolopacidae), Charadrius falklandicus (Charadriidae), Phalacrocorax brasilianus (Phalacrocoracidae) and L. dominicanus on the Patagonian coast (Cremonte & Etchegoin 2002, Diaz et al. 2011, Capasso et al. 2017), and from L. atlanticus on the Buenos Aires coast (La Sala et al. 2009). The present finding represents the first record from L. specularioides.

Notocotylidae Lühe, 1909

Notocotylus Diesing, 1839

Notocotylus primulus Diaz, Gilardoni, Lorenti & Cremonte, 2020

The study of the specimens collected in this study allowed the description of a new species of the genus Notocotylus (Diaz et al. 2020). Six species of this genus were registered parasitizing birds from Argentina: Notocotylus attenuatus (Rudolphi, 1809) infecting the Silver Teal Lophonetta versicolor Vieillot and the Black-necked Swan Cygnus melanocorypha (Molina) (Anatidae); Notocotylus gibbus (Mehlis in Vreplin, 1846) infecting the White-winged Coot Fulica leucoptera Vieillot (Rallidae) from the Buenos Aires province; Notocotylus biomphalariae Flores & Brugni, 2005 infecting Lophonetta sp. (Anatidae) and Gallus gallus domesticus (Linnaeus) (Phasianidae); and Notoctylus imbricatus (Noble, 1933) infecting the Chiloe Wigeon Lophonetta sibilatrix (Poepping) (Anatidae) from the Rio Negro province; Notocotylus chionis Baylis 1928 infecting the Snowy Sheathbill Chionis albus (Gmelin) (Chionidae); and Notocotylus tachyeretis Duthoit, 1931 in the Flying Steamerduck Tachyeres patachonicus (King) (Anatidae) from Patagonia (Lunaschi & Drago 2007 and reference there).

Paramonostomum Lühe, 1909

Paramonostomum sp. (Figure 8)

The morphological diagnosis agrees with species of the genus Paramonostomum (Graefe 1968, Odening 1982). Four species of this genus were registered parasitizing birds from South America; Paramonostomum fuscicollis Diaz & Guevara, 1970 parasitizing C. fuscicollis from Venezuela, P. ionorme Travassos, 1921 parasitizing the Common Gallinule Gallinula galeata galeata (Lichtenstein), the Plumbeous Rail Pardirallus sanguinolentus (Swainson), the Purple Gallinule Porphyrio martinicus (Linnaeus) (Rallidae), the Wattled Jacana jacana (Linnaeus) (Jacanidae), from Brazil and parasitizing P. martinicus from Venezuela and P. pseudalveatum Price, 1931 parasitizing the Yellow-billed Pintail Lophonetta georgica Gmelin (Anatidae) from Chile (Fernandes et al. 2015 and reference there). Other two species were recorded on the Antarctic Peninsula, P. antarticum Graefe, 1968 parasitizing C. alba and L. dominicanus (Graefe 1968, Odening 1982) and P. signiensis parasitizing C. alba (Jones & Williams 1969). At present, two larval stages (rediae with cercariae and metacercariae) of the family Notocotylidae were recorded from marine environments; one in the snail Laevilitorina caliginosa (Gould) (Littorinidae) from the Antarctic Peninsula (Graefe 1968), and other from the limpet N. magellanica from Patagonia, Argentina (Bagnato et al. 2015, Gilardoni et al. 2019). Specimens found at the present study were recorded for the first time in Argentina and this represents a new species awaiting study (E. Bagnato, G. Gilardoni & C. Cremonte unpublished data). Molecular sequences of larval stages from N. magellanica match with adults from H. ater (E. Bagnato, C. Gilardoni & F. Cremonte unpublished data).

Philophthalmidae Travassos, 1918

Parorchis Nicoll, 1907

Parorchis sp.

The morphological diagnosis agrees with the species recorded parasitizing L. dominicanus from the northern Patagonian coast, Argentina (Diaz et al. 2011). By the study of the new specimens recovered from the same host species and from C. fuscicollis, based on some morphological differences but clearly distinguished by molecular features, J.I. Diaz et al. (unpublished data) suggest that it may belong to a new species resembling P. acanthus. The snail Trophon geversianus (Pallas) (Muricidae) acts as the first intermediate host in the life cycle of this species harboring rediae with cercariae; the metacercariae are found encysted in the substrate (Bagnato et al. 2015, Gilardoni et al. 2019). The present record from L. scoresbii constitutes evidence of a new host for this species.

Renicolidae Dollfus, 1939; Renicola Cohn, 1904

Renicola spp. (Figure 9)

The morphological diagnosis agrees with species of the genus Renicola (Wrigth 1956). Some morphological features allow us to determine that different species are present in L. dominicanus and L. specularioides. Renicola sp. was recorded parasitizing L. dominicanus from Brazil (Wrigth 1956). Other three species were recorded in South America: Renicola cruzi Wright, 1956 parasitizing the South American Tern Sterna hirundinacea Lesson, Sterna sp., and the Royal Tern Sterna maxima Boddaert (Sternidae) from Brazil; Renicola cf. cruzi parasitizing S. maxima from Colombia; and Renicola mirandaribeiroi parasitizing the Brown Booby Sula leucogaster (Boddaert) (Sulidae) from Brazil (Fernandes et al. 2015 and references there). Two larval stages (sporocyst with cercariae) were recorded from the northern Patagonian coast, Argentina; one of them parasitizing the snail T. geversianus and the other parasitizing the limpet N. magellanica (Bagnato et al. 2015, Gilardoni et al. 2019). It means that two renicolid species cohabit on the Patagonian coast; the adult found in L. dominicanus could be a different species than that parasitizing L. specularioides. A renicolid metacercaria belonging to the same species to the redia found in T. geversianus was recorded in the mussel M. edulis (Bagnato et al. 2015). Other renicolid metacercariae were found parasitizing the limpet N. magellanica and the bivalves Lasaea adansoni and G. trapesina on the Patagonian coast (F. Cremonte & C. Gilardoni unpublished data). Species (as an adult stage) of this genus are recorded for the first time in Argentina.

Schistosomatidae Stiles & Hassall, 1898

Schistosomatidae gen. et sp. indet. (Figure 10)

The morphological diagnosis agrees with species of the family Schistosomatidae (Odhner 1910, Price 1929). Two species were recorded in birds from Argentina; Dendrithobilharzia rionegrensis Martorelli, 1981 parasitizing the Red-fronted Coot Fulica rufifrons Philippi & Landbeck (Rallidae) and Ornithobilharzia canaliculata (Rudolphi, 1849) Odhner, 1912 parasitizing L. maculipennis and L. dominicanus (Fernandes et al. 2015 and reference there). Larval stages (sporocyst with cercariae) of one species belonging to this family were recorded parasitizing the pulmonate marine snail S. lessonii (Alda & Martorelli 2009, Gilardoni et al. 2011), and it belongs to the same species of the schistosomatid adults found in L. dominicanus but not morphologically described at present (Brant et al. 2017).

NEMATODA

Spirurida (Diesing, 1861)

Acuariidae (Seurat, 1913), Acuariinae Raillet, Henry and Sisoff, 1912

Cosmocephalus obvelatus (Creplin, 1825)

The morphological diagnosis agrees with the species recorded parasitizing L. dominicanus from the northern Patagonian coast, Argentina (Diaz et al. 2011). This acuariid nematode has a wide geographical and host distribution (Diaz et al. 2011). In Larus spp., this species has been found in Canada, Brazil, Spain, New Zealand, and Chile (Diaz et al. 2011). In Argentina, the species was reported parasitizing the Magellanic Penguin and the Kelp Gull (Diaz et al. 2001, 2010, 2011). The species showed great morphological stability and it was concluded that it has high adaptability to different hosts and localities (Diaz et al. 2011).

Paracuaria adunca (Creplin, 1846)

The morphological diagnosis agrees with the species recorded parasitizing L. dominicanus from the northern Patagonian coast, Argentina (Diaz et al. 2004). This is a frequent nematode parasitizing several piscivorous birds (e.g. Laridae, Gaviidae, Podicipedidae, Diomedeidae, Anatidae) and widely distributed in North and Central America, Europe, and Asia (Anderson & Wong 1982). It was reported for the first time in South America and for L. dominicanus and later, the species was found from the same host in Chile (see Diaz et al. 2004, 2011).

Anisakidae Railliet & Henry, 1912

Anisakidae gen. et sp. indet. (larvae)

The morphological diagnosis agrees with species of the family Anisakidae (Navone et al. 1998). Anisakid nematodes have a worldwide distribution and are associated with fishes, birds, and marine mammals. Transmission of species usually involves aquatic invertebrates and fish as intermediate or paratenic hosts (Anderson 2000). In the Southwest Atlantic, larval stages of a different genus of this family were reported (Garbin et al. 2019a). Among them, species of Contracaecum Raillet and Henry, 1912 were registered in different Patagonian birds (Garbin et al. 2019b).

ACANTOCEPHALA

Polymorphidae Meyer, 1931

Profilicollis Meyer, 1931

Profilicollis chasmagnathi (Holcman-Spector, Mañé-Garzón & Dei-Cas, 1977)

The morphological diagnosis agrees with the species recorded parasitizing L. dominicanus from the northern Patagonian coast, Argentina (Diaz et al. 2011). Amin (2013) recognized 9 species of the genus Profilicollis. All of them are parasites of waterfowl and fish eating adult birds and use decapods as intermediate hosts (Rodríguez et al. 2017, Lorenti et al. 2018). In Argentina, P. chasmagnathi was reported in Larus atlanticus from the Bahía Blanca estuary, Buenos Aires Province (La Sala et al. 2013) and in L. dominicanus from the Chubut Province coast (Diaz et al. 2011). This finding represents the southernmost geographical record for P. chasmagnathi.

DISCUSSION

A total of 2 ectoparasites and 19 endoparasites taxa were recovered from the 4 coastal birds species here studied: 6 from Haematopus ater, 11 from Larus dominicanus, 3 from Leucophaeus scoresbii, and 5 from Lophonetta specularioides.

The study of ectoparasites, particularly lice, in aquatic birds from Argentina is very scarce. Most of the host-parasite associations known were described by materials collected in the country and later deposited abroad in museum collections such as the Natural History Museum of London, or the Kellogg Collection, University of California, USA. In this work, we only found two lice species, Quadraceps ridgwayi and Actornithophilus grandiceps from H. ater. Both of them were previously recorded parasitizing H. ater but without precise bibliographic references. Only one previous work focused on the lice of shorebirds in Argentina. Daciuk et al. (1981) reported three species parasitizing the Kelp Gulls from Península Valdés, Austromenopon transversum. Quadraceps punctatus, and Saemundssonia (Saemundssonia) lari. In a recent study, we analyzed and compared the community structure of lice infesting Kelp Gulls from anthropogenic environments, i.e. a urban waste landfill and fisheries discards, from two different locations in Argentina (E. Lorenti et al., unpublished data). In Puerto Madryn, Patagonia, we found 2 of the lice species previously reported as parasites of Kelp Gulls, S lari, and A. transversum. Eighty percent of the gulls were infested by at least one of these species. Despite there are no meaningful differences between populations, no latitudinal differences have been studied along the distribution of Kelp Gulls. In this sense, we assumed that the absence of lice might reflect a lower prevalence in this geographical area. In their recent work with shorebirds in Perú, Tavera et al. (2019) reported a prevalence of 62% Philopteridae and 49% Menoponidae. Despite the low number of birds analyzed in our work, the low infestation rates in Perú agree with our results. However, further research is needed to compare the ecology of lice in shorebirds and the possible differences between locations and host species.

This survey reports several new records of helminthes. Five species, Renicola sp. 1 from Larus dominicanus, Levinseniella sp., and Renicola sp. 2 from Lophoneta specularioides, and Paramonostomum sp. and Progynotaenia sp. from H. ater, are recorded for the first time in the mentioned coastal birds. For all birds, the helminth community was dominated by digeneans. These coastal birds feeding upon the intertidal zones and these areas are dominated by digeneans due to the high diversity of invertebrates acting as intermediate hosts.

Almost all the helminth species recovered parasitizing L. dominicanus in this survey were already previously recorded in Argentina (Diaz et al. 2011, Brant et al. 2017) excepting Renicola sp. 1. For the rest of the coastal birds analyzed, all findings represent new records, mainly because until now, parasite surveys for these bird species were practically non-existent. The three taxa (1 cestode and 2 digeneans) recorded for L. scoresbii and the four taxa (1 cestode and 3 digeneans) recorded for H. ater are the first records for these birds worldwide. Only 2 nematode species were previously recorded for L. specularioides (Agüero et al. 2015), then the five taxa (1 cestode and 4 digeneans) recovered in this survey constituted new records parasitizing this duck species.

This study contributes to the knowledge on marine biodiversity and elucidation of the parasites life cycles. Marine endoparasites are mainly transmitted using food webs; invertebrates usually act as intermediate hosts and vertebrates as definitive hosts (Lafferty et al. 2008). Therefore, birds parasites, the main top predators on the intertidal areas, can be indicators of diet and feeding habits.

The Kelp Gull L. dominicanus harbors a rich assemblage of parasites in agreement to its generalist feeding habits (Bertellotti & Yorio 1999, Diaz et al. 2011). Due to the presence of acuariid nematodes and cestodes that use fish as intermediate hosts, endoparasites reflect a diet including fish (Anderson & Wong 1982, Hoberg 1987). Crustaceans transmit the digenean Maritrema madrynense (Diaz & Cremonte 2010, Bagnato et al. 2015) and the acanthocephalan Profilicollis chasmagnathi (Lorenti et al. 2018). The digeneans Gymnophallus australis and Renicola sp. 1 are transmitted by mytilid bivalves (Szidat 1965, Cremonte et al. 2008, Bagnato et al. 2015).

Parasites of the Crested Duck L. specularioides allow us to infer that these birds feed upon crustaceans, which transmit two microphallid digeneans, and unknown bivalves which transmit the renicolid digenean. Notocotylid digeneans life cycles involve aquatic gastropods as intermediate hosts; cercariae usually encyst on vegetation or sometimes on the outer shell and/or operculum of the snail first intermediate host (Yamaguti 1975).

The limpet Nacella magellanica lives strongly adhered to the rocky substrate in the intertidal (Cortés & Narosky 1997) being a difficult prey for birds. Oystercatchers are adapted to eat limpets (Sapoznikow et al. 2008), and it is demonstrated by the presence of two digeneans, Gymnophalloides nacellae and Paramonostomum sp., which use this limpet species as intermediate hosts (Bagnato et al. 2015, Gilardoni et al. 2020, E. Bagnato, C. Gilardoni & F. Cremonte, unpublished data).

Birds, as definitive hosts, are the main promoters of the parasite diversity in aquatic environments (e.g., Fredensborg et al. 2006, Thieltges et al. 2011). The high vagility of birds compared to the other hosts in the trematode life cycle makes birds the main dispersal agents for trematodes. The close relationship between parasites and their hosts would allow understanding the ecological interactions in the coastal marine ecosystem.

ACKNOWLEDGMENTS

Fieldworks were conducted with permits provided by the Wildlife Secretary of Santa Cruz (Resolution Number 861/08). Authors thank Cristian Ituarte for his help in field and laboratory work; Alejandro Travaini for his help in field sampling; Ricardo Palma for helping in lice determination; Pablo Yorio for his help with the bird nomenclature. We also want to thank the anonymous reviewers for their valuable contributions. Financial support was provided by ANPCyT (PICTs, 2016-0653, 2015-0841, Préstamo BID), Universidad Nacional de La Plata (N859 to JID), and Conservation, Food and Health Foundation. All authors are members of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

REFERENCES

• AGÜERO ML & DIAZ JI. 2013. First Record of Streptocara formosensis (Nematoda: Acuariidae) from the Chubut Steamerduck, Tachyeres leucocephalus, Endemic to the Patagonian Coast, Southwest Atlantic. Comp Parasitol 80: 304-307.
• AGÜERO ML, GILARDONI C, CREMONTE F & DIAZ JI. 2015. Stomach nematodes of three sympatric species of anatid birds off the coast of Patagonia. J Helminthol 90: 663-667.
• ALDA P & MARTORELLI S. 2009. Larval digeneans of the siphonariid pulmonates Siphonaria lessoni and Kerguelenella lateralis and the flabelliferan isopod Exosphaeroma sp. from the intertidal zone of the Argentinean Sea. Comp Parasitol 76: 267-272.
• AMIN OM. 2013. Classification of the Acanthocephala, Folia Parasitol 60: 273-305.
• ANDERSON RC. 2000, The superfamily Ascaridoidea. In: Nematode parasites of vertebrates: their development and transmission. Anderson RC (Ed). Oxon, United Kingdom, CABI Publishing, p. 267-314.
• ANDERSON RC & WONG PL. 1982. The transmission and development of Paracuaria adunca (Creplin, 1846) (Nematoda: Acuarioidea) of gulls (Laridae). Can J Zool 60: 3092-3104.
• BAGNATO E, GILARDONI C, DI GIORGIO G & CREMONTE F. 2015. A checklist of marine larval trematodes (Digenea) in molluscs from Argentina, Southwestern Atlantic coast. Check List 11: 1706.
• BERTELLOTTI M & YORIO P. 1999. Spatial and temporal patterns in the diet of the Kelp Gull in Patagonia. The Condor 101: 790-798.
• BONA 1994. Familia Dilepididae Railliet & Henry, 1909. In: KHALIL LF, JONES A & BRAY RA (Eds). Key to the Cestode Parasite of Vertebrates. CAB International, Wallingford, p. 443-554.
• BRANT SV, LOKER ES, CASALINS L & FLORES V. 2017. Phylogenetic placement of a schistosome from an unusual marine snail host, the false limpet (Siphonaria lessonii) and gulls (Larus dominicanus) from Argentina with a brief review of marine schistosomes from snails. J Parasitol 103: 75-82.
• CAPASSO S & DIAZ JI. 2016. Arhythmorhynchus comptus (Acanthocephala: Polymorphidae) from shorebirds in Patagonia, Argentina, with some comments on a species of Profilicollis. Check List 12: 1910.
• CAPASSO S, D’AMICO V & DIAZ JI. 2017. Odhneria odhneri Travassos, 1921 (Trematoda: Microphallidae) in Migrant Shorebirds from Patagonia, Argentina. Rev Arg Parasitol Vol 6: 15-20.
• CAPASSO S, D’AMICO V & DIAZ JI. 2019. A new species of Maritrema (Trematoda: Microphallidae) parasitizing the Baird’s sandpiper Calidris bairdii, and comments about diversity of Microphallidae in two Nearctic Shorebirds at Patagonian sites in Argentina. Acta Trop 189: 10-14.
• CLAY T. 1981. The ischnoceran lice (Phthiraptera) of the oystercatchers (Aves: Haematopodidae). Can J Zool 59: 933-938.
• CLAY T. 1962. A key to the species of Actornithophilus Ferris, with notes and descriptions of new species. British Museum (Natural History).
• CORTÉS CN & NAROSKY T. 1997. Cien caracoles argentinos. Editoria Albatros, Buenos Aires, 158 p.
• CREMONTE F. 2001. Bartolius pierrei n. g., n. sp. (Digenea: Gymnophallidae) from the Península Valdés, Argentina. Syst Parasitol 49: 139-147.
• CREMONTE F. 2004. Life cycle and geographic distribution of the gymnophallid Bartolius pierrei (Digenea) on the Patagonian coast, Argentina. J Nat His 38: 1591-1604.
• CREMONTE F & ETCHEGOIN JA. 2002. First report of the microphallid digenean Odhneria odhneri Travassos, 1921 parasite of two birds from Patagonian coast, Argentina. Neotrópica 48: 58-60.
• CREMONTE F & MARTORELLI SR. 1998. Description of a new species of Maritrema (Digenea: Microphallidae) from Larus dominicanus (Aves: Laridae) in Buenos Aires coast, Argentina. Folia Parasit 45: 230-232.
• CREMONTE F, PINA S, GILARDONI C, RODRIGUES P, CHAI JY & ITUARTE C. 2013. A new species of gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. J Parasitol 99: 85-92.
• CREMONTE F, VÁZQUEZ N & ITUARTE C. 2008. The development of Gymnophallus australis Szidat, 1962 (Digenea: Gymnophallidae) from the Patagonian coast (Argentina) from metacercaria to adult, with an amended diagnosis of Gymnophallus Odhner, 1905. Syst Parasitol 69: 23-31.
• CZSPLINSKI B & VAUCHER C. 1994. Family Hymenolepididae Ariola, 1899. In: Keys to the Cestode Parasites of Vertebrates. Khalil LF, Jones A and Bray RA (Eds), Wallingford, UK: CAB International, p. 595-663.
• DACIUK J, CICCHINO AC, MAURI R & CAPRI JJ. 1981. Notas faunísticas y bioecológicas de Península Valdés y Patagonia. XXIV. Artrópodos ectoparásitos de mamíferos y aves colectados en la Península de Valdés y alrededores (provincia de Chubut, Argentina). Physis Secc C 39: 41-48.
• DIAZ JI & CREMONTE F. 2004. Himasthla escamosa n. sp. (Digenea: Echinostomatidae) from the Kelp gull, Larus dominicanus (Charadriiformes: Laridae) on the Patagonian coast, Argentina. J Parasitol 90: 308-314,
• DIAZ JI & CREMONTE F. 2010. Development from metacercaria to adult of a new species of Maritrema (Digenea: Microphallidae) parasitic in Kelp gull, Larus dominicanus, from Patagonian coast, Argentina. J Parasitol 96: 740-745.
• DIAZ JI, CREMONTE F & NAVONE GT. 2001. New host and distribution record of Cosmocephalus obvelatus (Creplin, 1825) (Nematoda: Acuariidae) with morphometric comparisons. Comp Parasitol 68: 277-282.
• DIAZ JI, CREMONTE F & NAVONE GT. 2004. First record of the acuarioid nematode Paracuaria adunca from South America, with new morphological details and discussion of cordons. Comp Parasitol 71: 238-242.
• DIAZ JI, CREMONTE F & NAVONE GT. 2010. Helminths of the Magellanic penguin, Spheniscus magellanicus (Sphenisciformes), during the breeding season in Patagonian coast, Chubut, Argentina. Comp Parasitol 77: 172-177.
• DIAZ JI, CREMONTE F & NAVONE GT. 2011. Helminths of the kelp gull, Larus dominicanus, from the northern Patagonian coast. Parasitol Res 109: 1555-1562 .
• DIAZ JI, GILARDONI C & CREMONTE F. 2012. Description of Maritrema formicae sp. nov. (Digenea, Microphallidae) parasitic in the kelp gull, Larus dominicanus, from the Patagonian coast, Argentina. Acta Parasitol 57: 149-153.
• DIAZ JI, GILARDONI C, LORENTI E & CREMONTE F. 2020. Notocotylus primulus n. sp. (Trematoda: Notocotylidae) from the crested duck Lophonetta specularioides (Aves, Anatidae) from Patagonian coast, southwestern Atlantic Ocean. Parasitol Int 74: 101976.
• ETCHEGOIN JA & MARTORELLI SR. 1997. Description of a new species of Maritrema (Digenea: Microphallidae) from Mar Chiquita coastal lagoon (Buenos Aires, Argentina) with notes on its life cycle. J Parasitol, p. 709-713.
• FAVERO M & SILVA RODRÍGUEZ MP. 2005. Estado actual y conservación de aves pelágicas que utilizan la plataforma continental argentina como área de alimentación. Hornero 20: 95-110.
• FERNANDES BMM, JUSTO MCN, CÁRDENAS MQ & COHEN SC. 2015. South American trematodes parasites of birds and mammals. Biblioteca de Ciências Biomédicas. ICICT, Fiocruz–RJ, Rio de Janeiro.
• FERRIS GF. 1916. Some generic groups in the mallophagan family Menoponidae. Can Entomol 48: 301-311.
• FREDENSBORG BL, MOURITSEN KN & POULIN R. 2006. Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail from small to large scale. Mar Biol 149: 275-283.
• GALAKTIONOV KV & SKIRNISSON K. 2000. Digeneans from intertidal molluscs of SW Iceland. Syst Parasitol 47: 87-101.
• GARBIN L, CAPASSO S, DIAZ JI, MORGENTHALER A, MILLONES A & NAVONE G. 2014. Nuevo hospedador y registro geográfico de Contracaecum australe (Nematoda, Anisakidae) parasitando a Phalacrocorax gaimardi (Aves, Phalacrocoracidae) en costas del Atlántico Sudoccidental. Rev Argen Parasitol 3: 6-11.
• GARBIN L, DIAZ JI, MORGENTHALER A, MILLONES A, KUBA L, FUCHS D & NAVONE GT. 2019a. Cormorant pellets as a tool for the knowledge of parasite-intermediate host associations and nematode diversity in the environment. Helminthologia 56: 296.
• GARBIN LE, DIAZ JI & NAVONE GT. 2019b. Species of Contracaecum parasitizing the Magellanic Penguin Spheniscus magellanicus (Spheniscidae) from the Argentinean Coast. J Parasitol 105: 222-231.
• GARBIN LE, NAVONE GT, DIAZ JI & CREMONTE F. 2008. A new Anisakid species parasitizing the Imperial Cormorant, Phalacrocorax atriceps from the North Patagonian Coast, Argentina. J Parasitol 94: 852-859.
• GILARDONI C, DI GIORGIO G, BAGNATO E & CREMONTE F. 2019. Survey of trematodes in intertidal snails from Patagonia, Argentina: new larval forms and diversity assessment. J Helminthol 93: 342-351.
• GILARDONI C, DI GIORGIO G, BAGNATO E, PINA S, RODRIGUES P & CREMONTE F. 2020. A potential zoonotic parasite, the digenean Gymnophalloides nacellae, on the Magellanic coast in the Southwestern Atlantic Ocean: its life cycle and geographical distribution. Pol Biol 43: 725-734.
• GILARDONI C, ETCHEGOIN J, DIAZ J, ITUARTE C & CREMONTE F. 2011. A survey of larval digeneans in the commonest intertidal snails from Northern Patagonian coast, Argentina. Acta Parasitol 56: 163-179.
• GRAEFE G. 1968. Paramonostomum antarcticum n. sp. (Trematoda: Notocotylidae) und Beobachtungen zur Larvenentwicklung in der Antarktis. Z Parasitenk 30: 207-232.
• HOBERG EP. 1987. Tetrabothrius shinni sp. nov. (Eucestoda) from Phalacrocorax atriceps Bransfieldensis (Pelecaniformes) in Antarctica with comments on morphological variation, host–parasite biogeography, and evolution. Can J Zool 65: 2969-2975.
• HOBERG EP. 1994. Keys to the genera and subgenenera of the family Tetrabothriidae. In: KHALIL LF, JONES A & BRAY RA (Eds), Key to the Cestode Parasite of Vertebrates, Albans, UK: CAB International, p. 295-307.
• JOHRI GN. 1963. On a new protogynous cestode with remarks on certain species of the genus Progynotaenia Fuhrmann, 1909. J Helminthol 37: 39-45.
• JONES NV & WILLIAMS IC. 1969. Paramonostomum signiensis n. sp. (Trematoda: Notocotylidae) from the sheathbill, Chionis alba (Gmelin), at Signy Island, South Orkney Islands. J Helminthol 43: 53-57.
• KHALIL LF. 1994. Family Progynotaeniidae Fuhrmann, 1936. In: Keys to the Cestode Parasites of Vertebrates. Khalil LF, Jones A and Bray RA (Eds), Wallingford, UK: CAB International, p. 381-385.
• LABRIOLA JS & SURIANO DM. 2001.Community structure of parasitic helminths of birds of the genus Larus from Mar del Plata, Argentina. Vie et Milieu 51: 67-76.
• LAFFERTY KD ET AL. 2008. Parasites in food webs: the ultimate missing links. Ecol Lett 11: 533-546.
• LA SALA LF, MARTORELLI SR, ALDA P & MARCOTEGUI P. 2009. Some Digeneans from Olrog’s Gull Larus atlanticus Olrog, 1958 (Aves: Laridae) from the Bahía Blanca Estuary, Argentina. Comp Parasitol 76: 113-116.
• LA SALA LF, PEREZ AM, SMITS JE & MARTORELLI SR. 2013. Pathology of enteric infections induced by the acanthocephalan Profilicollis chasmagnathi in Olrog’s gull, Larus atlanticus, from Argentina. J Helminthol 87: 17-23.
• LEONARDI MS & QUINTANA F. 2017. Lousy chicks: Chewing lice from the Imperial Shag, Leucocarbo atriceps. Int J Parasitol: Parasites and Wildlife 6: 229-232.
• LEONARDI MS, SVAGELJ WS, GÓMEZ LAICH A & QUINTANA F. 2018. The eldest sibling is the lousiest in an obligate brood-reducer seabird. Emu-Austral Ornithology 118: 212-217.
• LORENTI E, RODRÍGUEZ SM, CREMONTE F, D’ELÍA G & DIAZ JI. 2018. Life cycle of the parasite Profilicollis chasmagnathi (Acanthocephala) on the Patagonian coast of Argentina based on morphological and molecular data. J Parasitol 104: 479-485.
• LUNASCHI LI & DRAGO FB. 2007. Checklist of digenean parasites of amphibians and reptiles from Argentina. Zootaxa 1476: 51-68.
• MARCOGLIESE DJ. 2005. Parasites of the superorganism: Are they indicators of ecosystem health? Int J Parasitol 35: 705-716.
• MARIAUX J, TKACH V, VASILEVA, GP, WAESCHENBACH A & BEVERIDGE I. 2017. Cyclophyllidea van Beneden in Braun, 1900. Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth, p. 77-148.
• NAVONE GT, SARDELLA NH & TIMI JT. 1998. Larvae and adults of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda: Anisakidae) in fishes and crustaceans in the south west Atlantic. Parasite 5(2): 127-136.
• NIKOLOV PN, GEORGIEV BB, GVOZDEV EV & GULYAEV VD. 2005. Taxonomic revision of the cestodes of the family Progynotaeniidae (Cyclophyllidea) parasitising stone curlews (Charadriiformes: Burhinidae). Syst Parasitol 61: 123-142.
• ODENING K. 1982. Paramonostomum antarcticum (Trematoda, Notocotylidae) in Larus dominicanus from South Shetlands (Antarctica). Angew Parasitol 23: 137-143.
• ODHNER T. 1910. Gigantobilharzia acotylea ng, n. sp., ein mit den Bilharzien verwandter Blutparasit von enormer Länge. Zool Anz 35: 380-385.
• PALMA RL. 1995. A new synonymy and new records of Quadraceps (Insecta: Phthiraptera: Philopteridae) from the Galapagos Islands. New Zeal J Zool 22: 217-222.
• PIAGET É. 1880. Les pédiculines: essai monographique (Vol. 1). Brill.
• PRICE EW. 1929. A synopsis of the trematode family Schistosomidae, with descriptions of new genera and species. U S Natl Mus Proc 75: 1-39.
• PRICE RD, HELLENTHAL RA & PALMA RL. 2003. World checklist of chewing lice with host associations and keys to families and genera. The chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication 24: 1-448.
• RODRÍGUEZ S, DIAZ JI & D’ELIA G. 2017. Morphological and molecular evidence on the existence of a single estuarine and rocky intertidal acanthocephalan species of Profilicollis Mayer, 1931 along the Atlantic and Pacific coasts of southern South America. Syst Parasitol 94: 527-533.
• SAPOZNIKOW A, REEVES C, SESSA G, MANSUR L & DE LA RETA M. 2008. Aves marinas y playeras. Fundación Patagonia Natural. Puerto Madryn Argentina, 54 p.
• SCHMIDT GD. 1986. CRC handbook of tapeworm identification. CRC Press, Inc, USA, 675 p.
• SZIDAT L. 1964. Estudios helmintológicos comparativos de las gaviotas grandes argentinas Larus marinus dominicanus Lichtenstein y Larus ridibundus maculipenis Lichtenstein, juntamente con nuevas observaciones sobre la especiación de parásitos. Z Parasitenk 24: 351-414.
• SZIDAT L. 1965. Los parásitos de los mitílidos y los daños por ellos causados II. Los parásitos de Mytilus edulis platensis (mejillón del plata). Comunicaciones del Museo Argentino de Ciencias Naturales Bernardino Rivadavia 1: 1-16.
• TAVERA EA, MINAYA D, LOPEZ EO, IANNACONE J, LANJ DB. 2019. Chewing lice richness and occurrence in non-breeding shorebirds in Paracas, Perú. Wader Stud 126(3): 190-199.
• THIELTGES DW, HOF C, DEHLING DM, BRÄNDLE M, BRANDL R & POULIN R. 2011. Host diversity and latitude drive trematode diversity patterns in the European freshwater fauna. Global Ecol Biogeogr 20: 675-682.
• WRIGHT CA. 1956. Studies on the life history and ecology of the trematode genus Renicola Cohn, 1904. In: Proceedings of the Zoological Society of London, Vol. 126, No. 1, Blackwell Publishing Ltd, Oxford, UK, p. 1-50.
• YAMAGUTI S. 1975. Synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms, Keigaku Publishing Co., 219 p.
• YORIO P, BERTELLOTTI M & GARCÍA BORBOROGLU P. 2005. Estado poblacional y de conservación de gaviotas que se reproducen en el litoral marítimo argentino. El Hornero 20: 53-74.

Publication Dates

• Publication in this collection
  29 May 2023
• Date of issue
  2023

History

• Received
  2 Dec 2020
• Accepted
  26 May 2021