Helminths of three species of opossums (Mammalia, Didelphidae) from Mexico.

From August 2011 to November 2013, 68 opossums (8 Didelphis sp., 40 Didelphisvirginiana, 15 Didelphismarsupialis, and 5 Philanderopossum) were collected in 18 localities from 12 Mexican states. A total of 12,188 helminths representing 21 taxa were identified (6 trematodes, 2 cestodes, 3 acanthocephalans and 10 nematodes). Sixty-six new locality records, 9 new host records, and one species, the trematode Brachylaimadidelphus, is added to the composition of the helminth fauna of the opossums in Mexico. These data, in conjunction with previous records, bring the number of taxa parasitizing the Mexican terrestrial marsupials to 41. Among these species, we recognized a group of helminths typical of didelphids in other parts of the Americas. This group is constituted by the trematode Rhopaliascoronatus, the acanthocephalan Oligacanthorhynchusmicrocephalus and the nematodes Cruziatentaculata, Gnathostomaturgidum, and Turgidaturgida. In general, the helminth fauna of each didelphid species showed a stable taxonomic composition with respect to previously sampled sites. This situation suggests that the rate of accumulation of helminth species in the inventory of these 3 species of terrestrial marsupials in the Neotropical portion of Mexico is decreasing; however, new samplings in the Nearctic portion of this country will probably increase the richness of the helminthological inventory of this group of mammals.

Introduction

Less than 25% of the 525 species of mammals distributed in Mexico have been examined for helminth parasites (García-Prieto et al. 2012). To date, 336 nominal taxa of helminths have been recorded in mammals, 26 associated with 3 species of terrestrial opossums (Virginia opossum, Kerr, the common opossum Linnaeus, and the Gray four-eyed opossum Linnaeus) from this country. However, the knowledge of the helminth richness associated with this host group is incomplete due to the wide distribution of these mammals in Mexico. occurs from Tamaulipas State and west San Luis Potosí until the Yucatán peninsula. inhabits almost all of Mexico, except for the central Plateau and Baja California peninsula. occurs from south Tamaulipas State along the Gulf of Mexico coast and Chiapas State (Arcangeli-Álvarez 2010, Cervantes et al. 2010). The main objective of this work is to present new records of helminth species parasitizing these 3 species of opossums in Mexico and to compare the finding to previous records.

Materials and methods

From August 2011 to November 2013, 68 opossums (8 sp., 40 , 15 , and 5 ) were collected in 18 localities from 12 Mexican states (Table 1), under the collecting permit FAUT 0057 issued by the Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT), Mexico. Mammals were shot by local hunters or caught with Tomahawk traps and then killed with intraperitoneal sodium pentobarbital overdose. Opossums were dissected within the following 4 h. and all organs were examined under a stereomicroscope. Helminths were placed in Petri dishes with 0.85% saline solution. Platyhelminths and nematodes were fixed with hot 4% formalin and preserved in 70% ethanol; acanthocephalans were chilled in distilled water for 10–12 h. Once the proboscis was everted, they were preserved in 70% ethanol. Platyhelminths and acanthocephalans were stained with Mayer’s paracarmin, cleared with methyl salicilate, and mounted in Canada balsam. Nematodes were cleared using Amman’s lactophenol and temporarily mounted for morphological study (Lamothe-Argumedo 1997). Voucher specimens of all helminth species were deposited at Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City.

Table 1.

Sampling sites for opossum species analyzed in this study.

State	Locality†/collection date (month/year)	Geographic coordinates	Sample size/host species	Altitude (easl)
Campeche	Escárcega1 07/2012	18°37'00"N; 90°43'13”W	3/Didelphis virginiana; 1/Didelphis marsupialis	82
Chiapas	Agua Fría2 06/2012; 03/2013	16°15'26"N; 93°53'55"W	5/Didelphis sp.; 1/Didelphis virginiana	60
	Finca Brasil3 06/2012	15°05'41"N; 92°13'45"W	2/Didelphis sp.; 3/Didelphis virginiana; 2/Didelphis marsupialis	463
Colima	Coquimatlán4 09/2012	19°10'28"N; 103°50'39”W	6/Didelphis virginiana	550
Distrito Federal	Pedregal de San Ángel5 02/2014	19°19'14"N; 99°12'33"W	2/Didelphis virginiana	2268
Guanajuato	Rincón de Martínez6 02/2013	20°19'44"N; 101°34'42”W	2/Didelphis virginiana	1730
Hidalgo	Tianguistengo7 03/2014	19°10'50"N; 99°28'06"W	2/Didelphis virginiana	2620
Morelos	Tepoztlán8 08/2014	19°00'07"N; 99°06'00"W	1/Didelphis virginiana	1700
Oaxaca	Cerro del Tepezcuintle9 08/2013	18°15'28”N; 96°24'00"W	2/Didelphis virginiana	87
Puebla	Coapan10 08/2014	18°25'42"N; 97°24'30"W	1/Didelphis sp.; 1/Didelphis virginiana	1648
	Zapotitlán Salinas11 08/2014	18°19'45"N; 97°28'30"W	1/Didelphis virginiana	2240
Tabasco	Teapa12 06-07/2013	17°33'59"N; 92°57'00”W	2/Didelphis virginiana 1/Didelphis marsupialis	72
	Villahermosa13 01/2012	17°34'17”N; 92°57'09”W	3/Didelphis virginiana	10
Veracruz	Tlacotalpan14 02/2012	18°37'40”N; 95°40'40”W	2/Didelphis virginiana; 8/Didelphis marsupialis; 3/Philander opossum	10
	Los Tuxtlas14 08/2011; 03/2012	18°34'21”N; 95°04'30”W	3/Didelphis virginiana; 3/Didelphis marsupialis 2/Philander opossum	300
Yucatán	Mérida15 11/2013	20°58'04"N; 89°37'18"W	5/Didelphis virginiana	16
	Tzucacab16 11/2013	20°00'58"N; 89°01'12"W	1/Didelphis marsupialis	36

The superscript numbers indicate the position of the localities in the Figure 1.

Figure 1.

Map of Mexico showing the sampled localities in the present study.

Results

A total of 12,188 helminths representing 21 taxa were identified in the 68 opossums collected from 18 localities within 12 states of Mexico (Figure 1). Six trematode, 2 cestode, 3 acanthocephalan, and 10 nematode species were collected. Below, we present PageBreaka checklist of the helminth species recorded, indicating the site of infection, current records with State and locality where the hosts were collected, host species, CNHE accession numbers, and previous records from Mexico.

Parasite-Host list

† New locality record; ‡ New record for Mexico; * New host in Mexico.

Phylum

Class

Family

Site of infection. Gall-bladder.

Present records. VERACRUZ: Los Tuxtlas: *, *.

Specimens deposited. CNHE 9481–2.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: (Cañeda-Guzmán 1997).

Remarks. These specimens belong to due to the position of the reproductive organs and the separation of the vitelline glands in two fields lying anterior and posterior to the ovary. Furthermore, the uterus has a zig-zag shape, occupying intercecal extension and the S-shape of the excretory vesicle, sinuous between both testes (Caballero et al. 1952).

Site of infection. Intestine.

Present records. CAMPECHE: Escárcega†: *.

Specimens deposited. CNHE 9483–4.

Remarks. The specific identification of this material follows Premvati and Blair (1979) and is based on the disposition of the vitellaria which extending from pharynx to posterior end.

Family

Site of infection. Gall-bladder.

Present records. Los Tuxtlas: *, .

Specimens deposited. CNHE 9485–6.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: (Cañeda-Guzmán 1997).

Remarks. In accordance with Thatcher (1970) this species is characterised by having body flattened and pyriform, covered with small spines. Cirrus and cirrus sac large. Parasites in gall-bladder of marsupials.

Family

Site of infection. Intestine.

Present records. VERACRUZ: Tlacotalpan†: *.

Specimens deposited. CNHE 9487.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: sp. (Haverkost and Gardner 2008).

Remarks. is distinguished by the absence of oral and flanking spines, and because it has between 4 and 11 spines visible within tentacle sacs (Haverkost and Gardner 2008).

Site of infection. Intestine.

Present records. CHIAPAS: Agua Fría†: , , sp., ; Finca Brasil†: , , . OAXACA: Cerro del Tepezcuintle†, San Miguel Soyaltepec†: . TABASCO: Cunduacán†: ; Grutas de Coconá†, Teapa†: . VERACRUZ: Los Tuxtlas: PageBreak, , ; Tlacotalpan†: , sp. YUCATÁN: Mérida†: .

Specimens deposited. CNHE 9488–9504.

Previous records in Mexico. CHIAPAS: Motozintla: sp. (Caballero et al. 1944). NUEVO LEÓN: Colonia Country La Silla, Huinala, Los Lirios: (Romero 1981). OAXACA: Cuicatlán: sp. (Pérez-Ponce de León et al. 2007). QUINTANA ROO: Rancho La Ceiba: (Kingston and Tai 1968). VERACRUZ: Los Tuxtlas: , , (Cañeda-Guzmán 1997), sp. (Haverkost and Gardner 2008); Alvarado: (Monet-Mendoza et al. 2005).

Remarks. The diagnostic traits of this species are: flanking and oral spines present. Between 3 and 11 spines visible within tentacle sacs, which extend far beyond the posterior margin of the pharynx (Haverkost and Gardner 2008).

Site of infection. Intestine.

Present records. VERACRUZ: Los Tuxtlas: , sp., ; Tlacotalpan†: , .

Specimens deposited. CNHE 9505–9.

Previous records in Mexico. COLIMA: Comala: (Lamothe-Argumedo 1978); La Esperanza: (Miyazaki et al. 1980). CHIAPAS: Jaltenango: sp. (Caballero 1946); Motozintla: sp. (Caballero et al. 1944); Pueblo Nuevo (Pérez-Ponce de León et al. 2007). OAXACA: Carretera Temascal-Tuxtepec: (Monet-Mendoza et al. 2005). QUINTANA ROO: Rancho La Ceiba: (Kingston and Tai 1968). VERACRUZ: Alvarado: (Monet-Mendoza et al. 2005); Los Tuxtlas: , , (Cañeda-Guzmán 1997), sp. (Haverkost and Gardner 2008).

Remarks. This species was identified by having tentacle sacs that do not extend beyond the posterior margin of the pharynx and by having only flanking spines (Haverkost and Gardner 2008).

Class

Family

Site of infection. Intestine.

Present records. COLIMA: Colima: .

Specimens deposited. CNHE 9514.

Previous records in Mexico. CHIAPAS: Lagos de Colón: (Monet-Mendoza et al. 2005). COLIMA: Colima: (García-Prieto et al. 2012).

Remarks. This material represents a new species which will be described separately.

Family

Site of infection. Intestine.

Present records. CHIAPAS: Finca Brasil†: *, .

Specimens deposited. CNHE 9528.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: (Cañeda-Guzmán et al. 2001).

Remarks. In accordance with Cañeda-Guzmán et al. (2001), is distinguished by the morphology of the scolex that is formed by 4 well separated lobes each containing 1 noncircular sucker opening laterally inside the exterolateral cavity, a large-sized body and by the shape of gravid proglottids that are inversely craspedote, among others.

Phylum

Family

Site of infection. Intestine.

Present records. HIDALGO: Tianguistengo†: .

Specimens deposited. CNHE 9510.

Previous records in Mexico. CAMPECHE: Escárcega: , (López-Caballero et al. 2015). COLIMA: Tecomán: (García-Prieto et al. 2010). CHIAPAS: Agua Fría: , , (López-Caballero et al. 2015); Cascadas de Agua Azul: (Prado-Ancona 1993); Finca Brasil: , , (López-Caballero et al. 2015). MICHOACÁN: Agua Blanca: (Prado-Ancona 1993). GUANAJUATO: Rincón de Martínez: (López-Caballero et al. 2015). MORELOS: Progreso: (García-Prieto et al. 2010). OAXACA: Soyaltepec: (López-Caballero et al. 2015); Temascal: (García-Varela et al. 2000). TABASCO: Cunduacán: (López-Caballero et al. 2015); Ranchería el Boquerón: (García-Prieto et al. 2010); Río Oxolotán: (Prado-Ancona 1993). VERACRUZ: Los PageBreakTuxtlas: , , (Prado-Ancona 1993; Cañeda-Guzmán 1997); Tlacotalpan: (López-Caballero et al. 2015). YUCATÁN: Mérida: , (López-Caballero et al. 2015).

Remarks. With the exception of records made by López-Caballero et al. (2015) all other previous records were listed as , but this species is a junior synonym of (Richardson et al. 2014). The hook and cement gland number (36 and 8, respectively), as well as the eggs size (0.83-0.110 X 0.38-0.50) are considered as diagnostic traits of this species by López-Caballero et al. (2015).

Site of infection. Intestine.

Present records. VERACRUZ: Los Tuxtlas: *.

Specimens deposited. CNHE 9511–12.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: (Prado-Ancona 1993; Cañeda-Guzmán 1997).

Remarks. These specimens belong to because the dimensions of the proboscis, the number of hooks (36), as well as its size and arrangement fits to the morphology mentioned by Machado (1950).

Family

Site of infection. Intestine.

Present records. VERACRUZ: Los Tuxtlas: .

Specimens deposited. CNHE 9513.

Previous records in Mexico. CHIAPAS: Cascadas de Agua Azul: (Salgado-Maldonado and Cruz-Reyes 2002). TABASCO: Río Oxolotán: (Salgado-Maldonado and Cruz-Reyes 2002). VERACRUZ: Lago de Catemaco, Sontecomapan: (Salgado-Maldonado and Cruz-Reyes 2002); Martínez de la Torre: (Salgado-Maldonado and Cruz-Reyes 2002); Los Tuxtlas: , , (Salgado-Maldonado and Cruz-Reyes 2002).

Remarks. According to Salgado-Maldonado and Cruz-Reyes (2002), three characteristics diagnosed this acanthocephalan species: (1) a smaller proboscis, (2) the armature of proboscis bearing few rows and few hooks per row compared with other species, and (3) the male reproductive system occupying only the posterior half of trunk.

Phylum

Family

Site of infection. Lungs.

Present records. DISTRITO FEDERAL: Pedregal de San Ángel†: ; GUANAJUATO: Irapuato†: †. HIDALGO: Tianguistengo†: . MORELOS: Tepoztlán†: .

Specimens deposited. CNHE 8969, 9024, 9554–9556, 9562.

Previous records in Mexico. COLIMA: ND: (García-Márquez et al. 2012). GUERRERO: Laguna de Tres Palos, Taxco: (Monet-Mendoza et al. 2005). OAXACA: Temascal: (Monet-Mendoza et al. 2005).

Remarks. Our material was identified following Prestwood (1976); this species is characterised because the oral opening is surrounded by lips, the morphology and size of the spicules and the number and arrangement of bursal rays.

Family

Site of infection. Intestine.

Present record. TABASCO: Villahermosa†: *. VERACRUZ: Los Tuxtlas†: , *.

Specimens deposited. CNHE 8971–3.

Previous records in Mexico. CHIAPAS: Motozintla: sp. (Caballero and Zerecero 1944).

Remarks. These specimens were identified based on Jiménez-Ruiz et al. (2006) and compared with further description of the species made by Chagas-Moutinho et al. (2014). can be distinguished because the cephalic cordons exceed the level of the oral vestibule and touch the base of cephalic cap, as well as by having a digitiform projection on the left ventrolateral oral lip.

Family

Site of infection. Caecum.

Present records. CAMPECHE: Escárcega†: , . CHIAPAS: Arriaga†: sp., ; Tapachula†: PageBreak sp., , . COLIMA: Colima†: . DISTRITO FEDERAL: Pedregal de San Ángel†: . GUANAJUATO: Irapuato†: . HIDALGO: Tianguistengo†: . MORELOS: Tepoztlán†: . OAXACA: Soyaltepec†: . PUEBLA: Carretera Coapan-Huajuapan de León†: sp.; Coapan†: ; Zapotitlán Salinas†: . TABASCO: Teapa†: ; Villahermosa†: . VERACRUZ: Los Tuxtlas: , , ; Tlacotalpan†: , , . YUCATÁN: Mérida†: ; Tzucacab†: .

Specimens deposited. CNHE 8999, 9000–17, 9533–9540, 9557, 9563.

Previous records in Mexico. CHIAPAS: Motozintla: sp. (Caballero and Zerecero 1944); Jaltenango: (Caballero 1958). COLIMA: Comala: (García-Prieto et al. 2012); La Esperanza: (Miyazaki et al. 1980); ND: (Lamothe-Argumedo et al. 1981). DISTRITO FEDERAL: ND: sp. (Caballero 1937); Chapultepec: (Gutiérrez-Fuster 1966). ESTADO DE MÉXICO: ND: sp. (García-Prieto et al. 2012). HIDALGO: Tasquillo: sp. (Caballero 1937). JALISCO: Chamela: (García-Prieto et al. 2012). MORELOS: Reserva Estatal Sierra de Monte Negro: (Slava-Araujo 2005). NUEVO LEÓN: San Nicolás de los Garza: (García-Prieto et al. 2012). VERACRUZ: Los Tuxtlas: , , (Cañeda-Guzmán 1997); ND: (Flores-Barroeta 1957).

Remarks. We identify these nematodes according to the re-description made by Adnet et al. (2009), who established the number of caudal papillae (ten pairs of button-like papillae, symmetrically ventro-laterally located), as well as the single median papilla at the anterior cloacal lip and four pairs of post-cloacal papillae, as diagnostic traits of this species.

Family

Site of infection. Stomach (adult; larvae); liver (sub-adult).

Present records. CHIAPAS: Arriaga†: sp. COLIMA: Colima†: . OAXACA: Soyaltepec†: . TABASCO: Teapa†: . VERACRUZ: Tlacotalpan: .

Specimens deposited. CNHE 8979–86, 9548–9549.

Previous records in Mexico. CHIAPAS: Jaltenengo: (Caballero 1958). COLIMA: Laguna de Amela: (García-Márquez 2005). GUERRERO: Laguna de Tres Palos: (Monet-Mendoza et al. 2005). JALISCO: Carretera Juntas-Palmas (Puerto Vallarta): PageBreak (Monet-Mendoza et al. 2005); Chamela: (see Lamothe-Argumedo et al. 1998). MORELOS: Valle de Amilcingo: (Mosqueda-Cabrera 2003). OAXACA: Temascal: (Almeyda-Artigas et al. 2010), (Almeyda-Artigas et al. 2000, Oceguera-Figueroa 2002, Mosqueda-Cabrera 2003), (Lamothe-Argumedo et al. 1998, Almeyda-Artigas et al. 2000, Mosqueda-Cabrera 2003). SINALOA: Tecualilla: (Nawa et al. 2009, Díaz-Camacho et al. 2009). TABASCO: Rancho Mendoza Llergo: (León-Règagnon et al. 2005); Jardín Botánico de la UJAT, Oriente Segunda Sección, Ranchería El Limón, Ranchería Emiliano Zapata, Ranchería José María Pino Suárez, Ranchería La Palma: (Gallegos-Torres 2003). VERACRUZ: Laguna Los Vila, Laguna Novillera: (León-Règagnon et al. 2005); Tlacotalpan: (Almeyda-Artigas et al. 2000, Pérez-Álvarez et al. 2008), (Pérez-Álvarez et al. 2008).

Remarks. The presence of numerous points on the posterior end of cuticular spines at esophagus-intestine junction level, the body size, and the lack of spines in the posterior region of body, constitutes the diagnostic traits of this species in accordance with Bertoni-Ruiz et al. (2011).

Family

Site of infection. Stomach.

Present records. CHIAPAS: Tapachula†: .

Specimens deposited. CNHE 8970.

Remarks. Two species of the genus are distributed in Mexican didelphids: (in Chiapas and Veracruz) and (in Chiapas) (García-Prieto et al. 2012). The specific identification of our specimen was not possible because we collected only one female.

Family

Site of infection. Stomach.

Present records. CAMPECHE: Escárcega†: , . CHIAPAS: Arriaga†: sp.; Tapachula†: sp.; . COLIMA: Colima: . DISTRITO FEDERAL: Pedregal de San Ángel: . GUANAJUATO: Irapuato†: . HIDALGO: Tianguistengo†: . OAXACA: Soyaltepec†: PageBreak. PUEBLA: Coapan†: . TABASCO: Teapa: ; Villahermosa: . VERACRUZ: Los Tuxtlas: , ; Tlacotalpan†: , , .

Specimens deposited. CNHE 9018–23, 9025–36, 9541–9543.

Previous records in Mexico. CHIAPAS: Motozintla: sp. (Caballero and Zerecero 1944, 388); Tonalá: (García-Prieto et al. 2012). COLIMA: Colima: (Monet-Mendoza et al. 2005); Comala: (Monet-Mendoza et al. 2005), (García-Prieto et al. 2012); Dos Amates: (Monet-Mendoza et al. 2005); La Esperanza: (Miyazaki et al. 1980); Madrid: (Miyazaki et al. 1980), (Monet-Mendoza et al. 2005); ND: (Lamothe et al. 1981). DISTRITO FEDERAL: ND: sp. (Caballero 1937), (Monsivais-Aguilar 1958); Pedregal de San Ángel: (Pacheco-Coronel 2010); Chapultepec: (Gutiérrez-Fuster 1966). ESTADO DE MÉXICO: ND: sp. (García-Prieto et al. 2012): Tequesquinahuac: (Monet-Mendoza et al. 2005). GUERRERO: Carretera Coyuquilla-Zihuatanejo, Coyuquilla: (Monet-Mendoza et al. 2005); Carretera Aeropuerto-Ixtapa: (García-Prieto et al. 2012); Taxco El Viejo: (Monet-Mendoza et al. 2005). HIDALGO: Tasquillo: sp. (Caballero 1937). JALISCO: Chamela: (García-Prieto et al. 2012). MICHOACÁN: El Hortigal: (Monet-Mendoza et al. 2005). MORELOS: Reserva Estatal Sierra de Monte Negro: (Eslava-Araujo 2005). NAYARIT: Peñitas: (Monet-Mendoza et al. 2005). NUEVO LEÓN: Marín, Monterrey: (García-Prieto et al. 2012). OAXACA: Dominguillo: (see Monet-Mendoza et al. 2005); Nizanda: (Monet-Mendoza et al. 2005). VERACRUZ: Los Tuxtlas: , , (Cañeda-Guzmán 1997); Medellín: (Caballero-Deloya 1969).

Remarks. These specimens were identified based on the re-description of this species (Matey et al. 2001). Its diagnostic traits are: the presence of 2 spongelike areas on the inner side of each pseudolabia, and the number of caudal papillae (22).

Family

Site of infection. Caecum.

Present records. CAMPECHE: Escárcega†: . CHIAPAS: Arriaga†: sp. COLIMA: Colima†: . HIDALGO: TianPageBreakguistengo†: . MORELOS: Tepoztlán†: . YUCATÁN: Mérida†: ; Tzucacab†: .

Specimens deposited. CNHE 8974–78, 9550–9553.

Previous records in Mexico. VERACRUZ: Los Tuxtlas: , , (Cañeda-Guzmán 1997).

Remarks. Our material was identified based on the original description (Babero 1960). This species is characterised by the size of the spicule (0.47–0.6 mm), by having a spiny sheath, by the size of mature eggs (0.068 × 0.032 mm) and the posterior position of the vulva.

Site of infection. Lungs.

Present records. CAMPECHE: Escárcega: *, *

Specimens deposited. CNHE 9031–2.

Remarks. Identification was not possible because only eggs were obtained.

Family

Site of infection. Intestine.

Present records. CAMPECHE: Escárcega†: . CHIAPAS: Arriaga†: , *. COLIMA: Colima†: . OAXACA: Soyaltepec†: . PUEBLA: Coapan†: . TABASCO: Teapa†: ; Villahermosa†: . VERACRUZ: San Andrés Tuxtla†: , ; Tlacotalpan†: , *.

Specimens deposited. CNHE 8988–98; 9025–30, 9544–9547.

Previous records in Mexico. GUERRERO: Taxco El Viejo: (Monet-Mendoza et al. 2005).

Remarks. Our specimens were identified following Guerrero (1985). The synlophe of at mid-body has 3 ventral ridges orientated to left, short spicules (0.133-0.141 mm) and bursal ray arrangement 2-1-2 type.

Site of infection. Intestine (Adult).

Present records. CHIAPAS: Arriaga†: sp.

Specimens deposited. CNHE 8987.

Remarks. To date, 12 species of the genus have been described, all parasitizing New World marsupials; Travassos, 1935 is the only species of this genus recorded in Mexico as parasite of ; however, the finding of only 8 females make species identification difficult, because taxonomy of this group is based on male characteristics (Scheibel et al. 2014).

Discussion

As a result of this study, we reported 66 new locality records, 9 new host records, and added one species to the composition of the helminth fauna of the opossums in Mexico: the trematode parasitizing , which had not been recorded in this country (see García-Prieto et al. 2012). A total of 21 helminth taxa were obtained from the 3 opossums species analyzed (6 trematodes, 2 cestodes, 10 nematodes and 3 acanthocephalans), all in adult stage, with exception of the larvae of collected during their migration through the liver of the hosts. The richest helminth fauna among the 3 host species was recorded in , (parasitized by 17 species), followed by (11 species) and (8 species). The digestive tract had the highest number of helminth species (12 intestinals, 2 in gall-bladder, 2 in caeca, and 3 in stomach); only 2 of the 21 taxa, and gen. sp. were found in another site of infection (lungs). The geographic distribution of the helminth species was heterogeneous. The nematode was the only species found in all localities. Other helminth species were collected from 7 (), 8 () and 9 () localities; however, most taxa (12) were found in only one locality.

These data bring the number of taxa parasitizing , , and to 37, 21 and 20, respectively (García-Prieto et al. 2012). In this work we sampled in 9 previously unstudied localities; nevertheless, 47.2%, 52.4% and 40% of the taxa collected were reported previously from the Virginia opossum, Black-eared opossum and Gray four-eyed opossum, respectively. These species are typical of didelphids in other parts of the Americas (see Alden 1995; Corrêa Gomes et al. 2003; Haverskot and Gardner 2008; Bertoni-Ruiz et al. 2011; Richardson et al. 2014), conforming a group basically represented by the trematode , the acanthocephalan and the nematodes , , and ; these species have been recorded associated to any of the three opossum species in 7,10,15, 9, and 17 Mexican states, respectively. In states where the 3 host species are distributed sympatrically, and are the species more frequently shared between them. On the other hand, the most restricted geographic areas are presented by the trematodes , , and , the acanthocephalan , and the nematodes sp., and sp., which are present exclusively in one locality. In total, the records of this group of mammals come from 20 of the 32 states of the Mexican Republic; however, the geographic information is asymmetrical, PageBreakbecause most of the samplings were made in the state of Veracruz (13 sites). Other states, as Campeche and Quintana Roo, have been sampled once. Moreover, most of the species that have been found parasitizing these didelphid species represent point locality records in only one study about its parasites cover states or regions, particularly Los Tuxtlas, Veracruz. However, the host’s collections were made along 13 years, in different year season and with a very distinct sample size (see Cañeda-Guzmán 1997).

Considering only the 27 nominal helminth species recorded to date, the 3 host species shared 12 worm species along the sampled sites in Mexico; 8 were exclusively found in , and 2 are specialist to . The cestode and the acanthocephalan are shared by the 2 species of the genus but not by ; the Virginia opossum and the Grey four-eyed opossum shared the digenean and the nematode , whereas and shared only . The helminth fauna of these hosts throughout their range is composed by one group of 20 specialist species, and by , , , , , , and that act as generalist species. Accidental species have not been reported in any of the samples carried out to date in Mexico. At a local scale, both phenomena had been also observed in marsupials of French Guiana (Jiménez et al. 2011; Byles et al. 2013).

The structuring factor of the helminth fauna in the three didelphid species is the diet; most of the helminth species infect these host species through ingestion of eggs, larvae or intermediate hosts. Fifteen of the 27 named helminth species have indirect patterns of transmission (, , , , , , , , , , , , , , and ), five are transmitted directly by eggs ingestion (, , , , ) and for , , , , , and , the life cycle is unknown (Table 2). This result is in agreement with the generalist lifestyles and diets of the three species of opossums (Krause and Krause 2006), that exposed them to the same parasite species; local differences in composition and abundance of helminth species could be related to local availability of parasites (or their intermediate hosts), as well as to the compatibility among host and helminth species, as has been showed by Cañeda-Guzmán (1997) and Jiménez et al. (2011).

Table 2.

Life cycles of the helminth species collected in the present study.

Phylum	Taxa	Cycle/ Intermediate host	Reference
Platyhelminthes Trematoda	Amphimerus spp.	Heteroxenous/fish	Yamaguti (1975)‡
	Brachylaima spp.	Heteroxenous/snail	Yamaguti (1975)‡
	Philandrophilus magnacirrus	Unknown
	Rhopalias spp.	Unknown
Cestoda	Thaumasioscolex didelphidis	Heteroxenous/crustaceans	Scholz (1999)‡
Acanthocephala	Oligacanthorhynchus microcephalus	Heteroxenous/millipede	Richardson (2006)
	Oncicola luehei	Heteroxenous/insects, crustaceans	Kennedy (2006)
	Porrorchis nickoli	Heteroxenous/insects, crustaceans	Kennedy (2006)
Nematoda	Aspidodera raillieti	Monoxenous/eggs ingestion	Jiménez et al. (2011)
	Cruzia sp.	Monoxenous/eggs ingestion	Anderson (2000)
	Didelphostrongylus hayesi	Heteroxenous/snails	Prestwood (1976)
	Gnathostoma sp.	Heteroxenous/copepods	Kifune et al. (2004)
	Gongylonema sp.	Heteroxenous/insects	Anderson (2000)
	Turgida turgida	Heteroxenous/insects	Anderson (2000)
	Trichuris spp.	Monoxenous/eggs ingestion	Anderson (2000)
	Viannaia spp.	Unknown

Particular life cycle unknown; data obtained at supra-specific level.

The data obtained in this study came from 68 opossums collected from 18 localities (nine not previously sampled for helminths); however, the helminth fauna of each didelphid species showed a stable taxonomic composition with respect to previously sampled sites. Only one species of trematode not previously found in this group of hosts in the country was added to their parasitological record as results of our samples. In spite of the reduced scope of our samplings, this situation suggests that the rate of accumulation of helminth species in the inventory of the 3 species of terrestrial marsupials distributed in the Neotropical portion of Mexico included in this study is decreasing; however, new samplings in the Nearctic portion of this country will probably increase the richness of the helminthological inventory of this group of mammals.