Ecto- and endo-parasitic monogeneans (Platyhelminthes) on cultured freshwater exotic fish species in the state of Morelos, South-Central Mexico.

An extensive parasitological study of 365 freshwater exotic fish specimens belonging to 13 species of seven families (Cichlidae, Cyprinidae, Osphronemidae, Pangasidae, Poeciliidae, Characidae, and Loricariidae) collected from 31 Aquaculture Production Units (APU) from Central Mexico revealed the occurrence of 29 ecto- and endo-parasitic monogeneans found on gills and stomachs: Cichlidogyrussclerosus, C.thurstonae, C.tilapiae, Cichlidogyrus sp. 1, Cichlidogyrus sp. 2, Enterogyruscoronatus, E.malmbergi, Gusseviaspiralocirra, Sciadicleithrumiphthimum, Sciadicleithrum sp., Scutogyruslongicornis (all Dactylogyridae), Gyrodactyluscichlidarum, and G.yacatli (Gyrodactylidae) on Oreochromisniloticus, Pterophyllumscalare and Hemichromis sp. (Cichlidae); Dactylogyrusbaueri, D.formosus, D.intermedius, D.vastator, D.extensus, Dactylogyrus sp. (all Dactylogyridae), and G.kobayashii on Carassiusauratus, Cyprinuscarpio and Ctenopharyngodonidella (Cyprinidae); Trianchoratusacleithrium and T.trichogasterium (Dactylogyridae) on Trichogastertrichopterus (Osphronemidae); Thaparocleiduscaecus, T.siamensis (Dactylogyridae), and Dactylogyridae sp. on Pangasianodonhypophthalmus (Pangasidae); G.poeciliae on Poeciliareticulata (Poeciliidae); Diaphorocleidusarmillatus (Dactylogyridae) on Gymnocorymbusternetzy (Characidae); Unilatusunilatus (Dactylogyridae) and Gyrodactylidae sp. on Hypostomus sp. (Loricariidae). The paramount importance of the establishment of these monogeneans due to the importation/exportation of non-native ornamental and other exotic host fish species cultured for food in Mexico is briefly discussed. Quarantine is recommended for all transferred host species.

Introduction

At a global level, increasing attention is being paid to generate useful ecological indicators that favor invasiveness and geographic range expansion by introduced species (Lavergne and Molofsky 2007, Blackburn and Ewen 2017). Conjointly, introductions of species are rising sharply because of increased trade, transport, travel, and tourism associated with globalization (IPPC Secretariat 2005). Within this context, trade of the non-native ornamental fish industry and/or fish farms for food production, has been the main cause of introductions of fish and their parasites around the world (Barroso de Magalhães and Jacobi 2013, Mendoza et al. 2015). Furthermore, the same industries pose a growing threat to native wildlife if non-native fishes are later released into the wild (see Mendoza-Franco et al. 2012). Culture of non-native ornamental and food fishes represents major activities in the state of Morelos (south-central Mexico) since these fishes are commercially distributed within and outside of Mexico in large quantities (Martínez et al. 2010).

Although non-native aquatic organisms are important to Morelos aquaculture and the economy of the state of Morelos, the aquaculture industry should be made aware of the considerable local, state, and national concern over the potential ecological or economic problems arising from non-native fish introductions and their parasites in natural environments (i.e., parasite transfer and/or fish competition with native species) (Barroso de Magalhães and Jacobi 2013). Recently, a total of 44 helminth species on introduced freshwater fishes were listed for Mexico, of which five are invasive species, i.e., Paperna & Thurston, 1969 Mueller & Van Cleave, 1932 and (Paperna 1968) García-Vasquez & Hansen, 2007 (); (Nishigori 1924) Price, 1932 () and Yamaguti, 1934 (), all of them introduced with their Asian and African hosts (Tapia Osorio et al. 2014). The present study was conducted to identify the most common ecto- and endo-parasitic monogeneans inhabiting commercially important ornamental and/or food fish species that have been imported into Mexico.

Materials and methods

Ornamental fish species were collected from 2010 to 2014 from different municipalities (Axochiapan, Ayala, Cuautla, Jiutepec, Jojutla, Tlaltizapan, Tlaquiltenango, Xochitepec, and Zacatepec) located in the state of Morelos. Live fish were examined thoroughly externally under a stereo-microscope before opening the visceral cavity. Fish were sacrificed by puncturing the brain region and the gills of each fish were removed and placed in vials containing hot 4–5% formalin solution to fix any of the ectoparasites that might be present and labeled with data of each collection site. The internal cavity of each fish was exposed by an incision made along the venter from the anus to mouth. The entire alimentary canal was removed; the interior of the gut was thoroughly examined in situ, then placed in a Petri dish containing hot formalin solution 4–5%, where it was searched for monogeneans (Salgado-Maldonado et al. 2014). Subsequently, all monogeneans specimens were isolated and stained with Gomori’s trichrome and mounted in Canada balsam. In addition, some specimens were mounted in a mixture of lactic-acid (LA) and glycerin- ammonium picrate (GAP) and then remounted in Canada balsam as permanent preparations (Mendoza-Franco et al. 2013). Parasite identifications were made using a Leica microscope DM2500 with Nomarski interference contrast and based on descriptions provided in the following references: García-Vásquez et al. 2007, 2015, Jogunoori et al. 2004, Kritsky et al. 1989, Lim 1996, Mendoza-Palmero et al. 2012, Pariselle and Euzet 1995, Yamaguti 1963. Reference specimens were deposited in the National Helminthological Collection of Mexico (). Prevalence (percent of hosts infected), mean abundance (mean number of parasites per examined fish), and intensity range for each monogenean species follows Bush et al. (1997). Host species and common names follow those in the FishBase (Froese and Pauly 2017).

Results

A total of 365 fish specimens of 13 species belonging to 7 families was examined for monogeneans: , , , , , , and . Twenty-nine monogenean species infecting gills and/or stomachs were identified from hosts species of all families mentioned above from a total of 31 Aquaculture Production Units (APU) from different municipalities located in the state of Morelos (see Table 1 and Figure 1). The prevalence, mean abundance, and mean intensity of infections at each APU of individual species from different hosts are provided in Tables 2–4.

Table 1.

Ecto- and endo-parasitic monogeneans () on cultured exotic fish from several Aquaculture Production Units (APU) in the state of Morelos, South-Central Mexico.

Host species/Family	Monogeneans/CNHE	APU	Municipalities
Oreochromisniloticus (Cichlidae)	Cichlidogyrussclerosus† /10743	Acuícola Jaloxtoc El Cifón 7 Hermanos La cascada Acuícola Ayala Maricultura Argos	Ayala Zacatepec Cuautla Tlaltizapan Ayala Zacatepec
	Cichlidogyrusthurstonae† /10744	La Cascada	Tlaltizapan
	Cichlidogyrustilapiae† /10745	Acuícola Ayala	Ayala
		Maricultura Argos	Zacatepec
Oreochromis niloticus	*Cichlidogyrus sp. 1 † /10746 *Cichlidogyrus sp. 2 † /10747	Acuícola Ayala	Ayala
Hemichromis sp.	Enterogyruscoronatus‡ /10748	Maleny	Zacatepec
Oreochromis niloticus	Enterogyrusmalmbergi‡ /10749-10750	Acuícola Ayala Adilene Marisol San Tilapia Acuícola de Jiutepec Pliego	Ayala Ayala Tlaltizapan Juitipec Ayala
Oreochromis sp.	Enterogyrusmalmbergi‡ /10751	San Tilapia La buena Fortuna	Tlaltizapan Jojutla
Oreochromis niloticus	Gyrodactyluscichlidarum£ /10756	Acuícola Jaloxtoc Centro Zacatepec	Ayala Zacatepec
	Gyrodactylusyacatli£ /10757	Centro Zacatepec	Zacatepec
Pterophyllum scalare	*Gusseviaspiralocirra† /10752 *Sciadicleithrumiphthimum† /10753 *Sciadicleithrum sp. † /10754	Jesús Madariaga	Zacatepec
		El Chino	Juitepec
		Olascoaga	Juitepec
Oreochromis niloticus	Scutogyruslongicornis† /10755	La Cascada	Tlaltizapan
Carassiusauratus (Cyprinidae)	*Dactylogyrusbaueri† /10758 *Dactylogyrusformosus† /10759 *Dactylogyrusintermedius† /10760Dactylogyrusvastator† /10761-10762	Centro de acopio La Perla El Invernadero Los Huajes Linda Vista Platanar Grupo Carsal	Tlaltizapan Ayala Ayala Ayala Ayala Ayala
	*Gyrodactyluskobayashii£ /10765-10767	Linda Vista Los Huajes Grupo Carsal El Invernadero	Ayala Ayala Ayala Ayala
Cyprinus carpio	*Dactylogyrusextensus† /10763	Ornapez	Ayala
Ctenopharyngodon idella	*Dactylogyrus sp. † /10764	Centro Zacatepec	Zacatepec
Trichogastertrichopterus (Osphronemidae)	*Trianchoratusacleithrium† /10768	Consorcio Lugo-Galeana Granja Acuícola Foras	Jiutepec Axochiapan
	*Trianchoratustrichogasterium† /10769	Consorcio Lugo-Galeana	Jiutepec
Pangasianodon hypophthalmus (Pangasidae)	*Thaparocleiduscaecus† /10770 *Thaparocleidussiamensis† /10771-10772	Betta Fish Betta Fish La buena Fortuna	Xochitepec Xochitepec Jojutla
	*Dactylogyridae sp. †	La buena Fortuna	Jojutla
Poecilia reticulata (Poeciliidae)	*Gyrodactyluspoeciliae£ /10773	Huertas de Cuatla Exopez Agua Fría	Ayala Tlaltizapan Tlaquiltenengo
Gymnocorymbus ternetzy (Characidae)	*Diaphorocleidusarmillatus† /10774-10775	Aquafish Tropipez	Zacatepec
Hypostomus sp. (Loricariidae)	*Gyrodactylidae sp. £ /10777 *Unilatusunilatus† /10776	Consorcio Lugo-Galeana	Jiutepec
		Consorcio Lugo-Galeana	Jiutepec

* = new record in Mexico. Site of infection on host: † = gills lamellae; ‡ = stomach; £ = fins.

Figure 1.

Map of the state of Morelos, Mexico showing position of each APU: 1 7 Hermanos (2 Acuícola Ayala () 3 Acuícola de Jiutepec () 4 Acuícola Jaloxtoc () 5 Adilene Marisol () 6 Agua Fría () 7 Aquafish () 8 Betta Fish () 9 Centro Zacatepec () 10 Centro de Acopio La Perla () 11 Consorcio Lugo-Galeana () 12 El Chino () 13 El Cifón () 14 El Invernadero () 15 Exopez () 16 Granja Acuícola Foras (); 17. Grupo Carsal () 18 Huertas de Cuatla () 19 Jesús Madariaga () 20 La Buena Fortuna () 21 La Cascada () 22 Linda Vista () 23 Los Huajes () 24 Maleny () 25 Maricultura Argos () 26 Olascoaga () 27 Ornapez () 28 Platanar () 29 Pliego () 30 San Tilapia () 31 Tropipez ().

Table 2.

Parameters of infection of monogeneans on cichlids (APU: Aquaculture Production Unit; P%: Prevalence; MA: mean abundance; RI: range of infection; MI: mean intensity; IH: infected hosts).

APU	Hosts	Monogeneans	Inds.	P%	MA	RI	MI	IH
Maleny	Hemichromis sp.	Enterogyrus coronatus	36	50	5.14	1–13	3.6	10/20
7 hermanos	Oreochromis niloticus	Cichlidogyrus sclerosus	12	57	1.71	2–4	3.0	4/7
Acuícola de Jiutepec	Oreochromis niloticus	Enterogyrus malmbergi	18	50	2.57	2–5	3.6	5/10
Acuícola Jaloxtoc	Oreochromis niloticus	Gyrodactylus cichlidarum	18	20	2.57	18	18	1/5
	Oreochromis niloticus	Cichlidogyrus sclerosus	13	100	2.60	1–7	2.6	5/5
Adilene Marisol	Oreochromis niloticus	Enterogyrus malmbergi	53	100	7.57	2–13	5.3	10/10
Centro Zacatepec	Oreochromis niloticus	Gyrodactylus yacatli	15	10	2.14	15	15	1/10
El Cifón	Oreochromis niloticus	Cichlidogyrus sclerosus	7	40	1.00	3–4	3.5	2/5
Acuícola Ayala	Oreochromis niloticus	Cichlidogyrus tilapiae	159	100	22.71	3–37	15.9	10/10
	Oreochromis niloticus	Enterogyrus malmbergi	6	50	0.86	1–2	1.2	5/10
	Oreochromis niloticus	Enterogyrus malmbergi	1	10	0.14	1	1.0	1/10
Pliego	Oreochromis niloticus	Enterogyrus malmbergi	2	25	0.29	2	2.0	1/4
San Tilapia	Oreochromis niloticus	Enterogyrus malmbergi	34	100	4.86	1–17	8.5	4/4
	Oreochromis sp.	Enterogyrus malmbergi	23	60	3.29	1–7	3.83	6/10
La Buena Fortuna	Oreochromis sp.	Enterogyrus malmbergi	76	76.9	10.86	2–19	7.6	10/13
Jesús Madariaga	Pterophyllum scalare	Gussevia spiralocirra	5	10	0.71	5	5.0	1/10
El Chino	Pterophyllum scalare	Sciadicleithrum spp.	6	83.3	1.00	1–2	1.2	5/6
Olascoaga	Pterophyllum scalare	Sciadicleithrum sp.	9	75	1.29	1–4	3.0	3/4

Table 4.

Parameters of infection of monogeneans on characids, loricariids, osphronemids, pangasids, and poeciliids (APU: Aquaculture Production Unit; P%: Prevalence; MA: mean abundance; RI: range of infection; MI: mean intensity; IH: infected hosts).

APU	Host	Monogeneans	Inds.	P%	MA	RI	MI	IH
Aquafish	Gymnocorymbus ternetzi	Diaphorocleidus armillatus	131	100	13.1	2–24	13.1	10/10
Tropipez	Gymnocorymbus ternetzi	Diaphorocleidus armillatus	698	100	69.8	7–217	69.8	10/10
Consorcio Lugo-Galeana	Hypostomus sp.	Unilatus unilatus	15	60	1.5	1–11	2.5	6/10
	Hypostomus sp.	Gyrodactylus sp.	14	60	1.4	1–8	2.3	6/10
	Trichogaster trichopterus	Trianchoratus spp.	80	75	20	03–54	26.7	3/4
	Trichogaster trichopterus	Trianchoratus trichogasterium	250	80	25	16–61	31.3	8/10
Granja Acuícola Foras	Trichogaster trichopterus	Trianchoratus trichogasterium	564	90	56.4	1–262	62.7	9/10
Betta fish	Pangasianodon hypophthalmus	Thaparocleidus spp.	536	40	26.8	1–125	67.0	8/20
La Buena Fortuna	Pangasianodon hypophthalmus	Thaparocleidus siamensis	1000	100	200	130–300	200.0	5/5
	Pangasianodon hypophthalmus	Dactylogyridae sp.	10400	100	2080	1000–3000	1733.3	5/5
Exopez	Poecilia reticulata	Gyrodactylus poeciliae	4	33	0.67	2	2.0	2/6
Agua fría	Poecilia reticulata	Gyrodactylus poeciliae	75	90	7.5	1–37	8.3	9/10
Huertas de Cuautla	Poecilia reticulata	Gyrodactylus poeciliae	1	12.5	0.125	1	1.0	1/8

Discussion

Currently, 31 species of exotic monogeneans have been registered in the state of Morelos due to the introduction of their hosts that are cultured either for food or aquariums (present data; Caspeta-Mandujano et al. 2009). This current study on cultured exotic fish species revealed that cichlids (i.e., species of , , and ), harbored the highest number of monogeneans (14 species) followed by cyprinids with seven species of which Gussev, 1955, Kulwieć, 1927, Wegener, 1909, and Hukuda, 1940 are new geographical records in Mexico (see Tables 1 and 3). Despite the great number of parasitological studies on native and/or introduced species of in Mexico (Vidal-Martínez et al. 2001), studies on the parasite fauna of other exotic freshwater fishes, especially on their monogeneans, are relatively scarce. Exceptionally, there have been many reports of species of on species of (often called tilapia) (see Kritsky et al. 1994, Jiménez-García et al. 2001). Even so, intensity of infection is comparatively high as well as the number of new records of these monogeneans, the latter which continues to grow each year (see Table 3, Mendoza-Franco et al. 2015b). In the present study, the angelfish (Schultze) and sp. were studied for the first time and are shown to be parasitized with Kohn & Paperna, 1964, Kritsky, Thatcher & Boeger, 1989, sp. (new geographical records), and Pariselle, Lambert & Euzet, 1991.

Table 3.

Parameters of infection of monogeneans on hosts of the (APU: Aquaculture Production Unit; P%: Prevalence; MA: mean abundance; RI: range of infection; MI: mean intensity; IH: infected hosts).

APU	Hosts	Monogeneans	Inds.	P%	MA	RI	MI	IH
Consorcio Lugo-Galeana	Carassius auratus	Dactylogyrus sp.	520	100	52.0	13–154	86.7	10/10
El invernadero	Carassius auratus	Gyrodactylus kobayashii	525	100	87.5	5–314	87.5	6/6
	Carassius auratus	Dactylogyrus formosus	1	17	0.17	1–8	1.0	1/6
Grupo Carsal	Carassius auratus	Gyrodactylus kobayashii	28	100	20	0.3–54	26.7	3/3
	Carassius auratus	Dactylogyrus vastator	5	33	1.7	5	5.0	1/3
Linda vista	Carassius auratus	Gyrodactylus kobayashii	12	20	1.2	2–10	6	2/10
	Carassius auratus	Dactylogyrus vastator	3	10	0.3	3	3.0	1/10
Los Huajes	Carassius auratus	Dactylogyrus baueri	1	20	0.2	1	1.0	5/5
	Carassius auratus	Dactylogyrus spp.	38	100	7.6	2–25	7.6	5/5
	Carassius auratus	Gyrodactylus kobayashii	102	100	20.4	2–58	20.4	5/5
Centro Zacatepec	Ctenopharyngodon idella	Dactylogyrus sp.	100	14	14.3	100	100.0	1/7
Ornapez	Cyprinus carpio	Dactylogyrus extensus	5	20	0.5	2–3	2.5	2/10

Monogeneans usually exhibit high host specificity in comparison with other parasite groups, parasitizing a single or few closely related host species. The only zoogeographic range expansion of exotic monogeneans on native hosts is the discovery of species of and from tilapia on native cichlids and poeciliids, respectively, in natural environments of Mexico (Jiménez-García et al. 2001, García-Vásquez et al. 2007, 2017). The present study revealed the highest intensity of infection with (identified as a tilapia pathogen by García-Vásquez et al. 2017) and spp. on spp. (see Table 2). Therefore, preventing escape of these tilapia from culture systems due to their monogeneans’ ability to infest and persist on other non- or related wild fish is urgently required. Another example of the persistence of monogeneans is seen with the dactylogyrid Jogunoori, Kritsky & Venkatanarasaiah 2004. This monogenean was originally described from fishes introduced to India via the aquarium trade. Its type host, the green swordtail (Heckel) (), is naturally distributed in southern Mexico and Central America, where the native profundulid (Günther) also hosts . The problem is that has been artificially introduced along with to other hydrological systems such as India and northern Mexico (Jogunoori et al. 2004, Mendoza-Palmero and Aguilar-Aguilar 2008, Mendoza-Franco et al. 2015a) from which other cyprinodontiform hosts could potentially become infected with this parasite. Additionally, in the present study the black tetra (Boulenger) () was studied for the first time and is revealed to be highly infested with Jogunoori, Kritsky & Venkatanarasaiah, 2004 () (see Table 4). is native to South America and has been introduced via the aquarium trade to India and Mexico. Currently, there are nine species of dispersed on native bryconid and characid () hosts in the neotropics (South and Central America) (Santos et al. 2018). The transfer and/or evidence of extensive cryptic speciation of other monogenean groups from exotic to native or vice versa on closely related hosts in Mexico remains unknown, but that potential exists.

Similarly to the introduced tilapia in Mexico, cyprinids (i.e., ) are also widely distributed in the country including habitats located within areas protected for conservation (see Salgado Maldonado et al. 2014). These fishes were introduced to Central America (i.e., Mexico and Honduras) for aquaculture purposes from 1965-1980s (Salgado-Maldonado and Rubio-Godoy 2014, Salgado-Maldonado et al. 2015) and the presence of species of and (see Table 1, 3) in Morelos might be originally related to these introductions. Poeciliids (known as guppies, mollies, platies, and swordtails) have been studied for ectoparasitic monogeneans in Mexico and mainly gyrodactylids have been reported on the skin and/or gills on these fishes (García-Vásquez et al. 2015). Currently, there are 11 gyrodactylid species described and/or reported from poeciliids. Only species of () have been reported on the gills of the poeciliids of the two-spot livebearers (Heckel), , and (Regan) from Mexico and Panama (Mendoza-Franco et al. 2015). In the present study, Harris & Cable, 2000 was found for the first time on the guppy Peters from Mexico (see Tables 1, 4). This monogenean species has been reported on (Steindachner) and from their natural ranges of distribution (Venezuela and Trinidad, respectively). Among all species of mentioned above, only Turnbull, 1956 and Harris, 1986 have been reported on six poeciliid host species ( Girard, Valenciennes, , , sp., and ) from Mexico, Canada, Costa Rica, Peru, Trinidad, Australia, and Singapore (see García-Vásquez et al. 2015). Given the low host specificity of both gyrodactylid species and the invasive characteristic of poeciliids, the potential transfer of these gyrodactylids to native poeciliids and other ecologically-associated hosts in Mexico is high (see García-Vásquez et al. 2017, Mendoza-Franco et al. 2015).

The African tilapia () and the Asian catfish () are both freshwater whitefish aquaculture species that potentially compete for similar markets. In fact, in 2013 Mexico was recognized as the second largest importer of pangasius fillet in the world (Martínez et al. 2016). No analysis concerning the environmental impact of the introduction of these latter fishes and their parasites from Vietnam into Mexican aquaculture and/or in wild habitats (Martínez et al. 2016) has been made. (Sauvage) was studied for the first time in the present study and it revealed to be parasitized with three monogenean species: (Mizelle & Kritsky, 1969) Lim 1996, (Lim 1990) Lim, 1996, and sp. (Table 4). Finally, Loricariids, otherwise known as plecos (species of ) are very popular ornamental freshwater fish naturally found in tropical South America, Panama, and Costa Rica. In Mexico, (L.) was introduced into the Balsas Basin (see geographic position in Figure 1) to control macrophytes and algae, and are now established in multiple water bodies (Ramírez-Morales and Ayala-Pérez 2009). The only report of a gill monogenean species on an introduced pleco to Mexico is that of sp. () on the Amazon sailfin Castelnau from the Reserva de la Biosfera Montes Azules (BRMA) in the state of Chiapas (Mendoza-Franco et al. 2012). The present study provides two new monogenean records for Mexico, sp. and , the latter belonging to the which was previously reported on the snow pleco Eigenmann and Kennedy and on sp., from Brazil and Peru, respectively (Mendoza-Palmero et al. 2012).

The fish examined in the present study are ornamental and/or for food production that are commercialized in Mexico. Results clearly show that importation of these fish can carry several monogeneans, both ecto- and endo-parasitic species, which could infect other related fish in systems they invade. Therefore, determining the occurrence of parasitic species will help provide better aquaculture conditions and will help to solve some of the problems faced by fish farmers. In the literature, there are a number of reports dealing with the introduction of parasites by ornamental fish from which the consequences of parasite introduction can be detrimental to native fish. For example, epizootics that may lead to extensive mortality (i.e., on cyprinids, see Cone 1999) as shown for several species of monogeneans introduced into farms or aquariums, and from there to natural populations (Bakke et al. 2002, 2007; García-Vásquez et al. 2017). In addition to the identification of invasive host fish species, it is recommended that all freshwater fish imported into the country for food (farmed) or ornamental purposes must comply, at least, with quarantine regulations.