Hostname: page-component-7b9c58cd5d-dkgms Total loading time: 0 Render date: 2025-03-14T23:52:25.033Z Has data issue: false hasContentIssue false

Helminth parasites of finfish commercial aquaculture in Latin America

Published online by Cambridge University Press:  15 December 2016

L.C. Soler-Jiménez
Affiliation:
Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Km 6 Carretera Antigua a Progreso, Cordemex, Mérida, Yucatán 97310, México
A.I. Paredes-Trujillo
Affiliation:
Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Km 6 Carretera Antigua a Progreso, Cordemex, Mérida, Yucatán 97310, México
V.M. Vidal-Martínez*
Affiliation:
Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Km 6 Carretera Antigua a Progreso, Cordemex, Mérida, Yucatán 97310, México
Rights & Permissions [Opens in a new window]

Abstract

Latin America has tripled production by aquaculture up to 78 million tonnes in the past 20 years. However, one of the problems that aquaculture is facing is the presence of helminth parasites and the diseases caused by them in the region. In this review we have collected all the available information on helminths affecting commercial aquaculture in Latin America and the Caribbean (LAC), emphasizing those causing serious economic losses. Monogeneans are by far the most common and aggressive parasites affecting farmed fish in LAC. They have been recognized as serious pathogens in intensive fish culture because they reach high levels of infection rapidly, and can infect other phylogenetically related fish species. The next most important group comprises the larval stages of digeneans (metacercariae) such as Diplostomum sp. and Centrocestus formosanus, which cause serious damage to farmed fish. Since LAC aquaculture has been based mainly on exotic species (tilapia, salmon, trout and carp), most of their parasites have been brought into the region together with the fish for aquaculture. Recently, one of us (A.I.P.-T.) has suggested that monogeneans, which have generally been considered to be harmless, can produce serious effects on the growth of cultured Nile tilapia. Therefore, the introduction of fish together with their ‘harmless’ parasites into new sites, regions or countries in LAC should be considered a breakdown of biosecurity in those countries involved. Therefore, the application of quarantine procedures and preventive therapeutic treatments should be considered before allowing these introductions into a country.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

Introduction

Aquaculture has been experiencing continuous expansion in many countries worldwide and provides a livelihood for 8% of the world's population (540 million people) (FAO, 2014). It is estimated that world aquaculture production doubled from 32.4 million tonnes in 2000 to 66.6 million tonnes in 2012 (FAO, 2014). The fastest annual growth rate in production was observed in Africa (11.7%) and Latin America and the Caribbean (LAC) (10%). For LAC, the economic contribution of aquaculture has grown substantially in the past 10 years, with employment of more than 200,000 people directly, and about 500,000 indirectly (FIS México, 2016). While Chile, Brazil, Ecuador and Mexico account for more than 80% of the regional aquaculture volume, this activity occurs on different scales in almost every country of Latin America. With the exception of Penaeus vannamei in Mexico, most of the species under aquaculture conditions in LAC are exotic: salmonids (trout and salmon) in nine countries of the region, marine shrimp in 18 countries and tilapia in 20 countries (FAO, 2014).

An important limitation to the development of commercial aquaculture in LAC in recent decades has been the emergence of infectious diseases. Diseases of bacterial (Streptococcus iniae, Pseudomonas sp., Aeromonas sp.) and viral (Iridoviridae, Orthomixoviridae, Rhabdoviridae, Alloherpesviridae) origin are widely distributed and cause high mortalities, producing serious economic losses in aquaculture (Conroy, Reference Conroy2004; OIE, 2015). For example, the bacterium Francisella sp. in cultured tilapia has caused losses of US$2.5 million in Costa Rica and is currently present in Mexico, Brazil and Guatemala, with mortality of up to 85% in juveniles (Conroy, Reference Conroy2004). Likewise, parasites are often associated with important economic losses in aquaculture. For example, Bothriocephalus acheilognathi is a pathogenic helminth that causes serious mortalities among juvenile fish in culture conditions and in wild populations (Salgado-Maldonado et al., Reference Salgado-Maldonado, Guillen-Hernández and Osorio-Sarabia1986; Salgado-Maldonado & Pineda-López, Reference Salgado-Maldonado and Pineda-López2003); in fact, due to its pathogenicity it is considered a threat to endemic fish in Mexico (Velázquez-Velázquez et al., Reference Velázquez-Velázquez, González-Solis and Salgado-Maldonado2011).

Helminths are frequently neglected as causative agents of fish diseases. Indeed, several fish farmers frequently believed that these parasites are harmless (Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). However, under aquaculture conditions such as low water quality, high fish density and extreme environmental variables (e.g. high ammonia concentration, high temperature) these parasites can cause disease (e.g. Gonzáles-Fernández, Reference Gonzáles-Fernández2012a; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). The spread and establishment of parasitic helminths may have detrimental health consequences when present in high numbers within a cultured population with deficient management practices and a lack of biosecurity plans. Therefore, knowledge of the potential risks that helminths represent to farmed fish can be useful for designing appropriate contingency plans and management strategies (Bondad-Reantaso et al., Reference Bondad-Reantaso, Subasinghe, Arthur, Ogawa, Chinabut, Adlard, Tan and Shariff2005).

In this review, our main objective has been to present the extant information on helminths producing negative effects (e.g. histological or physiological) in finfish under aquaculture conditions. However, we have also included helminths that are apparently harmless, but that we consider potentially dangerous in view of the intensive aquaculture conditions that will be developed in the near future in LAC. For this purpose, this article is divided into five groups of cultured fish arranged according to their economic importance in LAC (salmonids, tilapia, carp, native fish and ornamental fish).

Salmonids

In Latin America, salmonid production is one of the most important aquaculture activities, with a sustained economic growth (586,289 tonnes in 2004) and is highly profitable (Rojas & Wadsworth, Reference Rojas, Wadsworth, Halwart, Soto and Arthur2005). Studies on parasites of salmonids have focused primarily on those that produce diseases in commercial fish. Most of the diseases in salmonids have a viral origin in Latin America (www.oie.int/es/). Consequently, it is difficult to determine the relative impact of helminth infections on salmonid farming (Shinn et al., Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015). Probable reasons for the scarcity of information on helminths include the difficulties in identifying parasites accurately at the farm level and poor record keeping. Table 1 shows the helminth species recorded from salmonid species farmed in Latin America.

Table 1. Helminth species recorded from salmonid species farmed in Latin America.

Monogeneans

There are records of Gyrodactylus sp. in Oncorhynchus mykiss for Mexico and Colombia with relatively high infection parameters (mean abundance 100 ± 87 parasites/host) (Salas-Benavides et al., Reference Salas-Benavides, López-Macías, Ortega-Salas and Gómez-Nieves2015). The clinical signs of Gyrodactylus sp. included irritation, bleeding and erosion of the gill tissue. These reports correspond to isolated findings and were not associated with mortality of farmed fish. However, further research is required to understand the presence of these metazoan parasites in farmed salmonids. Gyrodactylus salmonis was reported by Rubio-Godoy et al. (Reference Rubio-Godoy, Paladini, Freeman, García-Vásquez and Shinn2012a) from O. mykiss in Veracruz, Mexico. However, there are no reports of fish morbidity or mortality associated with gyrodactylid infection in rainbow trout farms in Veracruz, which would suggest a stable host–parasite interaction (Rubio-Godoy et al., Reference Rubio-Godoy, Paladini, Freeman, García-Vásquez and Shinn2012a).

Digeneans

Larval forms of diplostomids affecting the brain (Austrodiplostomum mordax) and eyes (Diplostomum sp.) have been reported in salmonids in LAC. Records in Argentina and Colombia indicate that diplostomiasis is widely distributed in natural environments (Semenas, Reference Semenas1998; Salas-Benavides et al., Reference Salas-Benavides, López-Macías, Ortega-Salas and Gómez-Nieves2015). The larval genus Diplostomum includes metacercariae in the tegument, which generates black spots on the skin, but the most common infections are caused by mesocercariae in the lens, causing oedema, congestion, leucocyte infiltration and bleeding. This damage affects the choroid and iris, causing muscular and retinal necrosis, and finally partial or total blindness of the eye, which forces fish to swim near the surface, making them easy prey for predatory birds.

Nematodes

Hysterothylacium is a nematode genus that has been suggested to affect the health of salmonids in production systems. This genus was first reported in marine cage farms of Chilean salmonids by Carvajal & González (Reference Carvajal and González1990). This anisakid nematode was present in the digestive tract of several native fishes (Fernández, Reference Fernández1985) and has been transmitted to the salmonids introduced in Chile for commercial aquaculture. Larvae and adults of Hysterothylacium aduncum have been recorded in Oncorhynchus kisutch, O. mykiss, Salmo salar and Oncorhynchus tshawytscha reared in floating cages in Chile and Argentina (Carvajal & Gonzalez, Reference Carvajal and González1995) and in S. salar from localities close to Puerto Montt (Sepulveda et al., Reference Sepulveda, Marin and Carvajala2004). The effect of Hysterothylacium spp. on salmonids has been poorly investigated, but published records indicate that H. aduncum causes mortality in juvenile fish (Balbuena et al., Reference Balbuena, Karlsbakk and Kvenseth2000) and heavy Hysterothylacium bidentatum infections induce digestive tract obstruction (Molnár et al., Reference Molnár, Buchmann, Székely and Molnár2006). It has also been reported that H. aduncum represents a zoonotic risk, due to reports of human infection in Japan (Yagi et al., Reference Yagi, Nagasawa, Ishikura, Nakagawa, Sato and Kikuchi1996).

Cestodes

Diphyllobothrium sp. plerocercoids have been isolated from the viscera of one specimen of O. mykiss reared in the south of Chile (Torres et al., Reference Torres, Gesche, Montefuso, Miranda, Dietz and Huijse1998). Since most salmonid production is undertaken in floating cages, some of these parasites are particularly important helminth species because of their zoonotic risk. Additionally, since these parasites complete their life cycles in natural environments, it would be expected that under aquaculture conditions, due to the high fish density in floating cages, the prevalence and abundance of this parasite would be higher. The tapeworm Diphyllobothrium denditricum has been detected in wild salmonids (Salmon coho and O. kisutch) introduced into Chile (Torres et al., Reference Torres, Gesche, Montefuso, Miranda, Dietz and Huijse1998). Previous research suggests that diphyllobothriasis and other parasitic infestations in wild fish are potential risks to salmon farming in Chile (Torres et al., Reference Torres, Gesche, Montefuso, Miranda, Dietz and Huijse1998), as proven in the northern hemisphere (Rahkonen et al., Reference Rahkonen, Aalto, Koski, Särkkä and Juntunen1996; Karasev et al., Reference Karasev, Mitenev and Kalinina1997). Furthermore, the larval stages of the tapeworm D. dendriticum and the nematode Contracaecum sp. are considered to be of zoonotic importance, since the consumption of salmon meat is the entry route to humans (Von Bonsdorff, Reference Von Bonsdorff1977).

Tilapia

The state of development of aquaculture in LAC suggests that several countries (Brazil, Colombia, Costa Rica, Ecuador and Mexico) predominate in the aquaculture of these African cichlids (FAO, 2014), with Jamaica being one of the largest producers of high-quality red tilapia (FAO, 2014). In many Latin American countries, tilapia was introduced during the 1960s, but this biotechnology was not developed as a commercial activity until the 1980s. Commercial production began in Jamaica in 1983, spread to Colombia, and shortly after to Costa Rica, Brazil, Ecuador, Honduras, Nicaragua and Venezuela (Castillo-Campo, Reference Castillo-Campo, Contreras-Sánchez and Fitzsimmons2006). Currently, tilapia is cultured in 20 out of 26 Latin America countries. With the intensification of tilapia farming, parasitic diseases began to appear, posing important limitations to the development of aquaculture in LAC. Table 2 shows the helminth species recorded from tilapia species farmed in LAC.

Table 2. Helminth species recorded from farmed tilapia species in Latin America.

Monogeneans

Members of the families Gyrodactylidae and Dactylogyridae are the most important parasites in tilapia aquaculture. Species of the family Capsalidae are also important parasites on tilapia cultured in seawater (Conroy & Conroy, Reference Conroy and Conroy2008; Rubio-Godoy et al. Reference Rubio-Godoy, Montiel-Leyva and Martínez-Hernández2011; Shinn et al., Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015). Several authors have shown that the main helminth species affecting fish health in intensive closed-system culture are monogeneans. These helminths are often present in the sex-reversal process, where their infestation is favoured by their direct life cycle at high fish densities (Conroy, Reference Conroy2001). For example, in Brazil, Martins et al. (Reference Ghiraldelli, Martins, Yamashita and Jeronimo2006) suggested that monogeneans are the ectoparasites responsible for the most important parasitic disease among farmed tilapia.

Overall, gyrodactylids are known to be very aggressive, tending to be extremely pathogenic to tilapia, especially to larvae and small fish at high population densities and intensive culture conditions. Infestations occur mainly on the body, rarely on the gills, and produce excessive secretion of mucus and epithelial cell proliferation. This leads to erosion of the skin surface and the possibility of secondary infections caused by bacteria and fungi. Due to their viviparous reproductive strategy, gyrodactylids are able to achieve high infestation levels in very short periods of time (Flores-Crespo & Flores-Crespo, Reference Flores-Crespo and Flores-Crespo2003; Conroy & Conroy, Reference Conroy and Conroy2008). Gyrodactylus cichlidarum is widely distributed in Latin America (Brazil, Colombia, Ecuador, Honduras, Mexico, Puerto Rico) and has been detected in Nile tilapia (Oreochromis niloticus), blue tilapia (O. aureus), Mozambique tilapia (O. mossambicus) and hybrid red tilapia (O. mossambicus × O. urolepis) (Bunkley-Williams & Williams, Reference Bunkley-Williams and Williams1994; Conroy, Reference Conroy2001; Jiménez, Reference Jiménez2007; García-Vásquez et al., Reference García-Vásquez, Hansen, Christison, Bron and Shinn2011; Lacerda et al., Reference Lacerda, Yamada, Antonucci, Tavares-Dias, Pavanelli, Takemoto and Eiras2013; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Gyrodactylus cichlidarum is especially harmful to tilapia kept in ponds, attacking mainly the skin and fins (García-Vázquez et al., Reference Rubio-Godoy, Montiel-Leyva and Martínez-Hernández2011; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Gyrodactylus niloticus has been recorded from Mexico on O. aureus, O. mossambicus and O. niloticus (Hernández-Martínez, Reference Hernández-Martínez1992; López-Jiménez, Reference López-Jiménez2001; Salgado-Maldonado et al., Reference Salgado-Maldonado, Pineda-López, García-Magaña, López-Jiménez, Vidal-Martínez, Aguirre-Macedo, Bueno-Soria, Santiago-Fragoso and Álvarez2005). However, García-Vásquez et al. (Reference García-Vásquez, Hansen, Christison, Rubio-Godoy, Bron and Shinn2010) considered G. niloticus to be synonymous with G. cichlidarum. Gyrodactylus yacatli was originally described by García-Vásquez et al. (Reference García-Vásquez, Hansen, Christison, Bron and Shinn2011) from O. niloticus and, for LAC, this species has only been reported from Mexico (García-Vásquez et al., Reference García-Vásquez, Hansen, Christison, Bron and Shinn2011; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014).

Dactylogyrids are highly pathogenic to their tilapia hosts, especially when they are present in high amounts. Infestations are mainly on the gills, where they give rise to marked hyperplasia and other proliferative changes in the epithelium, which leads to respiratory problems and mortality (Del Río-Zaragoza et al., Reference Del Río-Zaragoza, Fajer-Ávila and Almazán-Rueda2010). The genus Cichlidogyrus was first described by Paperna (Reference Paperna1960), with the type species Cichlidogyrus arthracanthus collected in Israel from the wild host species Tilapia zillii. This genus was reported from cultured tilapia in Africa by Douëllou (Reference Douëllou1993). Cichlidogyrus spp. were introduced into America from Africa along with their host in the early 1980s (Kritsky & Thatcher, Reference Kritsky and Thatcher1974; Arredondo-Figueroa, Reference Arredondo-Figueroa1983; Lazaro-Chávez, Reference Lazaro-Chávez1985; Prieto et al., Reference Prieto, Fajer and Vinjoy1985; Kritsky et al., Reference Kritsky, Vidal-Martínez and Rodríguez-Canul1994). In Cuba and Colombia massive infections of cultured tilapia by Cichlidogyrus spp. have been reported (Sánchez-Ramirez et al., Reference Sánchez-Ramirez, Vidal-Martínez, Aguirre-Macedo, Rodriguez-Canul and Gold-Bouchot2007). In Mexico, members of this genus have been reported with high prevalence in O. niloticus and O. mossambicus in Campeche, Veracruz and Yucatán (Vidal-Martínez et al., Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001; Aguirre-Fey et al., Reference Aguirre-Fey, Benítez-Villa, Pérez-Ponce de León and Rubio-Godoy2015; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Little is known about the biology of Cichlidogyrus, but apparently there is a link between poor water quality and high prevalence of this monogenean in aquaculture conditions.

The most widely distributed species of Cichlidogyrus in Latin America are Cichlidogyrus sclerosus and C. tilapiae, first recorded in Colombia, Mexico (Kritsky & Thatcher, Reference Kritsky and Thatcher1974; Kritsky et al., Reference Kritsky, Vidal-Martínez and Rodríguez-Canul1994) and Cuba (Prieto et al., Reference Prieto, Fajer and Vinjoy1985). These species have been recorded infecting various species of tilapia and their hybrids, including blue tilapia (O. aureus), Mozambique tilapia (O. mossambicus), Nile tilapia (O. niloticus) and red tilapia (O. urolepis) (Bunkley-Williams & Williams, Reference Bunkley-Williams and Williams1994; Santamaría & Medina, Reference Santamaría and Medina2000; Jiménez-García et al., Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001; Flores-Crespo & Flores-Crespo, Reference Flores-Crespo and Flores-Crespo2003; Ghiraldelli et al., Reference Martins, Ghiraldelli, Azevedo and Silva-Souza2006; Salgado-Maldonado, Reference Salgado-Maldonado2006; Lizama et al., Reference Lizama, Takemoto, Rizani-Paiva, Ayroza and Pavanelli2007a; Jeronimo et al., Reference Jeronimo, Speck, Cechinel, Gonçalves and Martins2011; Pantoja et al., Reference Pantoja, Neves, Dias, Marinho, Montagner and Tavares-Dias2012; Lacerda et al., Reference Lacerda, Yamada, Antonucci, Tavares-Dias, Pavanelli, Takemoto and Eiras2013; Bittencourt et al., Reference Bittencourt, Pinheiro, Cárdenas, Fernandes and Tavares-Dias2014; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014; Aguirre-Fey et al., Reference Aguirre-Fey, Benítez-Villa, Pérez-Ponce de León and Rubio-Godoy2015; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Infections with C. sclerosus have an important effect on the growth rate and relative condition factor of their hosts, which could have an economic effect on tilapia farmers (Sandoval-Gío et al., Reference Sandoval-Gío, Rodríguez-Canul and Vidal-Martínez2008; Le Roux, Reference Le Roux2010; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Sánchez-Ramirez et al. (Reference Sánchez-Ramirez, Vidal-Martínez, Aguirre-Macedo, Rodriguez-Canul and Gold-Bouchot2007) reported outbreaks of C. sclerosus during the winter months in O. niloticus under experimental culture in Yucatán, Mexico; apparently, the fish had a weak immune response in cold weather, which in turn favoured a high prevalence of this monogenean. The same epizootic pattern was reported by Aguirre-Fey et al. (Reference Aguirre-Fey, Benítez-Villa, Pérez-Ponce de León and Rubio-Godoy2015), who found a significant negative correlation between water temperature and parasite abundance. Pantoja et al. (Reference Pantoja, Neves, Dias, Marinho, Montagner and Tavares-Dias2012) recorded a prevalence of C. tilapiae of more than 90% in Nile tilapia farms in Amapá State, Brazil. Likewise, Salgado-Maldonado & Rubio-Godoy (Reference Salgado-Maldonado and Rubio-Godoy2014) considered that C. sclerosus is the most common monogenean in tilapia cultured in Mexico, and it has also been identified in different species of native cichlid fishes (Jiménez-García et al., Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001).

In a study of farmed O. niloticus from the Chavantes reservoir in Brazil, Martins (Reference Martins1998) showed that the dactylogyrids Cichlidogyrus halli and Scutogyrus longicornis were the most abundant monogeneans in the gills of this fish species. In cases of high infection intensity, these monogeneans can cause mortalities, especially in small fish (Jeronimo, Reference Jeronimo2009). Cichlidogyrus dossoui has been recorded from Oreochromis spp. cultured in Mexico, and has detrimental effects on the host (Aguirre-Fey et al., Reference Aguirre-Fey, Benítez-Villa, Pérez-Ponce de León and Rubio-Godoy2015; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). In addition, Roche et al. (Reference Roche, Leung, Franco and Torchin2010) reported the presence of C. dossoui on wild O. niloticus collected in Panama.

Jiménez-García et al. (Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001) first documented that O. aureus is also parasitized by the native monogenean Sciadicleithrum bravohollisae. This species was previously considered to be specific to American cichlids (Kritsky et al., Reference Kritsky, Vidal-Martínez and Rodríguez-Canul1994; Salgado-Maldonado et al., Reference Salgado-Maldonado, Pineda-López, Vidal-Martínez and Kennedy1997). The lack of a co-evolutionary history may often render invasive species non-competent hosts, and thus acquisition of native parasite species may not take place. However, this does not seem to be the case here, because both introduced tilapia and American native cichlids are phylogenetically related (Cichlidae) and thus direct transmission of this monogenean to the non-native hosts is the most probable explanation for this transfer.

Neobenedenia melleni has a negative impact on tilapia aquaculture in both brackish and marine waters. Khalil et al. (Reference Khalil, Robertson and Hall1988) and Robinson et al. (Reference Robinson, Khalil, Hall and Steele1992) reported problems caused by ‘Benedenia sp.’ (= N. melleni) in coastal marine aquaculture involving hybrid red tilapia (O. mossambicus × O. aureus) in southern Jamaica. Bunkley-Williams & Williams (1995) also found large amounts of N. melleni in blue tilapia (O. aureus), Mozambique tilapia (O. mossambicus) and hybrid red tilapia (O. mossambicus × O. urolepis) cultured in Puerto Rico and other areas of the Caribbean. They suggested that, as exotic species, these fishes do not have natural resistance against this monogenean species. High mortalities can occur in a very short time after the initial infestation. This was verified experimentally by Rubio-Godoy et al. (Reference Rubio-Godoy, Montiel-Leyva and Martínez-Hernández2011), who exposed O. mossambicus and Pargo-UNAM (a synthetic hybrid whose genetic composition is 50% Florida red tilapia, 25% Rocky Mountain tilapia, and 25% red variant O. niloticus) to seawater collected at Veracruz on the Gulf of Mexico. Both tilapia types became infected by Neobenedenia sp., and most of the fish died within a fortnight following exposure. Kaneko et al. (Reference Kaneko, Yamada, Brock and Nakamura1988) reported serious infections of N. melleni in Mozambique tilapia (O. mossambicus) cultured in floating cages in the coastal area of Hawaii.

Digeneans

The species of the genus Diplostomum causing problems in cultured tilapia include D. compactum and D. spathaceum. However, both species are extremely difficult to distinguish from each other morphologically (Aguirre-Macedo, pers. com.). Nevertheless, since D. compactum is the most frequently reported species in Latin America (Conroy & Conroy, Reference Conroy and Conroy2008), we will focus on it from now on. Metacercariae of D. compactum have been reported from the lens, retina, brain and vitreous humour, producing a condition known as ‘eye fluke’, ‘cataract’ or ‘parasitic blindness’ (Ostrowski de Núñez, Reference Ostrowski de Núñez1982). Fish infected with D. compactum have impaired vision, which decreases their capacity to look for food normally and consequently they do not grow properly. These infected fish also tend to swim near the water surface, which is an ideal situation for predators such as fish-eating birds (Conroy & Conroy, Reference Conroy and Conroy2008).

Diplostomosis is widely distributed in cichlids and other native fish species in fresh waters in Mexico and Central and South America and has been reported to cause disease problems in some native species (Jiménez-García et al., Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001). García et al. (Reference García, Osorio-Sarabia and Constantino1993) described the histological alterations caused by D. compactum in the ocular globes, vitreous humour and brain of O. aureus and O. mossambicus, including corneal and conjuctival lesions, optic neuritis, iridocyclitis, eosinophilic infiltration, front and rear uveitis and cataracts. In the brain, histological lesions include multifocal gliosis, eosinophilic meningitis, spongiosis and parasitic cyst in the telencephalon. Pineda-López (Reference Pineda-López1985) reported significant mortalities in farmed tilapia in Chiapas, Mexico as a result of diplostomatosis caused by D. compactum; they also mentioned that in most fish metacercariae were present in both eyes. González & González (Reference González and González1981) studied the effects of D. compactum metacercariae in native and introduced species of cichlids in Lake Valencia, Venezuela, finding between one and six metacercariae in each eye. Diplostomum compactum has been described by several authors as a native species of Latin America (Ostrowski de Núñez, Reference Ostrowski de Núñez1982; García et al., Reference García, Osorio-Sarabia and Constantino1993; Conroy, Reference Conroy2001), and for this reason tilapia farmers should consider the mechanical removal of the first intermediate host, Biomphalaria cf. havanensis (Violante-González et al., Reference Violante-González, García-Varela, Rojas-Herrera and Guerrero2009).

Another important larval trematode in tilapia farming is Clinostomum complanatum. This species is present in fish as metacercariae, using them as a second intermediate host (Thatcher, Reference Thatcher1981, Eiras et al., Reference Eiras, Dias, Pavanelli and Machado1999; Sutili et al., Reference Sutili, Gressler and Vilani de Pelegrini2014). The presence of this trematode has been described by several authors in different parts of the world and in different host species (Salgado-Maldonado, Reference Salgado-Maldonado2006), demonstrating that it is a cosmopolitan parasite. Salgado-Maldonado (Reference Salgado-Maldonado2006) generated a helminth parasite checklist in 194 native and 18 introduced freshwater fish species from 30 families from Mexico, and reported that the metacercariae of C. complanatum are present in 12 families and 49 species. These metacercariae, often referred to as ‘yellow grub’ or ‘the yellow spot disease’, infect the skin, muscle, fins, head, viscera and intestine, causing pathologies and changes in the host's behaviour and feeding habits, leading to poor body weight gain and loss of fecundity, and may culminate in death, with economic losses in fish farms (Eiras, Reference Eiras1994; Mitchell et al., Reference Mitchell, Goodwin, Salmon and Brandt2002; Pavanelli et al., Reference Pavanelli, Eiras and Takemoto2002; Vianna et al., Reference Mitchell, Overstreet, Goodwin and Brandt2005; Silva et al., Reference Silva, Monteiro, Doyle, Pedron, Filipetto and Radunz-Neto2008; Sutili et al., Reference Sutili, Gressler and Vilani de Pelegrini2014). In Brazil, C. complanatum has been a subject of study due to the economic losses caused by the poor appearance for fish marketing, due to the presence of yellow cysts under the skin (Thatcher, Reference Thatcher1981; Eiras et al., Reference Eiras, Dias, Pavanelli and Machado1999). García et al. (Reference García, Osorio-Sarabia and Constantino1993) found that the histological alterations produced by the metacercariae of C. complanatum encysted in the epidermis and dorsal fin caused an inflammatory reaction with eosinophilic infiltration in the skin of parasitized fish. In addition to the negative effect of the presence of C. complanatum in aquacultured fish, these metacercariae are potentially transmissible to humans (Dzikowski et al., Reference Dzikowski, Levy, Poore, Flowers and Paperna2004).

Centrocestus formosanus is an intestinal heterophyid trematode of Asian origin reported in birds and mammals, including humans (Scholz & Salgado-Maldonado, Reference Scholz and Salgado-Maldonado2000). The metacercariae cysts in gills produce asphyxia and mortality, as well as delayed development, which in turn cause damage to fish farming (Mitchell et al., Reference Mitchell, Overstreet, Goodwin and Brandt2005). The histopathological severity of the effect of the larval stages of C. formosanus on the gills of the fish host depends on the number of individuals infecting each host. However, from field data, it is evident that in many cases thousands of parasites are infecting individual fish hosts, with mortality occurring more frequently in juvenile fish less than 30 days old (Paperna, Reference Paperna1996; Pironet & Jones, Reference Pironet and Jones2000; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). Vogelbein & Overstreet (Reference Vogelbein and Overstreet1988) noted that C. formosanus induces an inflammatory response characterized by an unusual proliferation of fibroblasts, forming a continuous encapsulation around the parasite, which eventually destroys the gill tissue. Arguedas-Cortés et al. (Reference Arguedas-Cortés, Dolz, Romero-Zúñiga, Jiménez-Rocha and León-Alán2010), in an effort to identify the species of trematode pathogens for tilapia fry in Costa Rica, made the first records of the presence of metacercariae of C. formosanus. These authors reported intensities of between 1018 and 1027 metacercariae per parasitized fish in experimental infections, and a high fry mortality. Recently, Pinto et al. (Reference Pinto, Mati and Melo2014) reported that C. formosanus reached high prevalence (31%) and mean intensity of infection (3.42 (1–4.2)) in O. niloticus collected in an urban reservoir from Brazil, followed by the diplostomid D. compactum (29.5% and 1.27 (1–2)) recovered from eyes. The metacercariae of Drepanocephalus sp. and Ribeiroia sp. have also been found in the oral cavity of the fish but at low prevalence (8.2% and 1.6%, respectively) and intensities of infection (only one metacercaria of each species per fish). Records of these trematode species were reported for the first time by Pinto et al. (Reference Pinto, Mati and Melo2014) in O. niloticus from South America.

Cestodes

Bothriocephalus acheilognathi was found in tilapia under intensive aquaculture conditions in Cuba (Prieto et al., Reference Prieto, Fajer and Vinjoy1991). The parasite causes mechanical damage and inflammation of the intestinal mucosa, anorexia, weight loss, abdominal distension, anaemia and a tendency to swim at the surface of the water (Prieto et al., Reference Prieto, Fajer and Vinjoy1991; Pineda-López & González-Enríquez, Reference Salgado-Maldonado, Pineda-López, Vidal-Martínez and Kennedy1997; Gutiérrez-Cabrera et al., Reference Gutiérrez-Cabrera, Pulido-Flores, Monks and Gaytán-Oyarzún2005; Salgado-Maldonado, Reference Salgado-Maldonado2006; Pérez-Ponce de León et al., Reference Pérez-Ponce de León, Rosas-Valdez, Mendoza-Garfias, Aguilar-Aguilar, Falcón-Ordaz, Garrido-Olvera and Pérez-Rodríguez2009; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014).

Salgado-Maldonado & Rubio-Godoy (Reference Salgado-Maldonado and Rubio-Godoy2014) demonstrated that C. formosanus and B. acheilognathi are extremely invasive helminths, currently found in virtually all of Mexico and characterized by very low host specificity, thus infecting native fishes belonging to several families and genera.

Carp

Carp are cultivated in several Latin American countries, mainly in extensive and semi-intensive aquaculture. In 2004, the production of carp in LAC reached 59,105 tonnes, behind only salmon and tilapia (FAO, 2014). Table 3 shows the helminth species recorded from farmed carp in Latin America and the Caribbean.

Table 3. Helminth species recorded from carp species farmed in Latin America.

Monogeneans

Among Dactylogyrus species found on carp introduced into Latin America, Dactylogyrus extensus and Dactylogyrus vastator need special attention, due to their low host specificity and high pathogenicity (Ozer, Reference Ozer2002; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). Several species of Dactylogyrus have been reported for cultured carp in Mexico (table 3); however, D. extensus is the most prevalent and abundant species in carp in this country (Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). In Peru, D. vastator was found in wild carp, presumably released from aquaculture facilities (Jara & Escalante, Reference Jara and Escalante1983), while in Argentina, D. extensus was found in both cultured and wild carp. There is little information on the histological damage caused by these monogeneans, or whether they produce heavy mortality in LAC. This is partially due to the low market price of carp and to the fact that they are normally released in natural waterbodies for extensive aquaculture. However, Buchmann et al. (Reference Buchmann, Lindenstrøm, Bresciani, Wiegertjes and Flik2004) emphasized the damage produced by D. vastator in the gill epithelium of carp, hindering or preventing breathing. Golovina & Golovin (Reference Golovina and Golovin1988) showed that infection by D. extensus and D. vastator can lead to pathological changes in blood cells (gradual reduction in the number of lymphocytes).

Digeneans

The metarcercariae of the highly pathogenic non-native digenean C. formosanus have been reported in Cyprinus carpio in LAC. In Mexico, C. formosanus has been detected in several states in the country (Michoacán, Morelos, Veracruz, Tabasco, Jalisco, Hidalgo, Sonora, Tamaulipas and San Luis Potosí) (Aguilar-Aguilar et al., Reference Aguilar-Aguilar, Salgado-Maldonado, Contreras-Medina and Martínez-Aquino2008). However, the spread of this parasite to other states is highly probable (Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). Nevertheless, there are very few data on the pathogenicity of C. formosanus in fish hosts in Mexico. López-Jiménez (Reference López-Jiménez1987) reported that these metacercariae may cause severe pathological problems, decreasing the fish respiratory capacity and, in heavy infections, may lead to fry mortality. Vélez-Hernández et al. (Reference Vélez-Hernández, Constantino-Casas, García-Márquez and Osorio-Sarabia1998) demonstrated the presence of moderate to severe hyperplasia of the primary lamellae of cartilage due to C. formosanus. Other histological findings included mild hyperplasia of the lymphoid tissue in the gills, epithelial hyperplasia of lamellae, gill hyperaemia and congestion (Mitchell et al., Reference Mitchell, Salmon, Huffman and Brandt2000).

Clinostomun complanatum is another digenean that has been reported to infect farmed carp in Rio Grande do Sul, southern Brazil. This digenean has been reported to occur in wild fishes as well as in cultured carp, namely Rhamdia quelen, O. niloticus, Salminus brasiliensis, Ctenopharyngodon idella and C. carpio (Vélez-Hernández et al., Reference Vélez-Hernández, Constantino-Casas, García-Márquez and Osorio-Sarabia1998; Scholz & Salgado-Maldonado, Reference Scholz and Salgado-Maldonado2000). Dias et al. (Reference Dias, Eiras, Machado, Souza and Pavanelli2003) reported cysts in the eyes that did not cause complete blindness, but which certainly could impair fish vision, thereby facilitating predation by birds.

Cestodes

The Asian tapeworm B. acheilognathi, which may cause mortality in young carp, has successfully colonized many places in the world in which carp have been introduced (Scholz, Reference Scholz1999). The rapid spread of this parasite has been aided by fish trading for a variety of purposes, including aquaculture (Lafferty et al., Reference Lafferty, Harvell, Conrad, Carolyn, Friedman, Kent, Kuris, Powell, Rondeau and Saksida2014). In South America, this endoparasite was first introduced into Brazil together with C. carpio. The first record of this non-native cestode was in the 1990s, in carp grown in the state of Paraná, southern Brazil (Rego, Reference Rego1999). Mexican workers have documented carp losses associated with the presence of this parasite in official carp farms (Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). Bothriocephalus acheilognathi is widely distributed in practically all the states of Mexico, and it is present in several environments, including rivers, sinkholes, lakes and carp farms (Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). The pathology of the tapeworm in the fish gut includes intestinal blockage, flaking and erosion of the intestinal epithelium, and bowel perforation (Salgado-Maldonado & Pineda-López, Reference Salgado-Maldonado and Pineda-López2003). Although there are few reports from other Latin American countries, in Brazil and Argentina B. acheilognathi has been identified in cultured carp without apparent mortalities.

Cultured native species

In most Latin American countries there is incipient aquaculture of native species in both freshwater and marine environments. Among the species under experimental or low-scale freshwater aquaculture are tambaqui or cachama (Colossoma macropomum), channel catfish (Ictalurus punctatus), silver catfish (Rhamdia quelen), Mayan cichlid (Cichlasoma urophthalmus), bay snook (Petenia splendida), fat snook (Centropomus parallelus), common snook (Centropomus undecimalis), pacu (Piaractus mesopotamicus), Argentinian silverside (Odonthestes bonariensis), pirarucu (Arapaima gigas) and bocachico (Prochilodus magdalenae). For seawater aquaculture, the species involved are Pacific bluefin tuna (Thunnus thynnus), yellowtail kingfish (Seriola lalandi), spotted red snapper (Lutjanus guttatus), sea bass (Dicentrarchus labrax) and snowy grouper (Epinephelus niveatus). There is no doubt that Latin American aquaculture will face serious problems with helminth parasites in the near future, with the increase in fish density in all kinds of facilities such as floating cages, earth or concrete ponds, raceways, etc. (Mujica & Armas de Conroy, Reference Mujica and Armas de Conroy1985; Aragort & Moreno, Reference Aragort and Moreno1997). Helminths with direct life cycles, such as monogeneans, are the ones that will probably appear under aquaculture conditions, especially in floating cages. Table 4 shows the helminth species recorded from freshwater native fish species farmed in Latin America.

Table 4. Helminth species recorded from freshwater native fish species farmed in Latin America. G = groups of parasites, as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala, H = Hirudinea.

Colossoma macropomum is the main native fish species cultured commercially in Brazil, Colombia, Cuba, Peru and Venezuela. In this fish species the most important monogenean species due to their high prevalence and mean abundance values are: Dactylogyrus sp., Anacanthorus spatulatus, Linguadactyloides brinkmanni, Mymarothecium boegeri and Notozothecium janauachensis (Ceccarelli et al., Reference Ceccarelli, Figueira, Ferraz-Lima and Oliveira1990; Belmont-Jégu et al., Reference Belmont-Jégu, Domingues and Martins2004; Centeno et al., Reference Centeno, Silva-Acuña, Silva-Acuña and Pérez2004; Cohen & Kohn, Reference Cohen and Kohn2005; Tavares-Dias et al., Reference Centeno, Altuve, Gil, Matute, Pérez, Lunar and Urbaneja2006; Dias et al., Reference Dias, Neves, Marinho and Tavares-Dias2015a). However, A. spatulatus is considered to be the main gill ectoparasite on cachama cultivated in LAC (Conroy & Conroy, Reference Conroy and Conroy1998; Torres et al., Reference Torres, Castillo, Cortez, Bravo and Fortine2002b; Dias et al., Reference Dias, Neves, Marinho and Tavares-Dias2015a), being able to reach prevalence values of 98–100% in outbreaks in cultured cachama (Aragort, Reference Aragort1994; Torres et al., Reference Torres, Castillo, Cortez, Bravo and Fortine2002b). Moreover, A. spatulatus and L. brinkmanni have also been recorded in the gills of cachama reared in Peru (Conroy, Reference Conroy2001) and Venezuela (Mujica, Reference Mujica1982; Urquia, Reference Urquia1997), causing high mortality in both juveniles and adults (Mujica & Armas de Conroy, Reference Mujica and Armas de Conroy1985; Urquia, Reference Urquia1997). Furthermore, Centeno et al. (Reference Centeno, Silva-Acuña, Silva-Acuña and Pérez2004) also reported A. spatulatus in the gills of the hybrid ‘cachama’ × ‘morocoto’ (C. macropomum × Piaractus brachypomus), with prevalence rates of above 70%. Likewise, Silva et al. (Reference Silva, Tavares-Dias, Maycon, Dias and Marinho2013) and Dias et al. (Reference Dias, Neves, Marinho and Tavares-Dias2015a) investigated the parasitic fauna infesting the hybrid tambacu (C. macropomum × P. mesopotamicus) and tambatinga (C. macropomum × P. brachypomus) at fish farms in northern Brazil. Silva et al. (Reference Silva, Tavares-Dias, Maycon, Dias and Marinho2013) reported prevalences above 77% for A. spatulatus, N. janauachensis and Mymarothecium viatorum in tambacu. Dias et al. (Reference Dias, Neves, Marinho and Tavares-Dias2015a) found infections by L. brinkmanni and M. boegeri in tambatinga. With respect to the histological lesions caused by these monogeneans in the gills of C. macropomum, Aragort et al. (Reference Aragort, Morales, León, Pino, Guillén and Silva2002) found that the affected fish showed a significant reduction in haematocrit counts and severe hyperplasia associated with mixed infections of A. spatulatus and L. brinkmanni. Similarly, Mujica (Reference Mujica1982) reported that the main histological alterations caused by L. brinkmanni in the gill tissues of cachama were severe hyperplasia and hypertrophy.

With respect to digeneans, Paramphistomidae such as Dadaytrema oxycephala have been reported as parasites of cachama (Conroy, Reference Conroy1999). Regarding nematodes, Mujica (Reference Mujica1982) reported Chabaudinema americana in the gut of C. macropomum broodstock kept in tanks in Venezuela. Cucullanus colossomi, Procamallanus inopinatus (Nematoda), Proteocephalidae larvae (Cestoda) and Neoechinorhynchus buttnerae (Acanthocephala) have been reported by Silva et al. (Reference Silva, Tavares-Dias, Maycon, Dias and Marinho2013) and Dias et al. (Reference Dias, Neves, Marinho and Tavares-Dias2015a) from the hybrids tambacu and tambatinga in fish farms in Brazil.

Channel catfish, I. punctatus, is one of the most important fish species under intensive culture in LAC. In Mexico, the production of cultured channel catfish in 2008 was 970 tonnes (Comisión Nacional de Acuacultura y Pesca, 2008). However, there are few studies about the helminth species affecting the production of channel catfish (Rábago-Castro, Reference Rábago-Castro2010; Rábago-Castro et al., Reference Rábago-Castro, Sánchez-Martínez and Loredo-Osti2011; Galaviz-Silva et al., Reference Galaviz-Silva, Molina-Garza, Escobar-González and Iruegas-Buentello2013; Benavides-González et al., Reference Benavides-González, Gomez-Flores, Sánchez-Martinez, Rábago-Castro and Montelongo-Alfaro2014). Recently, Galaviz-Silva et al. (Reference Galaviz-Silva, Molina-Garza, Escobar-González and Iruegas-Buentello2013) provided new data on the prevalence and abundance of the parasitic fauna on I. punctatus in Mexico. These authors demonstrated a great diversity of helminth parasites, including Ligictaluridus floridanus and Corallobothrium fimbriatum, and new locality records for Megalogonia ictaluri, Centrocestus formosanus, Diplostomum compactum and Spiroxys sp. They also reported a new host and distribution record for Spinitectus tabascoensis, originally described from Ictalurus furcatus from Tabasco, southern Mexico. In total, 12 helminth species have been reported from I. punctatus (Jiménez-Guzmán et al., Reference Jiménez-Guzmán, Galaviz-Silva, Segovia-Salinas, Garza-Fernández and Wesche-Ebeling1988; Flores-Crespo & Flores-Crespo, Reference Flores-Crespo and Flores-Crespo1993, Reference Flores-Crespo and Flores-Crespo2003; Scholz & Salgado-Maldonado, Reference Scholz and Salgado-Maldonado2000; Rábago-Castro, Reference Rábago-Castro2010; Rábago-Castro et al., Reference Rábago-Castro, Sánchez-Martínez and Loredo-Osti2011; Galaviz-Silva et al., Reference Galaviz-Silva, Molina-Garza, Escobar-González and Iruegas-Buentello2013; Benavides-González et al., Reference Benavides-González, Gomez-Flores, Sánchez-Martinez, Rábago-Castro and Montelongo-Alfaro2014; Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). Rábago-Castro et al. (Reference Rábago-Castro, Sánchez-Martínez and Loredo-Osti2011) reported, for first time, the prevalence and mean intensitiesy of ectoparasites of cage-cultured channel catfish in an annual cycle. The results showed peaks of prevalence of L. floridanus in early autumn. However, the presence of L. floridanus was not associated with any fish mortality. In contrast, Benavides-González et al. (Reference Benavides-González, Gomez-Flores, Sánchez-Martinez, Rábago-Castro and Montelongo-Alfaro2014) showed that the gill monogenean L. floridanus is the most common parasite of cultured channel catfish, affecting fish growth and possibly promoting secondary infections.

With the exception of the papers of Vidal-Martínez et al. (Reference Vidal-Martínez, Kennedy and Aquirre-Macedo1998), there are no records of parasites or diseases of C. urophthalmus under aquaculture conditions in Mexico. Vidal-Martínez et al. (Reference Vidal-Martínez, Kennedy and Aquirre-Macedo1998) showed that the parasites that colonized caged C. urophthalmus were species with an active colonization strategy. This was the case for the monogenean Sciadicleithrum mexicanum, the larval digeneans Echinochasmus leopoldinae and Oligogonotylus manteri, and the nematodes Mexiconema cichlasomae and Contracaecum multipapillatum. Of these parasites, the most relevant for aquaculture is the monogenean S. mexicanum, due to its direct life cycle. This monogenean is also able to infect the Nile tilapia O. niloticus under experimental conditions (Jiménez-García et al., Reference Jiménez-García, Vidal-Martínez and López-Jiménez2001).

For bay snook P. splendida, the official statistics suggest the presence of several parasite species, such as Cichlidogyrus sp., Contracaecum spp., Diplostomum sp. and Gnathostoma sp. (DOF, 2013), the last being an emerging public health problem in Mexico, with several thousand cases reported (Herman & Chiodini, Reference Herman and Chiodini2009; Diaz, Reference Diaz2015). However, these records need to be re-examined. For example, Cichlidogyrus is a very specific monogenean genus of African cichlids (e.g. tilapia). If the identification is correct, then this would be a new record of an African monogenean infecting a native Mexican cichlid fish. Therefore, we consider it necessary to evaluate further the parasitological material deposited in proper museum collections. Recently, Tancredo et al. (Reference Tancredo, Marchiori, Roumbedakis, Cerqueira, Tavares-Dias and Martins2015) investigated the metazoan parasite fauna of C. parallelus and C. undecimalis, bred in southern Brazil, and its influence on the condition factor of hosts. The monogeneans Rhabdosynochus rhabdosynochus and Rhabdosynochus hudsoni were recorded in the gills of both species, and the digenean Acanthocollaritrema umbilicatum was reported from their digestive tracts. Prevalence of Rhabdosynochus spp. was high (100%) in both species. In contrast, mean intensity and abundance were higher in C. parallelus. A negative correlation was found between monogenean abundance and condition factor in C. parallelus, suggesting that gill monogeneans do alter fish welfare. There was no correlation between abundance of A. umbilicatum and length or weight of either C. parallelus or C. undecimalis.

Piaractus mesopotamicus is cultured in several countries in LAC, including Brazil (Lizama et al., Reference Lizama, Takemoto, Ranzani-Paiva, Silva-Ayroza and Pavanelli2007b). In Argentina, native pacu covers at least 30% of the domestic market demands (Macchi, Reference Macchi2004). Several species of monogeneans (Anacanthorus penilabiatus, A. spatulatus, L. brinkmanni, Mymarothecium viatorum, Dactylogyrus sp.) have been reported in aquaculture conditions (Ceccarelli et al., Reference Ceccarelli, Figueira, Ferraz-Lima and Oliveira1990; Boeger et al., Reference Boeger, Husak and Martins1995; Martins, Reference Martins1998; Conroy, Reference Conroy2001; Tavares-Dias et al., Reference Tavares-Dias, Moraes, Martins and Kronka2001; Martins et al., Reference Martins, Onaka, Moraes, Bozzo, Paiva and Goncalves2002; Cohen & Kohn, Reference Cohen and Kohn2005; Lizama et al., Reference Lizama, Takemoto, Ranzani-Paiva, Silva-Ayroza and Pavanelli2007b). However, A. penilabiatus and A. spatulatus have been registered as the most important gill parasites in the aquaculture of P. mesopotamicus in Bolivia, Cuba, Peru, Venezuela and Brazil (Conroy & Conroy, Reference Conroy and Conroy1998; Del Pozo, Reference Del Pozo2000; Tavares-Dias et al., Reference Tavares-Dias, Moraes, Martins and Kronka2001). With respect to the histopathological damage caused by A. penilabiatus in cultured P. mesopotamicus, Martins & Romero (Reference Martins and Romero1996) found an inflammatory reaction and moderate hyperplasia of epithelial cells in the gills. In the same study, the authors pointed out that the damage produced by this monogenean was not extensive in low to moderate infections (<33 parasites/host). However, in heavy infections (>33 parasites/host) the parasite caused considerable changes in primary and secondary lamellae, associated with multiple sites of bleeding, detachment of respiratory tissue and numerous necrotic foci. Lizama et al. (Reference Lizama, Takemoto, Ranzani-Paiva, Silva-Ayroza and Pavanelli2007b) also showed a negative correlation between the abundance of A. penilabiatus and the condition factor of farmed P. mesopotamicus in Brazil.

Knowledge on the helminth parasites infecting A. gigas under aquaculture conditions is scarce. Recently, Marinho et al. (Reference Silva, Tavares-Dias, Maycon, Dias and Marinho2013) found in Brazil that the host condition factor was negatively correlated with the number of Dawestrema cycloancistrium and Dawestrema cycloancistrioides, which demonstrates the pathogenicity of these parasites in gills of farmed A. gigas. Araújo et al. (Reference Araújo, Gomes, Tavares-Dias, Raújo, Andrade, Belem-Costa, Borges, Queiroz and Barbosa2009a, Reference Araújo, Tavares-Dias, Gomes, Andrade, Lemos, Oliveira, Cruz, Affonso and Tavares-Diasb) and Mathews et al. (Reference Mathews, Mathews and Ismiño2013) recorded the infection by D. cycloancistrium and D. cycloancistrioides as the most prevalent helminths parasitizing cultured A. gigas (100% and 85%, respectively). Aquaria, a specialized variant of aquaculture enterprises, have serious problems due to monogenean infections in A. gigas in LAC. This fish species experiences severe morbidity and heavy mortality due to D. cycloancistrium (Mathews et al., Reference Mathews, Chu-Koo, Tello, Malta, Varella and Gomes2007) in aquaria. In addition, infections by the nematodes Goezia spinulosa (Caldas-Menezes et al., Reference Caldas-Menezes, Cursino dos Santos, Ceccarelli, Tavares, Tortelly and Luque2011), Terranova serrata and Camallanus tridentatus have also been reported from A. gigas in aquaria (Araújo et al., Reference Araújo, Gomes, Tavares-Dias, Raújo, Andrade, Belem-Costa, Borges, Queiroz and Barbosa2009a, Reference Araújo, Tavares-Dias, Gomes, Andrade, Lemos, Oliveira, Cruz, Affonso and Tavares-Diasb). However, with the exception of monogeneans, the nematodes will eventually be lost in aquaria if the intermediate hosts needed to complete the life cycle are not present. A single report exists of the digenean Caballerotrema brasiliense in A. gigas from farms of the Peruvian Amazon (Serrano-Martínez et al., Reference Serrano-Martínez, Tantaleán, Leguía, Quispe and Casas2015).

The bocachico, P. magdalenae, is a native of Colombia's Magdalena region and the fourth most frequently cultivated species in Colombia. This fish has been cultivated for several years in ponds (Sarmiento & Rodríguez, Reference Sarmiento and Rodríguez2013), and several helminth species have been recorded infesting farmed P. magdalenae, including Dactylogyrus sp., Tetraonchus sp., Calocladorchis ventrastomis, Diplostomum sp., Lecithobotrioides mediacanoensis, Sacocoelios sp., Unicoeliun prochilodorum, Procamallanus sp., Raphidascaris sp. and Spinitectus jamundensis (Nickol & Thatcher, Reference Nickol and Thatcher1971; Thatcher & Dossman, Reference Thatcher and Dossman1974, Reference Thatcher and Dossman1975; Thatcher & Padilha, Reference Thatcher and Padilha1977; Chavarro, Reference Chavarro1983; López-González, Reference López-González1987; Sánchez-Páez, Reference Sánchez-Páez1993; Thatcher, Reference Thatcher1993; Eslava-Mocha et al., Reference Eslava-Mocha, Verján and Iregui-Castro2001; Álvarez-León, Reference Álvarez-León2007). However, so far, there are apparently no specific records of diseases caused by helminths in cultivated bocachicos.

Mariculture enterprises may also be hampered by severe parasitic helminth infections. Table 5 presents the helminth species recorded from native seawater species farmed in Latin America.

Table 5. Helminth species recorded from seawater native fish species farmed in Latin America. Groups of parasites (G) were as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala.

Marine aquaculture of bluefin tuna is based on fattening wild juveniles. Consequently, it makes sense to consider the parasites and diseases that these juveniles bring into floating cages. Sánchez-Serrano & Cásares-Martínez (Reference Sánchez-Serrano and Cásares-Martínez2011) reported nematodes of the genus Anisakis spp., trematodes of the subfamilies Nephrodidymotrematinae and Koellikeriinae, and acanthocephalans of the family Polymorphidae. The nematodes of the Anisakis genus are accidental parasites of humans, producing the disease known as anisakiasis. Consequently, sanitary measures should be adopted to avoid the presence of these parasites in tuna fillets. In the case of caged yellowtail (Seriola lalandi) in Mexico, the infections by the monogeneans Benedenia sp. and Heteraxine sp. are considered important because they produce decreases in feeding rate, anaemia, weakness and mortality (Avilés-Quevedo & Castello-Orvay, Reference Avilés-Quevedo and Castello-Orvay2004). In Chile, S. lalandi is one of the most important candidates for commercial aquaculture. In sea cages in northern Chile, S. lalandi is parasitized by the monogenean Benedenia seriolae (Capsalidae) on the body surface and by Zeuxapta seriolae (Heteraxinidae) as a sanguineous gill fluke (Oliva, Reference Oliva1986).

In official statistics, Neobenedenia has been reported infecting Lutjanus guttatus in aquaculture conditions in Mexico (DOF, 2013). However, we found no published records on this parasitic association. Other ectoparasites reported infecting L. guttatus in floating cages in Mexico were the monogeneans Euryhaliotrema perezponcei, Euryhaliotrema mehen and Haliotrematoides guttati (Soler-Jiménez et al., Reference Soler-Jiménez, Morales-Serna and Fajer-Ávila2015). The authors stressed that even under the juvenile fish densities studied (789/m3) no mortality was found, and a high number of E. perezponcei was reached (prevalence = 100%; mean intensity = 154–296 parasites per infected host) during 9 months of exposure. The authors concluded that the infection should be monitored over time to prevent outbreaks and mortality, especially under intensive aquaculture conditions. In fact, sublethal effects of the dactylogyrid monogeneans infecting cultured L. guttatus should also be considered carefully, since Del Río-Zaragoza et al. (Reference Del Río-Zaragoza, Fajer-Ávila and Almazán-Rueda2010) found that a high level of infection (≥100 monogeneans per fish) caused changes in the number of blood cells and histological alterations in gill tissue.

Cultured ornamental species

Ornamental fish export has emerged as an important activity, generating foreign exchange, for several Latin American countries (e.g. Brazil, Colombia, Mexico, Peru and Uruguay) (Carnevia, Reference Carnevia1999; Carnevia & Speranza, Reference Carnevia2003; Tavares-Dias et al., Reference Araújo, Gomes, Tavares-Dias, Raújo, Andrade, Belem-Costa, Borges, Queiroz and Barbosa2009a). For example, from 2006 to 2007 the revenue of the south-east region of Brazil included US$418,572 from sales of freshwater ornamental fish. In 2007, sales of freshwater ornamental fish increased 100% (Tavares-Dias et al., Reference Tavares-Dias, Lemos, Martins, Jeronimo and Tavares-Dias2009a). However, most of the income came from sales of ornamental fish captured from natural environments (principally the Amazonian basin) and only a small amount was generated from sales of fish from fish farms. Despite this, the demand for cultured ornamental fish is increasing, and consequently parasitic infections can be one of the most important problems for cultured fish in the region. However, few studies regarding parasitic infection of cultured ornamental fish have been published for LAC. Piazza et al. (Reference Piazza, Martins, Guiraldelli and Yamashita2006), Martins et al. (Reference Martins, García, Piazza and Ghiraldelli2007) and Tavares-Dias et al. (Reference Araújo, Gomes, Tavares-Dias, Raújo, Andrade, Belem-Costa, Borges, Queiroz and Barbosa2009a) recorded high prevalence rates of metazoan parasites, such as monogeneans and nematodes, from cultured ornamental fish farms or pet shops in Brazil. In table 6 we present the helminth species recorded from cultured ornamental fish in LAC.

Table 6. Helminth species recorded from ornamental fish species farmed in Latin America. G = groups of parasites, as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala.

Ornamental fish in intensive culture are continuously affected by management practices such as handling, crowding, transport and poor water quality that provoke stress to fish, rendering them susceptible to a variety of parasites. For LAC, there are several records of helminths affecting ornamental fish cultivated mainly in Brazil and Mexico. However, there are a few records of catastrophic negative impacts where a helminth is involved as a causative agent. For example, mixed infections by monogeneans such as Gyrodactylus sp. and Dactylogyrus sp. on gills and skin have been responsible for high mortality rates (60–70%) within a few days among golden carp, Carassius auratus, in aquarium fish in Peru (Gonzáles-Fernández, Reference Gonzáles-Fernández2012b). In this case, the pathology described was increased mucus in the gills, as well as a strong detachment of the epidermis and the loss of the caudal fin. Likewise, in Brazil, Alves et al. (Reference Alves, Luque, Paraguassu and Marques2000) reported high mortalities of Poecilia reticulata in fish farms due to infection with the nematode Camallanus cotti. This mortality was due to the pathology caused by C. cotti, with haemorrhage, congestion, oedema and extensive areas of eroded mucosa in the intestine and rectum (Menezes et al., Reference Menezes, Tortelly, Tortelly-Neto, Noronha and Pinto2006). Ortega et al. (Reference Ortega, Fajardo and Enríquez2009) found gill infections by Centrocestus formosanus metacercarie in 11 out of 25 species of ornamental fish cultured in Mexico, where the most affected species was goldfish, C. auratus. The negative effect of C. formosanus on farmed fish was confirmed in moribund individuals that manifested respiratory abnormality and, histologically, showed severe branchial lesions caused by metacercariae (Ortega et al., Reference Ortega, Fajardo and Enríquez2009). These authors stressed the low host specificity of C. formosanus, which is the main reason for a great variety of fish being infected with different degrees of prevalence and severity (Scholz & Salgado-Maldonado, Reference Scholz and Salgado-Maldonado2000; Vidal-Martínez et al., Reference Vidal-Martínez, Aguirre-Macedo, Scholz, González-Solís and Mendoza-Franco2001).

Discussion

The present contribution shows that more than 90% of the helminth parasites affecting finfish in aquaculture conditions in LAC are non-native. For example, 40 species of helminths have been introduced to Mexico, among which 33 are monogeneans (Salgado-Maldonado & Rubio-Godoy, Reference Salgado-Maldonado and Rubio-Godoy2014). This means that most of these helminths have been introduced with their hosts by commercial trade, suggesting an almost complete lack of application of biosecurity measures in LAC countries. However, there is a general trend among the aquaculture farm owners of the region to consider helminth parasites as non-pathogenic, because many of them do not produce significant mortalities or visible pathologies. The authors consider that this assumption is a mistake because helminth parasites can become harmful under the challenging environmental circumstances typical of fish farms (e.g. high temperature and productivity, low water exchange rate and high fish density) (Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). This is especially true for monogeneans, which are recognized as the most common, abundant and aggressive helminths affecting farmed fish (Whittington et al., Reference Whittington, Corneillie, Talbot, Morgan and Adlard2001; Ernst et al., Reference Ernst, Whittington, Corneille and Talbot2002; Whittington, Reference Whittington and Rohde2005; Soler-Jiménez et al., Reference Soler-Jiménez, Morales-Serna and Fajer-Ávila2015).

In LAC, there are several anecdotal reports of high mortalities of farmed fish caused by helminths, especially monogeneans, representing severe economic losses (Mujica & Armas de Conroy, Reference Mujica and Armas de Conroy1985; Kaneko et al., Reference Kaneko, Yamada, Brock and Nakamura1988; Conroy, Reference Conroy2001; García-Vásquez et al., Reference García-Vásquez, Hansen, Christison, Bron and Shinn2011). For example, infections with C. sclerosus have important effects on the growth rates and relative condition factors of their hosts, which in turn affects tilapia farmers economically (Sandoval-Gío et al., Reference Sandoval-Gío, Rodríguez-Canul and Vidal-Martínez2008; Le Roux, Reference Le Roux2010; Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader, Torres-Irineo, Romero and Vidal-Martínez2016a). Moreover, other helminth species, such as the ‘yellow grub’, are argued to produce economic losses due to the poor appearance that they produce in farmed fish (Mitchell et al., Reference Mitchell, Goodwin, Salmon and Brandt2002; Pavanelli et al., Reference Pavanelli, Eiras and Takemoto2002; Vianna et al., Reference Mitchell, Overstreet, Goodwin and Brandt2005; Silva et al., Reference Silva, Monteiro, Doyle, Pedron, Filipetto and Radunz-Neto2008; Sutili et al., Reference Sutili, Gressler and Vilani de Pelegrini2014). Unfortunately, none of these studies has included a bioeconomic analysis to determine the financial resources lost due to the presence of helminths in fish cultured in LAC. Such analyses are urgently needed.

It is difficult to calculate the economic costs attributable to helminth infections due to the complex interplay of numerous environmental and management factors that vary among individual fish farms at the global level. Similar concerns have been expressed by Shinn et al. (Reference Shinn, Pratoomyot, Bron, Paladini, Brooker and Brooker2015) with respect to salmonid diseases in temperate latitudes, and complexity is even more extreme in LAC, partly due to the reluctance of the farm owners to share information on the causes of fish mortality. As a notable exception, Paredes-Trujillo et al. (Reference Paredes-Trujillo, Velázquez-Abunader and Vidal-Martínez2016b) were able to obtain information on the mortality, environmental and management variables of 21 tilapia farms in Yucatan, Mexico, thanks to the kind collaboration of their owners. Using this dataset, a multivariate regression analysis was undertaken using the percentage of mortality as a dependent variable and 12 environmental and management variables (out of 45 variables), including the abundance of all the parasite species found per individual fish as an independent variable (table 7). The results of this analysis suggest that helminths can contribute to fish mortality, but only in synergy with other environmental and management variables. For the 21 tilapia farms in Yucatan, the mean percentage of mortality (± standard deviation) due to all those variables (including abundance of helminths) was 36 ± 43% (table 7). Considering the price of a kilogram of whole tilapia, between US$3 and 5 (https://www.alibaba.com/products/F0/tilapia_wholesale_price), the economic cost produced by mortality was between US$7821 ± 21,991 and US$13,034 ± 36,652 per year per farm. When an analysis was made considering only the effects of helminth parasites on fish mortality, the result was not significant (ANOVA with linear regression; F 1,396 = 0.76; P = 0.49). However, it is still possible that helminth parasites do not kill the fish, but that they produce a subtle and important debilitating effect on the condition factor of the tilapia at farms in Yucatan (Paredes-Trujillo et al., Reference Paredes-Trujillo, Velázquez-Abunader and Vidal-Martínez2016b). This generalized debilitation should be considered as part of the synergy mentioned above. The authors were not able to obtain datasets for salmonids or carp, similar to the one for tilapia, to quantify the economic cost of helminth infections. However, it is considered that the tilapia farms in Yucatan are a good model when trying to understand the sanitary circumstances of finfish aquaculture in LAC, with the results obtained here applying to rural areas of most countries where tilapia and other freshwater or marine fishes are farmed. The reason for the large values of the standard deviation of the percentage of mortality is associated with the fact that LAC farmers often lack the technical expertise in proper sanitary management at farm level. Very often, when disease occurs in the farm, chemotherapeutic treatments are applied, without strict dose control. However, the most important side-effects of the use and misapplication of chemical products (e.g. antibiotics, disinfectants) are microbial and parasite resistance, chemical toxicity and persistence of chemical residues (Chávez-Sánchez & Montoya-Rodríguez, Reference Chávez-Sánchez and Montoya-Rodríguez2004). Without a doubt, aquaculture in LAC needs appropriate biosecurity measures, including risk analysis, surveillance and monitoring, as well as planning to respond effectively to outbreaks of diseases in aquatic animals (Bondad-Reantaso et al., Reference Bondad-Reantaso, Subasinghe, Arthur, Ogawa, Chinabut, Adlard, Tan and Shariff2005). To reach this level of development in LAC, basic and applied research on specific sanitary problems of farmed aquatic animals is necessary, as well as institutional strengthening and human resource development (good extension programmes, education for both aquaculture farm owners and technicians, as well as training for aquatic animal health experts).

Table 7. Multivariate regression analysis using the percentage of mortality as a dependent variable, and the best 12 environmental and management independent variables (out of 45 variables) (see supplementary table S1) selected by a stepwise procedure. The coefficient of determination of this model was R 2 = 0.71 for N = 399. The best regression model was chosen based on the lowest values of the CpMallows (model selection method) and variance inflation factor (VIF) statistics. The maximum P value for each variable to entry the model was 0.01, and the maximum value for retention of the variable was 0.05. The normality of all variables was verified using Wilk–Shapiro rankit plots (WS), and if normality was not attained (WS > 0.8), then the variables were transformed to natural logarithms + 1.

Therefore, preventive and control measures should be implemented to limit the size of the helminth populations in cultured fish and to minimize the probability of potential diseases. A successful helminth control programme consists of the selection of fish free of helminth parasites from the place of origin, proper quarantine, good husbandry practices, prophylactic measures, correct diagnosis and, if necessary, therapeutic treatment (Abayomi et al., Reference Abayomi, Balogun, Omonona and Yusuf2013). Preventive measures in fish parasite control (including helminths), such as effective quarantine, are often ignored, resulting in a much higher economic expenditure to eliminate imported pathogenic parasites. It must be emphasized that prevention is the key and therapeutic treatment should be seen as the last alternative.

Nowadays, avoiding the entry of new helminth species to the region is one of the main challenges that aquaculture is facing in LAC. This is a very important topic because, in the same way that viral diseases have been translocated into LAC (e.g. white spot in shrimps in Mexico and infectious salmon anaemia (ISA) in salmonid fishes in Chile) (http://www.oie.int/en/), other harmful helminth parasites could be translocated into LAC. Unfortunately, it must be recognized that surveillance programmes for aquatic diseases in many LAC regions are weak. In addition, their implementation presents many problems: (1) the lack of standardization of diagnostic tests; (2) socio-economic factors and the lack of technological development in many regions in LAC; (3) the diversity of cultivated species, range and complexity of the environment; and (4) the intensity of practice, variety of farming systems and management types (Bondad-Reantaso et al., Reference Bondad-Reantaso, Subasinghe, Arthur, Ogawa, Chinabut, Adlard, Tan and Shariff2005). Moreover, it is important to realize that one of the most important current challenges in LAC is the lack of capacity to diagnose accurately and report diseases in aquatic animals. Vidal-Martínez (Reference Vidal-Martínez2012) reviewed the capacity of countries within LAC to diagnose and report selected World Organization for Animal Health (OIE)-listed diseases of aquatic animals, based on 16 years of data available in the OIE databases. This author found that diagnosis performance and reporting of OIE-listed diseases were significantly associated with aquaculture production in the countries. Three groups of countries were determined. The first group included countries with aquaculture production >200,000 tonnes/year, which had maintained their diagnostic capacities for 15 years (e.g. Brazil, Chile and the USA). The second group included countries with less than 200,000 tonnes of aquaculture production per year, which had maintained their diagnostic capacities for 10–15 years (e.g. Canada, Colombia and Mexico). The third group included countries that had been unable to maintain consistent diagnostic reporting for more than 5 years for OIE diseases (73% of the analysed countries in LAC). Countries in the third group are unprotected against the potential introduction of OIE-listed diseases and other kinds of important helminth parasites in aquaculture. Clearly, there is an urgent need to develop sound biosecurity programmes in these countries, as well as the physical and human capacity to deal with the proper diagnosis of these diseases and parasites (including helminths). Therefore, it is necessary to propose strategies to address transboundary diseases affecting the sector of Latin American aquaculture, including compliance with the international codes established by the World Organisation for Animal Health (OIE, 2015).

Vidal-Martínez (Reference Vidal-Martínez2012) proposed two strategic lines that should be considered for the development of the sanitary aspects of aquaculture in LAC in the near future. First, due to the incipient development of the diagnostic capacity for OIE-listed diseases and helminth parasitic diseases affecting aquaculture in LAC, there is a need for more experts in diseases of fish in the region. The freshwater and marine aquaculture producers need the support of experts, in view of the imminent development of the market in the region (see FAO, 2015). Second, academic institutions throughout the whole region need to be in touch with the producers, to generate the kind of experts needed to warrant the sanitary development of aquaculture in LAC. In addition, awareness at all levels (managers, officers, employees) of the correct application of sanitary measures, is one of the most important challenges that LAC faces to reduce the spread of diseases (FAO, 2016).

Therefore, the importance of health standards, surveillance and monitoring programmes suggested by international organizations (e.g. FAO, OIE) and enforced by national authorities, which guarantee and certify the quality of aquatic products that are distributed inside and outside each country, is evident. While these are not carried out properly, the future of sustainable aquaculture in LAC is uncertain.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/S0022149X16000833

Acknowledgements

The authors thank C. Vivas-Rodríguez, N. Herrera Castillo and A. Centeno-Chalé of CINVESTAV-Mérida for support with the field and laboratory work, and to M.A. Soler-Jiménez and L.F. Sauma-Castillo for support in the literature search.

Financial support

This work was supported by grant No. 201441 ‘Plataformas de observación oceanográfica, línea base, modelos de simulación y escenarios de la capacidad natural de respuesta ante derrames de gran escala en el Golfo de México’ of the Sectorial Hidrocarbon Fund Consejo Nacional de Ciencia y Tecnología (México)–Secretaría de Energía (CONACYT-SENER) to the Consorcio de Investigación del Golfo de Mexico (CIGoM) in which L.C.S.J. and V.M.V.M. participate.

Conflict of interest

None.

Footnotes

† These authors were equal contributors.

References

Abayomi, E., Balogun, O.S., Omonona, B. & Yusuf, S. (2013) An analysis of risk factors among urban fish famers in Kaduna, Kaduna State. Journal of Agriculture and Veterinary Science 2, 2135.Google Scholar
Aguilar-Aguilar, R., Salgado-Maldonado, G., Contreras-Medina, R. & Martínez-Aquino, A. (2008) Richness and endemism of helminth parasites of freshwater fishes in Mexico. Biological Journal of the Linnean Society 94, 435444.Google Scholar
Aguirre-Fey, D., Benítez-Villa, G., Pérez-Ponce de León, G. & Rubio-Godoy, M. (2015) Population dynamics of Cichlidogyrus spp. and Scutogyrus sp. (Monogenea) infecting farmed tilapia in Veracruz, México. Aquaculture 443, 1115.CrossRefGoogle Scholar
Ajiaco-Martínez, R.E. & Ramírez-Gil, H. (no date) Peces ornamentales: Manejo y prevención de enfermedades. Santafé de Bogotá, Colombia, Inpa-Cifpa/Corpoamazonia/Asopescam/Pronatta.Google Scholar
Álvarez-León, R. (2007) Asociaciones y patologías en los peces dulceacuícolas, estuarinos y marinos de colombia: aguas libres y controladas. Boletín Científico, Centro de Museos, Museo de Historia Natural 11, 81129.Google Scholar
Alves, D.R., Luque, J.L., Paraguassu, A.R. & Marques, F.A. (2000) Ocurrencia de Camallanus cotti (Nematida: Camallanidae) parasitando o guppy, Poecilia reticulate (Osteichthyes: Poecilidae) no Brasil. Revista Universitaria Rural Ciencia y Vida 22, 7779.Google Scholar
Alves, D.R., Luque, J.L. & Paraguassu, A.R. (2001) Metacercárias de Clinostomum marginatum (Digenea: Ciclostomidae) em acará-banderia Pterophyllum scalare (Osteichthyes: Ciclidae) no estado do Rio de Janeiro, Brasil. Parasitologia al Dia 25, 7072.Google Scholar
Aragort, W. (1994) Parasitismo por trematodos monogenénesicos branquiales en cachama, Colossoma macroporum, bajo condiciones de cultivo: El caso de la sub-Estación Experimental Papelón, Estado Portuguesa. Thesis, Universidad Central de Venezuela (UCV). Maracay, Venezuela.Google Scholar
Aragort, W.C. & Moreno, L.G. (1997) Indices epidemiológicos de trematodos monogenésicos en branquias de Colossoma macropomum, bajo cultivo. Acta Biologica Venezuela 17, 18.Google Scholar
Aragort, W., León, E., Guillén, A.T., Silva, M. & Balestrini, C. (1997) Fauna Parasitaria en Tilapias del Lago de Valencia. Veterinaria Tropical 22, 171187.Google Scholar
Aragort, W., Morales, G., León, E., Pino, L.A., Guillén, A. & Silva, M. (2002) Patologías asociadas a monogeneos branquiales en cachama bajo cultivo. Veterinaria Tropical 27, 7585.Google Scholar
Araújo, C.S.O., Gomes, A.L., Tavares-Dias, M., Raújo, S.M., Andrade, S.M., Belem-Costa, A., Borges, J.T., Queiroz, M.N. & Barbosa, M. (2009a) Parasitic infections pirarucu fry, Arapaima gigas Schinz, 1822 (Arapaimatidae) kept in a semi-intensive fish farm in Central Amazon, Brazil. Veterinarski Arhiv 79, 499507.Google Scholar
Araújo, C.S.O., Tavares-Dias, M., Gomes, A.L.S., Andrade, S.M., Lemos, J.R.G., Oliveira, A.T., Cruz, W.R. & Affonso, E.G. (2009b) Infecção parasitária e parâmetros sanguíneos em Arapaima gigas Schinz, 1822 (Arapamidae), cultivados no estado do Amazonas, Brasil. pp. 389424 in Tavares-Dias, M. (Ed.) Manejo e sanidade de peixes em cultivo. Macapá, Amapá, Brazil, Embrapa Amapá.Google Scholar
Arguedas-Cortés, D., Dolz, G., Romero-Zúñiga, J., Jiménez-Rocha, A.E. & León-Alán, D. (2010) Centrocestus formosanus (Opisthorchiida: Heterophyidae) como causa de muerte de alevines de tilapia gris Oreochromis niloticus (Perciforme: Cichlidae) en el Pacífico seco de Costa Rica. Revista de Biología Tropical 58, 14531465.Google Scholar
Arredondo-Figueroa, (1983) Especies animales acuáticas de importancia nutricional introducidas en México Biótica 8, 175199.Google Scholar
Avilés-Quevedo, A. & Castello-Orvay, F. (2004) Manual para el cultivo de Seriola lalandi (Pisces: Carangidae) en Baja California Sur de México. México D.F., México, Instituto Nacional de la Pesca.Google Scholar
Azevedo, T.M.P. (2004) Parasitofauna e características hematólogicas de Oreochromis niloticus mantido em sistema de cultivo integrado e intensivo no vale do río Tijucas, Santa Catarina. Dissertation (Maestado em Aquicultura), Universidad Federal de Santa Catarina, Florianopolis.Google Scholar
Balbuena, J.A., Karlsbakk, E. & Kvenseth, A.M. (2000) Growth and emigration of third-stage larvae of Hysterothylacium aduncum (Nematoda: Anisakidae) in larval herring Clupea harengus . Journal of Plankton Research 86, 12711275.Google Scholar
Belmont-Jégu, E., Domingues, M.V. & Martins, M.L. (2004) Notozothecium janauachensis n. sp. (Monogenoidea: Dactylogyridae) from wild and cultured tambaqui Colossoma macropomum (Teleostei: Characidae: Serrasalminae) in Brazil. Zootaxa 736, 18.Google Scholar
Benavides-González, F., Gomez-Flores, R.A., Sánchez-Martinez, J.G., Rábago-Castro, J.L. & Montelongo-Alfaro, I.O. (2014). In vitro and in vivo antiparasitic efficacy of praziquantel against monogenean Ligictaluridus floridanus in Channel Catfish (Ictalurus punctatus ). Thai Journal of Veterinary Medicine 44, 533539.Google Scholar
Bittencourt, L.S., Pinheiro, D.A., Cárdenas, M.Q., Fernandes, B. & Tavares-Dias, M. (2014) Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Brazilian Journal of Veterinary Parasitology 23, 4454.Google ScholarPubMed
Boeger, W.A., Husak, W.S. & Martins, M.L. (1995) Neotropical Monogenoidea. 25. Anacanthorus penilabiatus n. sp. (Dactylogyridae, Anacanthorinae) from Piaractus mesopotamicus (Osteichthyes, Serrasalmidae), cultivated in the State of São Paulo, Brazil. Memorias Instituto Oswaldo Cruz 90, 699701.Google Scholar
Bondad-Reantaso, M., Subasinghe, R., Arthur, J., Ogawa, K., Chinabut, B., Adlard, R., Tan, Z. & Shariff, M. (2005) Disease and health management in Asian aquaculture. Veterinary Parasitology 5, 120.Google Scholar
Buchmann, K., Lindenstrøm, T. & Bresciani, J. (2004) Interactive associations between fish hosts and monogeneans. pp. 161184 in Wiegertjes, G.F. & Flik, G. (Eds) Host–parasite interactions. Oxford, Garland Science/BIOS Scientific Publishers.Google Scholar
Bunkley-Williams, L. & Williams, E.H. (1994) Parasites of Puerto Rican freshwater sport fishes, Puerto Rico. Department of Natural and Environmental Resources, San Juan, PR and Department of Marine Sciences, University of Puerto Rico, Mayaguez, Puerto Rico.Google Scholar
Bunkley-Williams, L. & Williams, E.H. (1995) Parásitos de peces de valor recreativo en agua dulce de Puerto Rico. Departamento de Recursos Naturales y Ambientales y el Departamento de Ciencias Marinas, Universidad de Puerto Rico, Mayaguez, Puerto Rico.Google Scholar
Caldas-Menezes, R., Cursino dos Santos, M., Ceccarelli, P.S., Tavares, L.E., Tortelly, R. & Luque, J.L. (2011) Tissue alterations in the pirarucu, Arapaima gigas, infected by Goezia spinulosa (Nematoda). Brazilian Journal of Veterinary Parasitology 20, 207209.Google Scholar
Cardemil-Rebolledo, C.A. (2012) Estudio exploratorio de parásitos branquiales e intestinales en diferentes especies de peces del lago Yelcho. Thesis, Universidad Austral de Chile, Valdivia, Chile.Google Scholar
Carnevia, D. (1999) Ectoparasitosis diagnosticadas en Carassius auratus (Actinopterygii: Cypriniformes: Cyprinidae), en criaderos comerciales de Uruguay. Boletin I.I.P 17, 5358.Google Scholar
Carnevia, D. (2002) Parásitos y parasitosis diagnosticadas en peces cultivados en Uruguay. Jornada Parasitologica Veterinaria, Montevideo 4345.Google Scholar
Carnevia, D. (2003) Parásitos encontrados en bagre negro, Rhamdia quelen (Pisces, Pimelodidae) cultivados en Uruguay. Acta VII Jornadas Zoologicas, Uruguay 45.Google Scholar
Carnevia, D. & Speranza, G. (2003) Enfermedades diagnosticadas en peces ornamentales tropicales de criaderos de Uruguay. I. Parasitosis. Veterinaria (Montevideo) 38, 2934.Google Scholar
Carvajal, J. & González, L. (1990) Presencia de Hysterothylacium sp. (Nematoda: Anisakidae) en Salmón Coho de Chiloé cultivado en jaulas. Revista de Historia Natural 63, 165168.Google Scholar
Carvajal, J. & González, T. (1995) New record of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda: Anisakidae) in salmonids cultured in sea farms from southern Chile. Research & Reviews 55, 195197.Google Scholar
Castillo-Campo, L.F. (2006) América Latina, un gran futuro. pp. 211228 in Contreras-Sánchez, W.M. & Fitzsimmons, K. (Eds) Proceedings of the 7th International Symposium on Tilapia in Aquaculture, Boca del Río, Veracruz, México.Google Scholar
Castro-Castillo, A. (1980) Estudio sobre Diplostomulum sp. (Trematoda. Diplostomidae) que parasita los ojos de la mojarra amarilla en la estación Piscícola de Repelón. Thesis, Universidad de Bogotá Jorge Tadeo Lozano, Facultadad de Biologia Marina.Google Scholar
Ceccarelli, P.S., Figueira, L.B., Ferraz-Lima, C.L.B. & Oliveira, C.A. (1990) Observações sobre a ocorrência de parasitos no CEPTA entre 1983 e 1990. Boletim técnico do CEPTA 3, 4355.Google Scholar
Centeno, L. & Silva, A. (2002) Fauna ectoparasitaria identificada en ejemplares cultivados de cachama (Colossoma macropomum) y del híbrido cachama × morocoto (C. macropomum × P. brachipomus). Memorias VI Congreso Venezolano de Acuicultura San Cristóbal, p. 45. Venezuela, Edo. Táchira.Google Scholar
Centeno, L., Silva-Acuña, A., Silva-Acuña, R. & Pérez, J.L. (2004) Fauna ectoparasitaria asociada a Colossoma macropomum y al hibrido de Colossoma macropomum × Piaractus brachypomus, cultivados en el estado delta Anacuro, Venezuela. pp. 121126. Universidad Centro-Occidental Lisandro Alvarado Barquisimeto-Cabudare, Venezuela.Google Scholar
Centeno, L., Altuve, D., Gil, H., Matute, H.C., Pérez, J.L., Lunar, J.L.T. & Urbaneja, A. (2006) Evaluación parasitaria y hematológica en peces silvestres del Delta del Río Orinoco, Venezuela. Memorias XIII Congreso Venezolano de Industria y Producción Animal, Venezuela.Google Scholar
Chavarro, G. (1983) Contribución al conocimiento de los Trypanosoma sp. encintados en Prochilodus reticulatus magdalenae Steindachner y Pimelodus clarias. Thesis, Universidad Nalcional de Colombia, Facultad Ciencias, Bogotá.Google Scholar
Chávez-Sánchez, M.C. & Montoya-Rodríguez, L. (2004) Medidas de Bioseguridad para evitar la Introducción y Dispersión de Enfermedades Virales en Granjas Camaronícolas. Avances en nutrición acuícola VII. Memorias del VII Simposium Internacional de Nutrición Acuícola, México.Google Scholar
Cohen, S.C. & Kohn, A. (2005) A new species of Mymarothecium and new host and geographical records for M. viatorum (Monogenea: Dactylogyridae) parasites of freshwater fishes in Brazil. Folia Parasitologica 52, 307310.CrossRefGoogle ScholarPubMed
Comisión Nacional de Acuacultura y Pesca (2008) Anuario Estadístico de Acuacultura y Pesca 2008. Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación, México. Available at www.conapesca.sagarpa.gob.mx/wb/cona/ (accessed July 2016).Google Scholar
Conroy, G. (1999) Principales enfermedades detectadas en tilapias y cachamas de cultivo en Venezuela. pp. 496497 in Memorias IV Congreso Nacional de Ciencias Veterinarias, Maracaibo, Venezuela.Google Scholar
Conroy, G. (2001) Diseases found in tilapia culture in Latin America. Global Aquaculture Advocate 4, 5255.Google Scholar
Conroy, G. (2004) Importantes enfermedades detectadas en tilapias cultivadas en América Latina. Panorama Acuícola 6, 2025.Google Scholar
Conroy, G. & Conroy, D.A. (1998) Enfermedades y Parásitos de Cachamas, Pacus y Tilapias. Documento Técnico (3), Unidad de Diagnóstico y Asesoría Técnica en Patobiología Acuática (UDATPA), Pharma-Fish S. R. L., Maracay, Venezuela.Google Scholar
Conroy, G. & Conroy, D.A. (2008) Importantes enfermedades infecciosas y parasitarias de tilapias cultivadas. Schering-Plough Ltd.Google Scholar
Conroy, D.A. & Vásquez, C. (1975) Principales enfermedades infecto-contagiosas de los salmónidos: una guía a su diagnóstico y control para el Biólogo. pp. 252278. Bogotá, Colombia, INDERENA.Google Scholar
Dambros, A. (2007) Ectoparasitas em Symphysodon discus em aquarios na cidade de Cascavel/PR. Trabalho de Conclusao de Curso, Graduacao em Ciencias Biologicas, Faculdade Assis Gurgacz.Google Scholar
Del Pozo, C.F. (2000) Levantamento ectoparasitológico em brânquias de pacu Piaractus mesopotamicus (Holmberg, 1887) (Osteichthyes, Characidae) em pesque-pagues no município de Campo Grande. Dissertation (Mestrado em Biologia Parasitária), Universidade Federal do Mato Grosso do Sul, Campo Grande, Brasil.Google Scholar
Del Río-Zaragoza, O.B., Fajer-Ávila, E.J. & Almazán-Rueda, P. (2010) Haematological and gill responses to an experimental infection of dactylogyrid monogeneans on the spotted rose snapper Lutjanus guttatus (Steindachner, 1869). Aquaculture Research 110.Google Scholar
Dias, M.K.R., Neves, L.R., Marinho, R.G.B. & Tavares-Dias, M. (2015a) Parasitic infections in tambaqui from eight fish farms in Northern Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 67, 10701076.Google Scholar
Dias, M.K.R., Neves, L.R., Marinho, R.G.B., Pinheriros, D.A. & Tavares-Dias, M. (2015b) Parasitism in tambatinga (Colossoma macropomum × Piaractus brachypomus, Characidae) farmed in the Amazon, Brazil. Acta Amazonica 45, 231238.Google Scholar
Dias, M.L.G., Eiras, J.C., Machado, M.H., Souza, G.T.R. & Pavanelli, G.C. (2003) The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná river, Brazil. Parasitology Research 89, 506508.Google Scholar
Diaz, J.H. (2015) Gnathostomiasis: an emerging infection of raw fish consumers in Gnathostoma nematode-endemic and nonendemic countries. Journal of Travel Medicine 22, 318324.Google Scholar
DOF (2013) Carta Nacional Acuícola. Official Journal of the Federation. 9 September 2013. Available at www.inapesca.gob.mx/portal/publicaciones/carta-nacional-acuicola (accessed 25 March 2016).Google Scholar
Dossman, D. (1976) Los ectoparásitos de los peces de agua dulce del Valle del Cauca. Rupicola Notas 1, 116.Google Scholar
Douëllou, L. (1993) Monogeneans of the genus Cichlidogyrus Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Systematic Parasitology 25, 159186.Google Scholar
Dzikowski, R., Levy, M.G., Poore, M.F., Flowers, J.R. & Paperna, I. (2004) Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. Journal of Parasitology 90, 413414.Google Scholar
Eiras, J.C. (1994) Elementos de ictioparasitologia. 1st edn. Porto, Fundação Eng. Antônio de Almeida.Google Scholar
Eiras, J.C., Dias, M.L.G.G., Pavanelli, G.C. & Machado, M.H. (1999) Histological studies on the effects of Clinostomum marginatum (Digenea: Clinostomidae) in its second intermediate host Loricariichthys platymetopon (Osteichthyes, Loricariidae) of the upper Paraná, Brazil. Acta Scientiarum 21, 237241.Google Scholar
Ernst, I., Whittington, I., Corneille, S. & Talbot, C. (2002) Monogenean parasites in sea-cage aquaculture. Austasia Aquaculture 2, 4648.Google Scholar
Eslava-Mocha, P.R., Verján, N. & Iregui-Castro, C.A. (2001) Platihelmintos (tremátodos) en cultivos de cachama blanca Piaractus brachypomus: aspectos clínicos y patológicos de tratamiento y control. UNILLANOS-IIOC. Revista Orinoquía 5, 138154.Google Scholar
Falcón-Ordaz, J., Monks, S., Pulido-Flores, G., García-Prieto, L. & Lira-Guerrero, G. (2015) Riqueza de helmintos parásitos de vertebrados silvestres del estado de hidalgo, México. Biodiversidad 2, 2037.Google Scholar
FAO (2014) El estado mundial de la pesca y la acuacultura. Oportunidades y desafios. Rome, Food and Agriculture Organization.Google Scholar
FAO (2015) El estado mundial de la pesca y la acuacultura. Oportunidades y desafios. Rome, Food and Agriculture Organization.Google Scholar
FAO (2016) Diagnóstico base para la preparación del plan rector acuícola y pesquero del estado de Yucatán. Mexico, Food and Agriculture Organization.Google Scholar
Fernández, J.A. (1985) Estudio parasitológico de Merluccius australis (Hutton, 1872) (Pisces: Merluccidae): aspectos sistemáticos, estadísticos y zoogeográficos. Boletín de la Sociedad de Biología de Concepción Otile 56, 3141.Google Scholar
Figueira, L.B. & Ceccarelli, P.S. (1991) Observações sobre a presença de ectoparasitas em pisciculturas tropicais de interior (CEPTA e região). Boletim técnico do CEPTA 4, 5765.Google Scholar
FIS México (2016) Outstanding aquaculture growth experienced in Latin America. Available at http://www.fis.com/fis/worldnews/worldnews.asp?l=e&country=0&special=&monthyear=&day=&id=82701&ndb=1&df=0 (accessed 28 March 2016).Google Scholar
Flores-Crespo, J. & Flores-Crespo, C.R. (1993) Principales trematodos y Cestodos de importancia económica en acuicultura. Tópicos de parasitología animal cestodos y trematodos 11, 1336. Universidad Nacional Autonoma del estado Morelos.Google Scholar
Flores-Crespo, J. & Flores-Crespo, R. (2003) Monogeneos, parásitos de peces en México: estudio recapitulativo. Técnica Pecuaria en México 41, 175192.Google Scholar
Flores-Crespo, J., Ibarra, F., Flores-Crespo, R. & Vásquez, C.G. (1992) Variación estacional de Dactilogyrus sp. en dos localidades productoras de tilapia del Estado de Morelos. Técnica Pecuaria en México 30, 109118.Google Scholar
Franceschini, L., Zago, A.C., Schalch, S.H.C., García, F., Romera, D.M. & da Silva, R.J. (2013) Parasitic infections of Piaractus mesopotamicus and hybrid (P. mesopotamicus × P. brachypomus) cultured in Brazil. Revista Brasileira de Parasitologia Veterinaria 22, 407414.Google Scholar
Fujimoto, R.Y., Vendruscolo, L., Schalch, S.H.C. & Morales, F.R. (2006) Avaliação de três diferentes métodos para o controle de monogenéticos e Capillaria sp. (Nematoda: Capillariidae) parasitos de acará-bandeira (Pterophyllum scalare Liechtenstein, 1823). Boletim do Instituto de Pesca 32, 183190.Google Scholar
Galaviz-Silva, L., Molina-Garza, Z.J., Escobar-González, B. & Iruegas-Buentello, F. J. (2013) Metazoan parasites of the channel catfish (Ictalurus punctatus) from three dams in Nuevo Leon, Mexico. Hidrobiológica 23, 394398.Google Scholar
García, F., Fujimoto, R., Martins, M.L. & Morales, F.R. (2003) Parasitismo de Xiphophorus spp. por Urocleidoides sp. e sua relacao co os parametros hidricos. Boletim do Instituto de Pesca 29, 123131.Google Scholar
García, L., Osorio-Sarabia, D. & Constantino, F. (1993) Prevalencia de los parásitos y las alteraciones histológicas que producen a las tilapias de la laguna de Amela, Tecomán, Colima. Veterinaria México 24, 199205.Google Scholar
García-Vásquez, A., Hansen, H., Christison, K.W., Rubio-Godoy, M., Bron, J.E. & Shinn, A.P. (2010) Gyrodactylids (Gyrodactylidae, Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): A pan-global survey. Acta Parasitologica 55, 215229.Google Scholar
García-Vásquez, A., Hansen, H., Christison, K.W., Bron, J.E. & Shinn, A.P. (2011) Description of three new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitizing Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae). Acta Parasitologica 56, 2033.Google Scholar
Ghiraldelli, L., Martins, M.L., Yamashita, M.M. & Jeronimo, G.T. (2006) Ectoparasites influence on the hematological parameters of Nile tilapia and carp cultured in the State of Santa Catarina, Brazil. Journal Fish Aquatic Science 1, 270276.Google Scholar
Golovina, N.A. & Golovin, P.P. (1988) Pathogenicity of Dactylogyrus vastator, for young carp and methods of its evaluation. International Symposium within the Program of Soviet-Finnish Cooperation January, pp. 47–54.Google Scholar
Gonzáles-Fernández, J. (2012a) Parasitofauna of tilapia cause mortalities in fingerlings in two fish farms, Lima, Perú. Neotropical Helminthology 6, 219229.Google Scholar
Gonzáles-Fernández, J. (2012b) Parasite fauna in varieties of the ornamental fish Carassius auratus and description of the biological cycle of Ichthyophthirius multifiliis (Ciliatea Ichthyophthiriidae), causing mortalities in a hatchery from Lima, Perú. Neotropical Helminthology 6, 8595.Google Scholar
González, H., Garrido, V., Martens, P. & Aguirrebeña, R. (1978) Identificación de Diphyllobothrium sp. en especies salmonídeas del lago Rupanco, Chile. Boletín Chileno de Parasitología 33, 2534.Google Scholar
González, M.C. & González, M.D. (1981) Estudios sobre Diplostomum sp. (Trematoda: Diplostomatidae), parásito ocular de cíclidos del Lago de Valencia. Thesis presented in partial fulfilment of the requirements for the degree of ‘Licenciado en Biología’, Universidad Central de Venezuela, Facultad de Ciencias, Escuela de Biología, Caracas, Venezuela.Google Scholar
Guinard-Voelkl, E.M. & Morales-Morales, R.A. (1990) Evaluación de ectoparásitos en peces ornamentales de exportación. Thesis, Universidad Nalcional de Colombia, Facultad de Medicina Veterinaria y Zootecnia, Bogotá.Google Scholar
Gutiérrez-Cabrera, A.E., Pulido-Flores, G., Monks, S. & Gaytán-Oyarzún, J.C. (2005) Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoidea: Bothriocephalidae) in freshwater fishes from Metztitlán, Hidalgo, México. Hidrobiológica 15, 283288.Google Scholar
Herman, J.S. & Chiodini, P.L. (2009) Gnathostomiasis, another emerging imported disease. Clinical Microbiology Reviews 22, 484492.Google Scholar
Hernández-Martínez, M. (1992) Estudio helmintológico de tres especies peces cultivados en dos centros acuícolas del estado de Sonora, México. Universidad y Ciencia 9, 111115.Google Scholar
Hernández-Ocampo, D., Pineda-López, R.F., Ponce-Palafox, J.T. & Arredondo-Figueroa, J.L. (2012) Parasitic helminth infection in tropical freshwater fishes of commercial fish farms, in Morelos State, Mexico. International Journal of Animal and Veterinary Advances 4, 338343.Google Scholar
Jara, C. & Escalante, H. (1983) Parásitos de peces de agua dulce: Dactylogyrus vastator Nibelin y Haliatroma mugilimus Hargis, 1955 (Monogenea: Dactylogyridae) en peces de la provincia de Trujillo-Perú. Hidrobios 7, 2637.Google Scholar
Jeronimo, GT. (2009). Influência da sazonalidade sobre as características hematológicas e incidência de parasitos em Tilápia do Nilo cultivadas em três regiões do Estado de Santa Catarina. Dissertation (Mestrado em Aqüicultura/Centro de Ciências Agrárias), Universidade Federal de Santa Catarina, Santa Catarina.Google Scholar
Jeronimo, G.T., Speck, G.M., Cechinel, M.M., Gonçalves, E.L.T. & Martins, M.L. (2011) Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Brazilian Journal of Biology 71, 365373.Google Scholar
Jiménez, R. (2007) Enfermedades de Tilapia en Cultivo. Universidad de Guayaquil, Facultad de Ciencias Naturales, Proyecto: SENACYT – PIC – 229, Guayaquil, Ecuador. pp. 108.Google Scholar
Jiménez-García, M.I., Vidal-Martínez, V.M. & López-Jiménez, S. (2001) Monogeneans in introduced and native cichlids in México: evidence for transfer. Journal of Parasitology 87, 907909.Google Scholar
Jiménez-Guzmán, F., Galaviz-Silva, L., Segovia-Salinas, F., Garza-Fernández, H. & Wesche-Ebeling, P. (1988) Parásitos y enfermedades del bagre (Ictalurus spp.). Mexico, D.F. Secret, Pesca (in Spanish).Google Scholar
Kaneko, J., Yamada, R., Brock, J.A. & Nakamura, R.M. (1988) Infection of tilapia, Oreochromis mossambicus (Trewavas), by a marine monogenean, Neobenedenia melleni (MacCallum, 1927) in Kaneohe Bay, Hawaii, USA, and its treatment. Journal of Fish Diseases 11, 295300.Google Scholar
Karasev, A.B., Mitenev, V.K. & Kalinina, N.R. (1997) Parasite fauna of cage-reared rainbow trout Oncorhynchus mykiss (Walbaum). Research in freshwater farms (Kola Peninsula, Russia). Bulletin of the European Association of Fish Pathologists 17, 177179.Google Scholar
Khalil, L.F., Robertson, R.D. & Hall, R.N. (1988) Monogenean causing mortality of hybrid cichlids cultured in coastal waters of Southern Jamaica. Abstracts Vth. European Multicolloquium of Parasitology, Budapest, Hungary.Google Scholar
Kritsky, D.C. & Thatcher, V.E. (1974) Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater fishes of Colombia, South America. Journal of Helminthology 48, 5966.Google Scholar
Kritsky, D.C., Vidal-Martínez, V.M. & Rodríguez-Canul, R. (1994 ) Neotropical Monogenoidea 19. Dactylogyridae of Cichlids (Perciformes) from the Yucatán Peninsula, with descriptions of three new species of Sciadicleithrum Kritsky, Thatcher, and Boeger, 1989. Journal of the Helminthological Society of Washington 61, 2633.Google Scholar
Kubitza, F. (2005) Antecipando-se às doenças na tilapicultura. Panorama da Aqüicultura 15, 1523.Google Scholar
Kubitza, L.M. & Kubitza, F. (2000) Principais parasitoses e doenças em tilápia. Panorama Aquicuicola 10, 3953.Google Scholar
Lacerda, A.C.F., Yamada, F.H., Antonucci, A.M. & Tavares-Dias, M. (2013) Peixes introduzidos e seus parasitos. pp. 169193 in Pavanelli, G.C., Takemoto, R.M. & Eiras, J.C. (Eds) Parasitologia de peixes de água doce do Brasil. Maringá, Brasil, Eduern.Google Scholar
Lafferty, K.D., Harvell, C.D., Conrad, J.M., Carolyn, C., Friedman, S., Kent, M.L., Kuris, A.M., Powell, E.N., Rondeau, D. & Saksida, S.M. (2014) Infectious diseases affect marine fisheries and aquaculture economics. Annual Review of Marine Science 7, 126.Google Scholar
Lazaro-Chávez, E. (1985) Analisis patologico de las alteraciones producidas por ectoparasitos en reproductores de Tilapia Sarotherodon hornarum (Trewavas) y Oreochromis mossambicus (Peters). Revista Latinoamericana de Acuicultura 25, 2430.Google Scholar
Leonardo, J.M.L.O., Pereira, J.V.P. & Krajevieski, M.E. (2006) Ocorrência de Ectoparasitas e estacionalidade em Alevinos de tilápiado-Nilo (Oreochromis Niloticus) Após A Reversão Sexual, Na Região Noroeste do Paraná. Iniciação Científica CESUMAR 8, 185191.Google Scholar
Le Roux, L. (2010) Aspects of the morphology, ecology and pathology of Cichlydogyrus philander collected from Pseudocrenilabrus philander philander in the Padda dam South Africa. University of Johannesburg. pp. 103–105.Google Scholar
Lima, H., Stefani, L., Pedron, F., Baldissera, M. & Da Silva, A. (2013) Proinflammatory cytokines in the serum of silver catfish (Rhamdia quelen) naturally infected by Clinostomum complanatum: A preliminary study. Journal of Parasitology 100, 142147.Google Scholar
Lizama, M.A.P., Takemoto, R.M., Rizani-Paiva, M.J.T., Ayroza, L.M.S. & Pavanelli, G.C. (2007a) Relação parasito-hospedeiro em peixes de piscicultura da região de Assis, estado de São Paulo. Brasil. 1. Oreochromis niloticus (Linnaeus 1957). Acta Scientiarum Biological Sciences 29, 223231.Google Scholar
Lizama, M.A.P., Takemoto, R.M., Ranzani-Paiva, M.J.T., Silva-Ayroza, L.M. & Pavanelli, G.C. (2007b) Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. 2. Piaractus mesopotamicus (Holmberg, 1887). Acta Scientiarum Biological Sciences 29, 437445.Google Scholar
López-González, H. (1987) Hallazgos de ectoparásitos en pescado comercializado en la plaza de Paloquemado de Bogotá. Thesis, Universidad Nalcional de Colombia, Facultad Medicina Veterinaria y Zootecnia, Bogotá.Google Scholar
López-Jiménez, S. (1987) Enfermedades más frecuentes de las carpas cultivadas en México. Acuavisión. Revista Mexica de Acuacultura 9, 1113.Google Scholar
López-Jiménez, S. (2001) Estudio parasicológico de los peces de aguas dulces del estado de Tabasco. Gaceta Sigolfo Sistema de Investigación del Golfo de México 810.Google Scholar
Macchi, P. (2004) Respuestas de Galaxias maculatus a la depredación por Percichthys trucha y los salmónidos introducidos en ambientes lénticos de la Patagonia norte. Doctoral thesis, Bariloche, Universidad Nacional del Comahue.Google Scholar
Marengoni, N.G., Santos, R.S., Gonçalves-Júnior, A.C., Gino, D.M., Zerbinatti, D.C.P. & Lima, F.S. (2009) Monogenoidea (Dactylogyridae) em tilápias-do-nilo cultivadas sob diferentes densidades de estocagem em tanques-rede. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 61, 393400.CrossRefGoogle Scholar
Marinho, R.G.B. (2013) Condição de saúde de pirarucus Arapaima gigas (Schinz, 1822) cultivados em Macapá, Estado Do Amapá. Doctoral thesis, Universidade Federal do Amapá, Programa de Pós-Graduação em Biodiversidade Tropical.Google Scholar
Marinho, R.G.B., Tavares-Dias, M., Dias-Grigório, M.K.R., Neves, L.R., Yoshioka, E.T.O., Boijink, C.L. & Takemoto, R.M. (2013). Helminthes and protozoan of farmed pirarucu (Arapaima gigas) in eastern Amazon and host–parasite relationship. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 65, 11921202.Google Scholar
Marinho, R.G.B., Tostes, L.V., Borges, M., Oba-Yoshioka, E.T. & Tavares-Dias, M. (2015) Hemathological responses of Arapaima gigas (Pisces: Arapaimidae) naturally parasited by protozoans and metazoans. Biota Amazónia 5, 105108.Google Scholar
Martins, M.L. (1998) Doenças infecciosas e parasitárias de peixes. 2nd edn. Funep, Brasil, Jaboticabal.Google Scholar
Martins, M.L. & Romero, N.G. (1996) Efectos del parasitismo sobre el tejido branquial em peces cultivados: estúdio parasitológico e histopatologico. Revista Brasilera de Zoologia Curitiba 13, 489500.Google Scholar
Martins, M.L., Onaka, E.M., Moraes, F.R., Bozzo, F.R., Paiva, A.M. & Goncalves, A. (2002) Recentes studies on parasitic infecctions of freshwater cultivated fish in the state of Sao Paulo, Brazil. Acta Scientiarum Animal Sciences 24, 981985.Google Scholar
Martins, M.L., Tavares-Dias, M., Fujimoto, R.Y., Onaka, E.M. & Nomura, D.T. (2004) Haematological alterations of Leporinus macrocephalus (Osteichtyes: Anostomidae) naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 5, 122.Google Scholar
Martins, M.L., Ghiraldelli, L. & Azevedo, T.M.P. (2006) Ectoparasitos de Tilápias (Oreochromis niloticus) cultivadas no Estado de Santa Catarina, Brasil. pp. 253270 in Silva-Souza, A.T. (Eds) Sanidad de organismos acuáticos no Brasil. Maringá, Brasil, Abrapoa.Google Scholar
Martins, M.L., García, F., Piazza, R.S. & Ghiraldelli, L. (2007) Camallanus maculatus n. sp. (Nematoda: Camallanidae) in an ornamental fish Xiphophorus maculatus (Osteichthyes: Peocillidae) cultivated in Sao Paulo State, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59, 12241230.Google Scholar
Mathews, D.P., Chu-Koo, F.W., Tello, M.S., Malta, J.C.O., Varella, A.M.B. & Gomes, S.A.L. (2007) Fauna ectoparasitaria en alevinos de paiche Arapaima gigas (Schinz, 1822) cultivados en el centro de Investigaciones de Quistococha, Loreto, Perú. Folia Amazonica 16, 2327.Google Scholar
Mathews, P.D., Mathews, J.D. & Ismiño, R.O. (2013) Parasitic infections in juveniles of Arapaima gigas (Schinz, 1822) cultivated in the Peruvian Amazon. Annals of Parasitology 59, 4348.Google Scholar
Menezes, R.C., Tortelly, R., Tortelly-Neto, R., Noronha, D. & Pinto, R. M. (2006) Camallanus cotti Fujita, 1927 (Nematoda, Camallanoidea) in ornamental aquarium fishes: pathology and morphology. Memorias Instituto Oswaldo Cruz 101, 683687.Google Scholar
Mitchell, A.J., Salmon, M.J., Huffman, D.G. & Brandt, T.M. (2000) Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two central Texas spring-fed rivers. Journal of Aquatic Animal Health 12, 283289.Google Scholar
Mitchell, A.J., Goodwin, A.E., Salmon, M.J. & Brandt, T.M. (2002) Experimental infection of an exotic heterophyid trematode, Centrocestus formosanus, in four aquaculture fishes. North American Journal of Aquaculture 64, 5559.Google Scholar
Mitchell, J.R., Overstreet, R.M., Goodwin, A.E. & Brandt, T.M. (2005) Spread of an exotic fish-gill trematode: a far-reaching and complex problem. Fisheries 30, 1116.Google Scholar
Molnár, K., Buchmann, K. & Székely, C. (2006) Fish diseases and disorders . pp. 416434 in Molnár, K. (Ed.) Protozoan and metazoan infections. Canada, CABI press.Google Scholar
Monks, S., Zarate-Ramírez, V.R. & Pulido-Flores, G. (2005) Helminths of freshwater fishes from the Metztitlan Canyon Reserve of the Biosphere, Hidalgo, México. Comparative Parasitology 72, 212219.Google Scholar
Mujica, M.E. (1982) Estudios preliminares sobre enfermedades que afectan a los peces de aguas cálidas continentales aptos para el cultivo en la Estación Hidrobiológica de Guanapito, Estado Guárico, Venezuela. Thesis, Universidad Central de Venezuela (UCV), Caracas.Google Scholar
Mujica, M.E. & Armas de Conroy, G. (1985). Una trematodosis en Colossoma macropomum (Cuvier 1881), bajo condiciones de cultivo. Revista Facultad de Ciencias Veterinarias UCV 32, 103111.Google Scholar
Muñoz, J.M. (2001) Identificación y prevalencia de parásitos en las primeras etapas de producción en tilapia nilótica Oreochromis niloticus (Pisces: Cichlidae) cultivada intensivamente, en Cañas, Guanacaste. Postgraduate thesis in Veterinary Science, Universidad Nacional, Heredia, Costa Rica.Google Scholar
Nickol, B.B. & Thatcher, V.E. (1971) Two new Acanthocephalus from neotropical fish Neoechinorhyrenus prochilodorum n. gen. et n. sp. (Trematoda: Haploporidae) from fresh water fish (Prochilodus reticulatus). Transactions of the American Microscopical Society 93, 261264.Google Scholar
Noreña-Serna, A. (1981) Principales enfermedades de peces ornamentales exóticos en criaderos. Thesis, Universidad de Bogotá Jorge Tadeo Lozano, Facultad Biologia Marina.Google Scholar
OIE (2015) Código Sanitario de Animales Acuáticos. 16th edn. Paris, France, Organización Mundial de Sanidad Animal.Google Scholar
Oliva, M.E. (1986) Monogenea in marine fishes from Antofagasta, Chile, with description of Caballerocotyla australis n. sp. (Capsalidae). Revista Chilena de Historia Natural 59, 8794.Google Scholar
Onaka, E.M. (2009) Acompanhamento do estado parasitológico de peixes mantidos em tanques-rede e em ambiente natural nos reservatórios de Nova Avanhandava e Ilha Solteira (SP). In Castellani, D. (Ed.) I Workshop de Piscicultura do Noroeste Paulista; Votuporanga, São Paulo, Brazil.Google Scholar
Ortega, C., Fajardo, R. & Enríquez, R. (2009) Trematode Centrocestus formosanus infection and distribution in ornamental fishes in Mexico. Journal of Aquatic Animal Health 21, 1822.Google Scholar
Ortubay, S.G., Semenas, L.G., Úbeda, C.A., Quaggiotto, A.E. & Viozzi, G.P. (1994) Catálogo de peces dulceacuícolas de la Patagonia Argentina y sus parásitos metazoos. Dirección de Pesca Subsecretaría de recursos Naturales, Provincia de Río Negro, Argentina.Google Scholar
Ostrowski de Núñez, M. (1982) Die Entwicklungs-zyken von Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois, 1970 und D. (A.) mordax (Szidat and Nani, 1951) n. comb. in Südamerika. Zoologischer Anzeiger 208, 393404.Google Scholar
Ozer, A. (2002) Co-existence of Dactylogyrus anchoratus Dujardin, 1845 and D. extensus Mueller & Van Cleave, 1932 (Monogenea), parasites of common carp (Cyprinus carpio). Helminthologia 39, 4550.Google Scholar
Pamplona-Basilio, M.C., Kohn, A. & Feitosa, V.A. (2001) New host records and description of the egg of Anacanthorus penilabiatus (Monogenea, Dactylogyridae). Mememorias del Instituto Oswaldo Cruz 96, 667668.CrossRefGoogle ScholarPubMed
Pantoja, W., Neves, L., Dias, M., Marinho, R., Montagner, D. & Tavares-Dias, M. (2012) Protozoan and metazoan parasites of Nile tilapia Oreochromis niloticus cultured in Brazil. Revista MVZ Córdoba 17, 28122819.Google Scholar
Paperna, I. (1960) Studies on monogenetic trematodes in Israel. 2. Monogenetic trematodes of cichlids. Bamidgeh, Bulletin of Fish Culture in Israel 12, 2033.Google Scholar
Paperna, I. (1996) Parasite, infections and diseases of fishes in Africa. An update. Rome, Food and Agriculture Organization.Google Scholar
Paredes-Trujillo, A., Velázquez-Abunader, I., Torres-Irineo, E., Romero, D. & Vidal-Martínez, V. (2016a) Geographical distribution of protozoan and metazoan parasites of farmed tilapia in Yucatán, México. Parasites & Vectors 9, 6682.Google Scholar
Paredes-Trujillo, A., Velázquez-Abunader, I. & Vidal-Martínez, V. (2016b) The negative effect of Cichlidogyrus sclerosus Paperna & Thurston, 1969 (Monogenea: Dactylogyridae) on the relative condition factor of farmed Tilapia (Oreochromis niloticus) in Yucatan, Mexico. Journal of Parasitology (submitted).Google Scholar
Pavanelli, G.C. & Takemoto, R.M. (1995) New species of Proteocephalus (Cestoda-Proteocephalidae) parasitic in fishes from the Paraná River, Paraná, Brazil. Mememorias del Instituto Oswaldo Cruz 90, 593596.Google Scholar
Pavanelli, G.C., Eiras, C.J. & Takemoto, R.M. (2002) Doencas de peixes: Profilaxia, diagnóstico e tratamento. Maringá, EDUEM.Google Scholar
Pérez-Ponce de León, G., García-Prieto, L., Osorio-Sarabia, D. & León-Regagnon, V. (1996) Listado faunístico de México. Helmintos parásitos de peces de aguas continentales de México. Biodiversitas 37, 711.Google Scholar
Pérez-Ponce de León, G., Rosas-Valdez, G.R., Mendoza-Garfias, B., Aguilar-Aguilar, R., Falcón-Ordaz, J., Garrido-Olvera, L. & Pérez-Rodríguez, R. (2009) Survey of endohelminth parasites of freshwater fishes in the upper Mezquital River basin, Durango state, Mexico. Zootaxa 2164, 120.Google Scholar
Piazza, R., Martins, M.L., Guiraldelli, L. & Yamashita, M.M. (2006) Parasitic diseases of freshwater ornamental fishes commercialized in Florianópolis, Santa Catarina, Brazil. Boletim do Instituto de Pesca 32, 5157.Google Scholar
Pineda-López, R. (1985) Infección por metacercarias (Platyhelminthes: Trematoda) en peces de agua dulce de Tabasco. Universidad y Ciencia 2, 4760.Google Scholar
Pineda-López, R. & González-Enríquez, C. (1997) Bothriocephalus acheilognathi: presencia e importancia de un invasor asiático infectando peces de Querétaro. Zoología Informa 35, 512.Google Scholar
Pinto, H., Mati, V.L.T. & Melo, A.L. (2014) Metacercarial infection of wild Nile tilapia (Oreochromis niloticus) from Brazil. The Scientific World Journal 2014, 17.Google Scholar
Pironet, F.N. & Jones, J.B. (2000) Treatments for ectoparasites as diseases in captive Western Australian dhufish. Aquaculture International 8, 349361.Google Scholar
Portes-Santos, C.P. & Moravec, F. (2009a) Tissue-dwelling philometrid nematodes of the fish Arapaima gigas in Brazil. Journal of Helminthology 83, 295301.Google Scholar
Portes-Santos, C.P. & Moravec, F. (2009b) Goezia spinulosa (Nematoda: Raphidascarididae), a pathogenic parasite of the arapaima Arapaima gigas (Osteichthyes). Folia Parasitologica 56, 5563.Google Scholar
Portes-Santos, C.P., Moravec, F. & Rossana Venturieri, R. (2008) Capillostrongyloides arapaimae sp. n. (Nematoda: Capillariidae), a new intestinal parasite of the arapaima Arapaima gigas from the Brazilian Amazon. Memórias do Instituto Oswaldo Cruz 103, 392395.Google Scholar
Prieto, A., Fajer, E.J. & Vinjoy, M. (1985) Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinidae) en Tilapia hornorum × Tilapia mossambica (perca dorada) en cultivo intensivo. Revista de Salud Animal 7, 291295.Google Scholar
Prieto, A., Fajer, E. & Vinjoy, M. (1991) Manual para la Prevención y el Tratamiento de Enfermedades en Peces de Cultivo en Agua Dulce. Santiago de Chile, Chile, Food and Agriculture Organization, Regional Office for Latin America and the Caribbean.Google Scholar
Rábago-Castro, J. (2010) Monitoreo y distribución de infecciones bacterianas y parasitarias en el cultivo de bagre Ictalurus Punctatus en Tamaulipas. Doctoral thesis, Universidad Autónoma de Nuevo León, Facultad de Ciencias Biológicas, México.Google Scholar
Rábago-Castro, J., Sánchez-Martínez, J.G. & Loredo-Osti, J. (2011) Temporal and spatial variations of ectoparasites on cage-reared channel catfish, Ictalurus punctatus, in Tamaulipas, Mexico. Journal of the World Aquaculture Society 42, 406411.Google Scholar
Rahkonen, R., Aalto, J., Koski, P., Särkkä, J. & Juntunen, K. (1996) Cestode larvae Diphyllobothrium dendriticum as a cause of a heart disease leading to mortality in hatchery reared sea trout and brown trout. Diseases of Aquatic Organisms 25, 1522.Google Scholar
Ranzani-Paiva, M.J.T., Felizardo, N.N. & Luque, J.L. (2005) Parasitological and hematological analysis of the tilapia Oreochromis niloticus Linnaeus, 1757 from Guarapiranga Reservoir, São Paulo State, Brazil. Acta Scientiarum Biological Sciences 27, 231237.Google Scholar
Rego, A.A. (1999) Cestodes in South American freshwater teleost fishes: keys to genera and brief description of species. Revista Brasileira de Zoologia 16, 299367.Google Scholar
Rey-Castaño, A.L. (1999) Casos de diagnóstico en tilapia roja (Oreochromis spp.). Memorias III Jornadas de Acuicultura: Sanidad de Peces. COLCIENCIAS. UNAL. UNILLANOS-IALL, Villavicencio, Meta, Colombia.Google Scholar
Rey-Castaño, A.L., Iregui, C.A. & Verján, N. (2002) Diagnostico clinico patologico de brotes de engfermedad en Tilapia roja (Oreochromis spp.). Revista de Medicina Veterinaria y Zootecnia 49, 1321.Google Scholar
Robinson, R., Khalil, L.F., Hall, R.N. & Steele, R.D. (1992) Infection of red hybrid tilapia with a monogenean in coastal waters off southern Jamaica. Proceedings of the Gulf and Caribbean Fisheries Institute 42, 441447.Google Scholar
Roche, D.G., Leung, B., Franco, E.F.M. & Torchin, M.E. (2010) Higher parasite richness, abundance and impact in native versus introduced cichlid fishes. International Journal for Parasitology 40, 15251530.Google Scholar
Rodríguez-Gómez, H. (1981) Parásitos piscícolas, en aguas continentales de Colombia. Bogotá, D.E. (Colombia), INDERENA, Subgerencia de Pesca y Fauna Terrestre.Google Scholar
Rojas, A. & Wadsworth, S. (2005) Estudio de la acuicultura en jaulas: América Latina y el Caribe. pp. 73104 in Halwart, M., Soto, D. & Arthur, J.R. (Eds) Acuicultura en jaulas. Estudios regionales y panorama mundial. Food and Agriculture Organization, Documento Técnico de Pesca 498. Rome, FAO.Google Scholar
Rozas-Serri, M.A. (2006) Estudio parasitológico de Diphyllobothrium spp. en especies salmonídeas cultivadas intensivamente en Chile. Revista Científica de la Sociedad Española de Acuicultura 25, 17.Google Scholar
Rozas-Serri, M.A., Bohle, H., Sandoval, A., Ildefonso, R., Navarrete, A. & Bustos, P. (2012) First molecular identification of Diphyllobothrium dendriticum plerocercoids from feral rainbow trout (Oncorhynchus mykiss) in Chile. Journal of Parasitology 98, 12201226.Google Scholar
Rubio-Godoy, M., Montiel-Leyva, A. & Martínez-Hernández, J.A. (2011) Comparative susceptibility of two different genetic types of tilapia to Neobenedenia sp. (Monogenea). Diseases of Aquatic Organisms 93, 171177.Google Scholar
Rubio-Godoy, M., Paladini, G., Freeman, M.A., García-Vásquez, A. & Shinn, A.P. (2012a) Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum). Veterinary Parasitology 186, 289300.Google Scholar
Rubio-Godoy, M., Muñoz-Córdova, G., Garduño-Lugo, M., Salazar-Ulloa, M. & Mercado-Vidal, G. (2012b) Microhabitat use, not temperature, regulates intensity of Gyrodactylus cichlidarum long-term infection on farmed tilapia – Are parasites evading competition or immunity? Veterinary Parasitology 183, 305316.Google Scholar
Salas-Benavides, J., López-Macías, J.N., Ortega-Salas, A.L. & Gómez-Nieves, V.Y. (2015) Caracterización parasitaria de la trucha arcoíris (Oncorhynchus mykiss) y su efecto en la producción de la estación piscícola flotante Intiyaco, en el lago Guamuez (Nariño). Veterinaria y Zootecnia 8, 87101.Google Scholar
Salgado-Maldonado, G. (2006) Checklist of helminth parasites of freshwater fishes from Mexico. Zootaxa 24, 1357.Google Scholar
Salgado-Maldonado, G. & Pineda-López, R.F. (2003). The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in México. Biological Invasions 5, 261268.Google Scholar
Salgado-Maldonado, G. & Rubio-Godoy, M. (2014) Helmintos parásitos de peces agua dulce introducidos. pp. 269285. México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.Google Scholar
Salgado-Maldonado, G., Guillen-Hernández, S. & Osorio-Sarabia, D. (1986) Presencia de Bothriocephalus acheilognathi Yamaguti 1934 (Cestoda: Bothriocephalidae) en peces de Patzcuaro, Michoacan, México. Anales del Instituto de Biología, Universidad Nacional Autonoma de México, Serie Zoología 57, 213218.Google Scholar
Salgado-Maldonado, G., Rodriguez-Vargas, M.I. & Campos-Perez, J.J. (1995) Metacercariae of Centrocestus formosanus (Nishigori, 1924) (Trematoda) in freshwater fishes in México and their transmission by the thiarid snail Melanoides tuberculate . Studies on Neotropical Fauna and Environment 30, 245250.Google Scholar
Salgado-Maldonado, G., Pineda-López, R., Vidal-Martínez, V.M. & Kennedy, C.R. (1997) A checklist of metazoan parasites of cichlid fish from México. Journal of the Helminthological Society of Washington 64, 195207.Google Scholar
Salgado-Maldonado, G., Pineda-López, R., García-Magaña, L., López-Jiménez, S., Vidal-Martínez, V.M. & Aguirre-Macedo, L. (2005) Helmintos parásitos de peces dulceacuícolas. pp. 145166 in Bueno-Soria, J., Santiago-Fragoso, S. & Álvarez, F. (Eds) Biodiversidad del estado de Tabasco, México. México, Instituto de Biología. UNAM.Google Scholar
Sanabria-Tamayo, C.M. & Useche-López, R.A. (1995) Determinación de ecto y endoparásitos en híbridos de tilapia roja. Thesis, Universidad Nalcional de Colombia, Facultad de Medicina Veterinaria y Zootecnia, Bogotá.Google Scholar
Sánchez-Páez, C.L. (1993) Evalución preliminar de ectoparásitos en Oreochromis niloticus y control de los mismos en condiciones de cultivo. Thesis, Universidad de Bogotá Jorge Tadeo Lozano, Facultad de Biologia Marina, Bogotá.Google Scholar
Sánchez-Ramirez, C., Vidal-Martínez, V.M., Aguirre-Macedo, L., Rodriguez-Canul, R. & Gold-Bouchot, B. (2007) Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinae) and its host, the Nile tilapia (Oreochromis niloticus), as bioindicators of chemical pollution. Journal of Parasitology 93, 10971106.Google Scholar
Sánchez-Serrano, S. & Cásares-Martínez, J. (2011) Registro helmintológico en el atún aleta azul del norte (Thunnus thynnus orientalis) de la costa del Pacífico mexicano. Ciencia Pesquera 19, 512.Google Scholar
Sandoval-Gío, J.J., Rodríguez-Canul, R. & Vidal-Martínez, V.M. (2008) Humoral antibody response of the tilapia Oreochromis niloticus against Cichlidogyrus spp. (Monogenea). Journal of Parasitology 94, 404409.Google Scholar
Santos, C.P., Buchmann, K. & Gibson, D.I. (2000) Pseudorhabdosynochus spp. (Monogenea: Diplectanidae) from the gills of Epinephelus spp. in Brazilian waters. Systematic Parasitology 45, 145153.Google Scholar
Santamaría, J.D. & Medina, F.A. (2000) Estimación de la prevalencia e intensidad de parásitos internos y externos en la Tilapia (Oreochromis nitoticus) en la granja piscícola UNA-ADPESCA, Managua, Nicaragua. Thesis, Universidad Nacional Agraria, Nicaragua.Google Scholar
Sarmiento, J. & Rodríguez, A. (2013) Lerneosis en alevinos de Prochilodus magdalenae, Prochilodontidae, cultivados en laboratorio. Revista Intropica 8, 99103.Google Scholar
Scholz, T. (1999) Parasites in cultured and feral fish. Veterinary Parasitology 5, 317335.Google Scholar
Scholz, T. & Salgado-Maldonado, G. (2000) The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review. American Midland Naturalist 143, 185200.Google Scholar
Semenas, L. (1998) Primer registro de Diplostomiasis ocular en trucha arcoíris cultivada en Patagonia Argentina. Archivo Medico Veterinario 30, 165170.Google Scholar
Sepulveda, F., Marin, S. & Carvajala, J. (2004) Metazoan parasites in wild fish and farmed salmon from aquaculture sites in southern Chile. Aquaculture 23, 89100.Google Scholar
Serrano-Martínez, E., Tantaleán, M., Leguía, G., Quispe, M. & Casas, G.C. (2015) Parasites in Arapaima gigas from the Peruvian Amazon by age group. Revista de Investigaciones Veterinarias del Perú 26, 303309.Google Scholar
Shinn, A.P., Pratoomyot, J., Bron, J.E., Paladini, G., Brooker, E. & Brooker, A.J. (2015) Economic costs of protistan and metazoan parasites to global mariculture. Parasitology 142, 196270.Google Scholar
Silva, A.S., Monteiro, S.G., Doyle, R.L., Pedron, F.A., Filipetto, J.E. & Radunz-Neto, J. (2008) Ocorrência de Clinostomum complanatum em diferentes espécies de peixes de uma piscicultura do Município de Santa Maria – RS. Veterinaria e Zootecnia 15, 2732.Google Scholar
Silva, A.S., Pedron, F.A., Zanette, R.A., Monteiro, S.G. & Radünz Neto, R. (2009) Eficácia do praziquantel no controle ao parasito Clinostomum complanatum Rudolphi, 1918 (Digenea, Clinostomidae) em peixes da espécie Rhamdia quelen Quoy & Gaimard, 1824. Pesquisa Agropecuária Gaúcha 15, 7376.Google Scholar
Silva, O.A.M., Tavares-Dias, M. & Fernandes, J.S. (2011) Helminthes parasitizing Semaprochilodus insignis Jardine, 1841 (Osteichthyes: Prochilodontidae) from the central Amazonia (Brazil), and their relationship with the host. Neotropical Helminthology 5, 225233.Google Scholar
Silva, O.A.M., Tavares-Dias, M., Maycon, W.R.D., Dias, M.K.R. & Marinho, R.G.B. (2013) Parasitic fauna in hybrid tambacu from fish farms. Pesquisa Agropecuária Brasileira 48, 10491057.Google Scholar
Soler-Jiménez, L.C., Morales-Serna, F. & Fajer-Ávila, E.J. (2015) Rapid infection and proliferation of dactylogyrid monogeneans on gills of spotted rose snapper (Lutjanus guttatus) after transfer to a sea-cage. Veterinary Parasitology 210, 186193.Google Scholar
Sutili, F.J., Gressler, L.T. & Vilani de Pelegrini, L.F. (2014) Clinostomum complanatum (Trematoda, Digenea): a parasite of birds and fishes with zoonotic potential in southern Brazil. A review. Revista Brasileira de Higiene e Sanidade Animal 8, 99114.Google Scholar
Szidat, L. (1969) Structure, development and behavior of new strigatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753786.Google Scholar
Tancredo, K.R., Marchiori, N., Roumbedakis, K., Cerqueira, V.R., Tavares-Dias, M. & Martins, M. (2015) Observations on parasite fauna of Centropomus undecimalis and C. parallelus (Perciformes) bred in southern Brazil, and its possible influence on the welfare of fishes. Pan-American Journal of Aquatic Sciences 10, 116121.Google Scholar
Tanzola, R.D., Semanas, L. & Viozzi, G. (2009) Manejo y estado actual del conocimiento de los parásitos de peces cultivados en Argentina. pp. 438468 in Tavares-Dias, M. (Ed.) Manejo e sanidade de peixes em cultivo. Brasil, Embrapa Amapá.Google Scholar
Tavares-Dias, M., Moraes, F.R., Martins, M.L. & Kronka, S.N. (2001) Parasitic fauna of cultivated fishes in feefishing farm of Franca, State of Sao Paulo, Brazil. II. Metazoans. Revista Brasileira de Zoologia 18, 8195.Google Scholar
Tavares-Dias, M., Lemos, J.R.G. & Andrade, S.M.S. (2006) Ocorrência de ectoparasitos em Colossoma macropomum Cuvier, 1818 (Characidae) cultivados em estação de pisciculturas na Amazônia Central. Congreso Iberoamericano Virtual de Acuicultura 4, 726731. Available at http://www.revistaaquatic.com/civa2006/coms/completo.asp?cod=150 (accessed 30 March 2016).Google Scholar
Tavares-Dias, M., Hernandez, L.E. & Bashirullah, A.K. (2008) Studies on the life cycle of Haplorchis pumilio (Looss, 1896) (Trematoda: Heterophyidae) in Venezuela. Revista Científica, FCV-LUZ 18, 3542.Google Scholar
Tavares-Dias, M., Lemos, J.G., Martins, M.L. & Jeronimo, G.T. (2009a) Metazoan and protozoan parasites of freshwater ornamental fish from Brazil. pp. 469494 in Tavares-Dias, M. (Ed.) Manejo e sanidade de peixes em cultivo. Brasil, Embrapa Amapá.Google Scholar
Tavares-Dias, M., Brito, M.L.S. & Lemos, J.G. (2009b) Protozoários e metazoarios parasitos do cardinal Paracheirodon axelrodi Schultz, 1956 (Characidae), peixe ornamental proveniente de exportador de Manaus, Estado do Amazonas, Brasil. Acta Scientiarum Biological Sciences 31, 2328.Google Scholar
Thatcher, V.E. (1981) Patologia de peixes da Amazônia brasileira, 1. Aspectos gerais. Acta Amazonica 11, 125140.Google Scholar
Thatcher, V.E. (1993) Trematódeos neotropicais. Manaos (Amazonas) Brasil, Instituto Nacional de Pesquisas da Amazônia.Google Scholar
Thatcher, V.E. & Dossman, D. (1974) Lecithobotrioides mediacanoensis n. gen. et n. sp. (Trematoda: Haploporidae) from fresh water fish (Prochilodus reticulatus). Transactions of the American Microscopical Society 93, 261264.Google Scholar
Thatcher, V.E. & Dossman, D. (1975) Unicoelium prochilodorum n. gen. et n. sp. (Trematoda: Haploporidae) from freshwater fish (Prochilodus reticulatus) in Colombia. Journal of the Helminthological Society of Washington 42, 2830.Google Scholar
Thatcher, V.E. & Padilha, T.N. (1977) Spinitectus jamundensis sp. n. (Nematoda: Spiruroidea) from a Colombian freshwater fish (Prochilodus reticulatus). Revista Brasileira de Biologia 37, 799801.Google Scholar
Torres, P. (1995) Some trematode, nematode, and acanthocephalan parasites of rainbow trout, Oncorhynchus mykiss, introduced into Chile. Journal of the Helminthological Society of Washington 62, 257259.Google Scholar
Torres, P., Cabezas, X., Arenas, J., Miranda, J.C., Jara, C. & Gallardo, C. (1991a) Ecological aspects of nematode parasites of introduced salmonids from Valdivia River basin, Chile. Memorias do Institute Oswaldo Cruz 86, 115122.Google Scholar
Torres, P., Cubillos, W., Gesche, C., Rebolledo, A., Montefusco, C., Miranda, J., Arenas, A., Mira, M., Nilo, M. & Abello, C. (1991b) Difilobotriasis en salmonidos introducidos en lagos del sur de Chile: Aspectos patologicos, relacion con infection humana, animales domesticos y aves piscivoras. Archivos de Medicina Veterinaria 23, 165183.Google Scholar
Torres, P., Contreras, A., Revenga, J. & Fritz, N. (1993) Helminth parasites in fishes from Valdivia and Tornagaleones river estuaries in the south of Chile. Memorias do Instituto Oswaldo Cruz 88, 1623.Google Scholar
Torres, P., Gesche, W., Montefuso, A., Miranda, J.C, Dietz, P. & Huijse, R. (1998) Diphyllobothriasis in man and fishes from lake Rinihue, Chile: effect of health education, seasonal distribution and relationship to sex, size and diet of the fish. Archivo de Medicina y Veterinaria 30, 3145.Google Scholar
Torres, P., Aedo, E., Figueroa, A., Siegmun, I., Silva, B., Navarrete, N., Puga, S., Marín, F. & Aedo, E. (2000) Infección por helmintos parásitos en salmón coho, Oncorhynchus kisutch, durante su retorno al río Simpson, Chile. Boletín Chileno de Parasitología 12, 123127.Google Scholar
Torres, P., Lopez, J., Cubillos, V., Lobos, C. & Silva, R. (2002a) Viceral diphyllobothriosis in a cultured rainbow trout, Oncorhynchus mykiss (Walbaum), in Chile. Journal of Fish Disease 25, 375379.Google Scholar
Torres, J., Castillo, O., Cortez, G., Bravo, J. & Fortine, M. (2002b) Prevalencia de tremátodos monogenesicos branquiales en cachamas Colossoma macropomum de la Estacion Piscicola Papelon. VI Congreso Venezolano de Acuicultura, San Cristobal, Venezuela. Summaries, pp. 51.Google Scholar
Trujillo, A.A.P. (1987) Monogeneos (Platyhelmintes) parasitos de peces de interes comercial sometidos a cultivo intesivos en Cuba: sistematica, patologia y control . Thesis (Doutorado en Ciencias), Habana, Instituto Superior de Ciencias Agropecuarias de la Habana.Google Scholar
Urquia, C. (1997) Control de enfermedades de Cachama en granjas de Venezuela. Revista Cubana de Investigaciones Pesqueras 21, 6064.Google Scholar
Varella, A.M.B., Peiro, S.N., Malta, J.C.O. & Lourenco, J.N.P. (2003) Monitoramento da paritofauna de Colossoma macroporum (Cuvier, 1818) (Osteichthyes: Characidae) cultivado en tanque-rede em um lago de várzea na Amazonia, Brasil. Simposio Brasileiro de Aquicultura 12, 95106.Google Scholar
Velázquez-Velázquez, E., González-Solis, D. & Salgado-Maldonado, G. (2011) Bothriocephalus acheilognathi (Cestoda) in the endangered fish Profundulus hildebrandi (Cyprinodontiformes), Mexico. Revista de Biología Tropical 59, 10991104.Google Scholar
Vélez-Hernández, E.M., Constantino-Casas, F., García-Márquez, L.J. & Osorio-Sarabia, D. (1998) Gill lesions in common carp, Cyprinus carpio L., in Mexico due to the metacercariae of Centrocestus formosanus . Journal of Fish Diseases 21, 229232.Google Scholar
Vianna, R.T., Pereira, J.J. & Brandão, D.A. (2005) Clinostomum complanatum (Digenea, Clinostomidae) density in Rhamdia quelen (Siluriformes, Pimelodidae) from South Brazil. Brazilian Archives of Biology and Technology 48, 635642.Google Scholar
Vidal-Martínez, V.M. (1995) Process structuring the helminth communities of native cichlid fishes from Southern Mexico. Doctoral thesis, University of Exeter, Exeter, England.Google Scholar
Vidal-Martínez, V.M. (2012) Disease diagnosis and reporting for aquatic animals in OIE member countries in the Americas. Proceedings of the OIE Global conference on aquatic animal health programmes. Their benefits for global food security, 28–30 June 2011, Panamá, Panamá, pp. 4552.Google Scholar
Vidal-Martínez, V.M., Kennedy, C.R. & Aquirre-Macedo, M.L. (1998) The structuring process of the macroparasite community of an experimental population of Cichlasoma urophthalmus through time. Journal of Helminthology 72, 199207.Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Scholz, T., González-Solís, D. & Mendoza-Franco, E. (2001) Atlas of the helminth parasites of cichlid fish of México. Praga, Academia.Google Scholar
Violante-González, J., García-Varela, M., Rojas-Herrera, A. & Guerrero, S.G. (2009) Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, México. Parasitology Research 105, 803807.Google Scholar
Vogelbein, W.K. & Overstreet, R.M. (1988) Life-history and pathology of a heterophyid trematode infecting Florida-reared ornamental fishes. International Association for Aquatic Animal Medicine Proceedings 19, 138.Google Scholar
Vogelsang, E.G. (1929) Enfermedades de peces en el Uruguay. Anales Escuela Veterinaria Uruguay 1, 6769.Google Scholar
Von Bonsdorff, B. (1977) Diphyllobothriasis in man. 2nd edn. pp. 1–189. New York, Academic Press.Google Scholar
Waicheim, A., Blasetti, G., Cordero, P., Rauque, C. & Viozzi, G. (2014) Macroparasites of the invasive fish, Cyprinus carpio, in Patagonia, Argentina. Comparative Parasitology 81, 270275.Google Scholar
Whittington, I.D. (2005) Monogenea Monopisthocotylea (ectoparasitic flukes). pp. 6372 in Rohde, K. (Ed.) Marine parasitology. Melbourne, Australia, CABI.Google Scholar
Whittington, I.D., Corneillie, S., Talbot, C., Morgan, J.A. & Adlard, R.D. (2001) Infections of Seriola quinqueradiata Temminck & Schlegel and S. dumerili (Risso) in Japan by Benedenia seriolae (Monogenea) confirmed by morphology and 28S ribosomal DNA analysis. Journal of Fish Diseases 24, 421425.Google Scholar
Yagi, K., Nagasawa, K., Ishikura, H., Nakagawa, A., Sato, N. & Kikuchi, K. (1996) Female worm Hysterothylacium aduncum excreted from human: a case report. Japanese Journal of Parasitology 45, 1223.Google Scholar
Zago, A.C., Franceschini, L., García, F., Canello Schalch, S.E., Gozi, K.S. & Silva, R.J.D. (2014) Ectoparasites of Nile tilapia (Oreochromis niloticus) in cage farming in a hydroelectric reservoir in Brazil. Revista Brasilera de Parasitologia Veterinaria 23, 171178.Google Scholar
Zanolo, R. & Yamamura, M.H. (2006) Parasitas em tilápias do Nilo criadas em sistema de tanques-rede. Semina: Ciencias Agrararias 27, 281288.Google Scholar
Zanolo, R., Leonhardt, J.H., Silva e Souza, A.T. & Yamamura, M.H. (2009) The influence of branchial parasitism by monogenoid trematodes on the development of Nile tilapia (Oreochromis niloticus) Linnaeus, 1757 bred in net-pond systems in Capivara Dam, PR. Revista Brasilera de Parasitologia Veterinaria 18, 4752.Google Scholar
Figure 0

Table 1. Helminth species recorded from salmonid species farmed in Latin America.

Figure 1

Table 2. Helminth species recorded from farmed tilapia species in Latin America.

Figure 2

Table 3. Helminth species recorded from carp species farmed in Latin America.

Figure 3

Table 4. Helminth species recorded from freshwater native fish species farmed in Latin America. G = groups of parasites, as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala, H = Hirudinea.

Figure 4

Table 5. Helminth species recorded from seawater native fish species farmed in Latin America. Groups of parasites (G) were as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala.

Figure 5

Table 6. Helminth species recorded from ornamental fish species farmed in Latin America. G = groups of parasites, as follows: M = Monogenea, D = Digenea, N = Nematode, C = Cestode, A = Acanthocephala.

Figure 6

Table 7. Multivariate regression analysis using the percentage of mortality as a dependent variable, and the best 12 environmental and management independent variables (out of 45 variables) (see supplementary table S1) selected by a stepwise procedure. The coefficient of determination of this model was R2 = 0.71 for N = 399. The best regression model was chosen based on the lowest values of the CpMallows (model selection method) and variance inflation factor (VIF) statistics. The maximum P value for each variable to entry the model was 0.01, and the maximum value for retention of the variable was 0.05. The normality of all variables was verified using Wilk–Shapiro rankit plots (WS), and if normality was not attained (WS > 0.8), then the variables were transformed to natural logarithms + 1.

Supplementary material: File

Soler-Jiménez supplementary material

Supplementary Table

Download Soler-Jiménez supplementary material(File)
File 253.6 KB