Current knowledge of trematodes (Platyhelminthes:

Digenea, Aspidogastrea) in Chile

Authors: Oyarzún-Ruiz, Pablo, and González-Acuña, Daniel

Source: Revue suisse de Zoologie, 129(1) : 1-17
Published By: Muséum d'histoire naturelle, Genève
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 Revue suisse de Zoologie (March 2022) 129(1): 1-17 ISSN 0035-418

Current knowledge of trematodes (Platyhelminthes: Digenea, Aspidogastrea) in Chile

Pablo Oyarzún-Ruiz1,2* & Daniel González-Acuña1

1
Laboratorio de Parásitos y Enfermedades en Fauna Silvestre, Facultad de Ciencias Veterinarias, Universidad de
Concepción, Chillán, Chile
2
Becario ANID Programa de Doctorado en Ciencias Veterinarias, Facultad de Ciencias Veterinarias, Universidad de
Concepción, Chillán, Chile
* Corresponding author: pablooyarzunruiz@[Link]

Abstract: The aim of the present review was to evaluate the state of knowledge of trematodes (Platyhelminthes:
Trematoda) in Chile, covering taxonomy, biology, geographic distribution, and a checklist of all taxa reported in the
country. A total of 277 articles published between 1849 and December 2020, have been analyzed. A total of 215 taxa
belonging to the subclasses Digenea and Aspidosgastrea have been reported from Chile, 119 of them identified to species
level and only three species with completely described life cycles. Trematodes from Chile were found parasitizing both
native and exotic species, however, no records from insects and most crustacean classes exist. Overall, 159 out of 3989
potential host native species were reported as hosts for trematodes. Molecular tools were used in more recent taxonomic
studies. Although research on trematodes in Chile is on the rise, there is a clear need for more detailed taxonomic studies
to include integrative taxonomy approach, deposition of helminths in collections and the training of new generation of
parasitologists to better understand the diversity, ecology and evolutionary relationships of trematodes in the region.

Keywords: Trematoda, Digenea, Aspidogastrea, biodiversity, checklist.

INTRODUCTION and summarize of knowledge on their diversity, taxo-

nomy, biology, and geographic distribution. We also
The class Trematoda is subdivided in two subclasses,
outline the areas most urgently needing, attention and/or
Aspidogastrea and Digenea. The former group is small
improvement in future research.
and comprises only four families, 12 genera and about
80 species (Roberts et al., 2013; Collins, 2017). On
the other hand, digeneans are a very diverse group of
MATERIAL AND METHODS
parasites with more than 2500 genera and 18 000 nominal
species (Kostadinova & Pérez-del-Olmo, 2014; Collins, Literature search
2017). However, there is a significant number of yet
We performed an exhaustive bibliographic review of
undescribed species, with some estimates suggesting that
trematodes reported from domestic and wild animals,
the total number of digenean species may exceed 44 000
including humans, in Chile. Data from freshwater,
(Carlson et al., 2020a).
marine and terrestrial environments, and all invertebrate
Gay (1849) was the first to mention a trematode
and vertebrate hosts were included in this review.
in Chile. It was a report of the liver fluke Fasciola
To achieve this objective, we analyzed 275 research
hepatica (Fasciolidae) in cattle. Since then, trematodes
articles, one book and one book chapter from physical
have been reported from a variety of hosts across the
libraries and electronic databases such as NCBI,
country. Previously published checklists were restricted
ScholarGoogle, Scopus and Web of Science (WOS).
to particular groups of hosts or types of ecosystems
The time cut-off for the published data was until
(see Garín & González-Acuña, 2008; Muñoz & Olmos,
December 2020. The present review did not consider
2008; Oyarzún-Ruiz & González-Acuña, 2021), while
“grey” literature (i.e. technical reports, conference
an overview covering the whole trematode fauna in
proceedings, congress posters, theses) because they are
the country is currently lacking. The aim of the present
not subjected to a peer review process.
review was to analyze the data on trematodes in Chile

Manuscript accepted 23.08.2021

DOI: 10.35929/RSZ.0059
Appendices 1 and 2 are available as supplementary material S1
DOI: 10.35929/RSZ.0059.S1

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 2 P. Oyarzún-Ruiz & D. González-Acuña

Taxonomy of hosts and parasites 73°31’14.417’’ W), XII= Magallanes y de la Antártica

Chilena region (53°21’9.906’’ S 71°33’17.201’’ W).
The taxonomic classification for host species was
stated as follows: AviBase ([Link]
for birds; FishBase ([Link]
RESULTS
php) for fishes; GBIF ([Link] and ITIS
(Integrated Taxonomic Information System; https:// Over the last 120 years, there is a clear tendency for the
[Link]/), in this order of priority, for freshwater increase of number of publications reporting trematodes
mollusks, reptiles, amphibians and mammals; and in Chile, with a first peak in the 1980s and a second peak
WoRMS (World Register of Marine Species; http:// in the 2010s (Fig. 1).
[Link]/) and SeaLifeBase (https://
[Link]/), in this order of priority, for
marine mollusks and crustaceans. We followed Gibson Trematodes
et al. (2002), Jones et al. (2005), Bray et al. (2008), A total of 215 taxa of trematodes belonging to two
Roberts et al (2013), GBIF and WoRMS for the subclasses, three orders, 47 families and 127 genera
taxonomy of trematodes. have been recorded in Chile. Of these, 119 (55.35 %;
119/215) taxa were identified to species level, with three
species belonging to Aspidogastrea subclass and 116 to
Hosts Digenea subclass (Table 1).
The most common digenean families mentioned for
The categorization of hosts as native, endemic, or exotic
particular host groups were Fellodistomidae for mollusks,
species followed Ministerio de Medio Ambiente (MMA,
Microphallidae for crustaceans, Opecoelidae for fishes,
2018a, b) and PNUD (2017). In addition, the diversity
Gorgoderidae for amphibians, Echinochasmidae
of native, endemic, and exotic animal species for
and Echinostomatidae for birds, and Fasciolidae for
every host group present in Chile was stated according mammals. Only family Opisthogonimidae was reported
to Valdovinos (1999), Martínez & González (2017), from reptiles.
PNUD (2017) and Ministerio de Medio Ambiente Complete life cycles are known for only 3 out 119
(2018a, b; [Link] species of trematodes reported in the country, namely
Fasciola hepatica, Proctoeces lintoni (Fellodistomidae)
and Prosorhynchoides carvajali (Bucephalidae).
Locations
The collection sites were attributed to Chilean regions
represented by roman numbers and ordered according Hosts
its geographical distribution from northern Chile Trematodes were reported from 159 out of 3989
to Chilean Patagonia following the Biblioteca del potential native animal species (including 14 out of
Congreso Nacional de Chile (BCN) ([Link] 1081 endemic species) and 12 out of 92 exotic animal
cl/siit/mapoteca/regiones) and Ministerio de Medio species known in Chile (Table 2). So far, there are
Ambiente (MMA) (2018a): (i) Northern Chile: XV= no records of trematodes from insects or classes of
Arica y Parinacota region (18°22’4.8’’ S 70°13’1.199’’ crustaceans other than Malacostraca.
W), I= Tarapacá region (20°9’49.202’’ S 69°32’46.841’’ The highest diversity of trematodes was found in
W), II= Antofagasta region (23°36’14.873’’ S representatives of the following host orders: Mytilida (9
69°5’3.401’’ W), III= Atacama region (27°33’25.842’’ taxa) in mollusks, order Decapoda (3 taxa) in crustaceans,
S 70°0’56.477’’ W), IV= Coquimbo region order Perciformes (75 taxa) in fishes, order Anseriformes
(30°45’16.795’’ S 70°54’1.992’’ W); (ii) Central Chile: (21 taxa) in birds, and orders Carnivora and Cetacea (7
V= Valparaíso region (32°35’51.392’’ S 70°51’10.711’’ taxa each) in mammals. One order of reptiles and one
W), RM= Metropolitan region (33°30’13.172’’ S order of amphibians were reported as hosts.
70°45’44.692 W), VI= Libertador General Bernardo
O’Higgins region (34°32’4.337’’ S 71°2’7.735’’ W),
VII= Maule region (35°35’50.022’’ S 71°29’19.248’’ Geographical distribution
W); (iii) Southern Chile: XVI= Ñuble region Taxonomic diversity of trematodes at family level
(36°37’13.518’’ S 72°6’5.983’’ W), VIII= Biobío region across different regions of Chile is presented in Figs
(37°20’20.907’’ S 72°24’38.456’’ W), IX= Araucanía 2-4. A total of 428 records were plotted for all trematode
region (38°40’4.424’’ S 72°15’39.623’’ W), XIV= families. These records represent the sum of all taxa
Los Ríos region (39°58’27.448’’ S 72°40’2.92’’ W), reported for every trematode family in every region of
X= Los Lagos region (42°18’3.038’’ S 73°6’19.393’’ the country. Our analysis showed certain patterns in the
W); (iv) Chilean Patagonia: XI= Aysén del General distribution of several digenean families. For instance,
Carlos Ibáñez del Campo region (46°28’16.16’’ S families Allocreadidae, Brauninidae, Dicrocoeliidae,

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 Trematodes in Chile 3

Fig. 1. Temporal tendendy in the number of publications related to trematodes in Chile.

Table 1. Parasitic taxa isolated from each host group.

Moll‡ Crus Fishes* Am Rep Birds Mam

Species 8 1 74 3 0 27 17
New species 3† 1† 22 3 0 0 3
Incompletely described 21 4 59 0 1 14 5
Genus sp. 7 0 49 0 1 11 4
Family gen. sp. 10 2 9 0 0 3 0
Subfamily gen. sp. 0 2 0 0 0 0 0
incertae sedis 4 0 1 0 0 0 1

Symbols and abbreviations: Moll= Mollusks; Crus= Crustaceans; Am= Amphibians; Rep= Reptiles; Mam= Mammals;
‡Including classes Gastropoda and Bivalvia; *including classes Actinopterygii, Holocephali and Elasmobranchii; †These
species were also described from fishes.

Himasthlidae, Multicalycidae, Phaneropsolidae and Checklist

Pleurogenidae have been recorded only in Southern
The checklist of the trematodes and their associated
Chile. Meanwhile, the Fasciolidae has been reported
hosts is provided in the Appendix 1 [supplementary
throughout the entire country.
material S1]. The stage of development, parasitized
The highest diversity of trematodes was recorded on
organs, localities and references are also stated.
Biobío region (VIII), Southern Chile, with 98 taxa
An additional table provides a host-parasite list the
belonging to 36 families, followed by Valparaíso region
Appendix 2 [supplementary material S1].
(V), Central Chile, with 62 taxa belonging to 20 families.
On the other hand, the region with the lower diversity of
trematodes was Libertador General Bernardo O’Higgins
region (VI), Central Chile, with only 1 taxon (see Fig. 3).

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 4 P. Oyarzún-Ruiz & D. González-Acuña

Table 2. Number of host species per host group in Chile (top 3 rows), and number and percentage, between parenthesis, of recorded
species hosting trematodes in Chile (bottom 3 rows).

Moll Crus Fishes Am Rep Birds Mam† Total

Native species 1187 606 1401 57 135 443 160 3989
biodiversity
Hosts

Endemic species 886 21 35 34 82 10 13 1081

Exotic species 35 0 26 1 2 9 19 92
Native species 24 (2.02) 12 (1.98) 84 (6.00) 3 (5.26) 1 (0.74) 19 (4.29) 16 (10.00) 159 (3.99)
Review
Present

Endemic species 0 0 9 (25.71) 2 (5.88) 1 (1.22) 0 2 (15.38) 14 (1.30)

Exotic species 0 0 2 (7.69) 0 0 0 10 (52.63) 12 (13.04)

Abbreviations: Moll= Mollusks; Crus= Crustaceans; Am= Amphibians; Rep= Reptiles; Mam= Mammals; †= excluding human being.

Fig. 2. Number of taxa per trematode family in Northern Chile (NC). Every color in the pie chart represents a particular family.
The highest number of taxa for trematode families in every region is given between parentheses. The name of every region
represented as a roman number is detailed in Material and Methods.

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 Trematodes in Chile 5

Fig. 3. Number of taxa per trematode family in Central Chile (CC) and Southern Chile (SC), regions XVI, VIII and IX. Every color
in the pie chart represents a particular family. The highest number of taxa for trematode families in every region was stated
between parentheses. The name of every region represented as a roman number is detailed in Material and Methods.

DISCUSSION in Chile should be considered with caution (Valdivia

et al., 2010; Oliva et al., 2018). The same is true for
A significant trematode diversity has been recorded
from Chile since the first publication by Gay (1849). Helicometrina nimia (Opecoelidae), another European
However, the identification of a number of reported taxa fluke reported in Chile, which needs additional analysis
is questionable, therefore, the collection of new quality to establish its identity (Oliva et al., 2015).
specimens as well as the thorough re-examination of Although complete life cycles are known for only
specimens deposited in museums are necessary. A 3 species of digeneans reported from Chile, larval
number of species reported from Chile do not have stages of some other species have been reported. For
descriptions or illustrations. For instance, Proctoeces instance, metacercariae of Stephanoprora uruguayense
lintoni (Fellodistomidae) (originally described from (Echinochasmidae), parasitic as an adult in seabirds,
Europe) was reported in native fishes from Chile without have been reported from two native fish species (Torres
adequate descriptions (Valdivia et al., 2010; Oliva et al., et al., 1982, 1983, 1991, 1992a, 1993a, 2017; Viozzi
2018). In the absence of DNA sequence data, comparisons et al., 2008). Although in Chile the first intermediate
with the two native species from Chile, P. humboldti host of this digenean remains unknown, aquatic snails
and P. sicyases, is not possible (George-Nascimento & of family Hydrobiidae have been recorded as its first
Quiroga, 1983; Valdivia et al., 2010; Oliva et al., 2018). intermediate host in Argentina (Ostrowski de Núñez,
Taking into account the uncertainty of the identification, 2007). Members of family Hydrobiidae are distributed
the information on life cycle and presence of P. lintoni in Chile (Valdovinos, 1999), therefore, we anticipate that

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 6 P. Oyarzún-Ruiz & D. González-Acuña

Fig. 4. Number of taxa per trematode family in Southern Chile (SC), regions XIV and X, and Chilean Patagonia (CP). Every color
in the pie chart represents a particular family. The highest number of taxa for trematode families in every region was stated
between parentheses. The name of every region represented as a roman number is detailed in Material and Methods.

future surveys may reveal the local transmission pathway do exist, there are no records of trematodes on these
of this trematode. vertebrates (see Rojas et al., 1971; Landaeta-Aqueveque
The insufficient coverage of host species diversity by et al., 2014, 2018; Seguel et al., 2017).
parasitological studies in Chile (see Garín & González- Only a small proportion of studies on trematodes in Chile
Acuña, 2008; Muñoz & Olmos, 2008; Oyarzún-Ruiz were performed using experimental infections (e.g. Tagle,
& González-Acuña, 2021) might underestimate the 1944; Fernández, 1987b; Rebolledo et al., 2014; Muñoz
complete richness of trematode species in the country. et al., 2015). Thus, authors want to emphasize the need
This echoes the situation of the coverage of South for performing this kind of studies, because these would
American fishes by parasitological studies with only help to a better understanding of the relationships between
5 % of their total diversity examined for parasites so far parasites and their hosts, mechanisms of transmission,
(Choudhury et al., 2016). pathological changes, behavioral manipulation, among
Among introduced animals, cattle, and lagomorphs have others (Fried, 2000; Ostrowski de Núñe et al., 2004;
been reported as hosts of F. hepatica (e.g. Alcaíno & Morley & Lewis, 2014; Blasco-Costa & Poulin, 2017;
Gorman, 1999; Courtin et al., 1975, 1979; Oyarzún-Ruiz Karvonen et al., 2017).
et al., 2019b), and some salmonid fishes were reported The present review highlights the clear need for the
as hosts of digeneans (Arata et al., 1977; Torres, 1995; broader use of molecular tools in the taxonomic studies of
Torres et al., 1992a). While publications on the helminth trematodes in Chile. Although the first study using DNA
fauna of other exotic species such synanthropic rodents sequencing was published in 2010 (Valdivia et al., 2010),
(Rattus rattus, Rattus norvegicus, and Mus musculus) the number of works applying molecular techniques is

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 Trematodes in Chile 7

still limited. The combined use of morphological and reviewers and subject editor for their useful suggestions.
molecular approaches (aka integrative taxonomy) is the This publication is dedicated to professor D. González-
most promising approach to advance our knowledge of Acuña, who passed away recently.
biodiversity, classification, diagnostics, and phylogenetic
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