ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2020, 14(1), ene-jun:9-17.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

THE HELMINTHIC PARASITE FAUNA OF THE WORLD-WIDE INVADER MICROPTERUS

SALMOIDES (LACEPÉDE, 1802) IN BRAZIL: A CASE OF CO-INTRODUCTION AND

SPILLBACK

HELMINTOS PARÁSITOS DE MICROPTERUS SALMOIDES (LACEPÉDE, 1802) UNA ESPECIE

INVASORA EN BRASIL: UN CASO DE CO-INTRODUCCIÓN Y SPILLBACK

1Laboratory of Ecology and Conservation, Federal University of Paraná, Curitiba, Paraná, Brazil.

Avenida São José, n 700, Ap 41 Bc E, Curitiba, Paraná, Brazil.

2 Laboratory of Ichthioparasitology, State University of Maringá, Maringá, Paraná, Brazil.

*Corresponding author: anapaulalula@gmail.com

1 2 1

Ana Paula Lula Costa ,*; Ricardo M. Takemoto & Jean Ricardo S. Vitule

ABSTRACT

Keywords: Biological invasion – Largemouthbass – Neotropical Ichytioparasitology –Nonnative parasites

The largemouth bass, Micropterus salmoides (Lacepéde, 1802), is a centrarchid fish from North America

that is now globally distributed because of wide-spread introductions for sport fishing. Its introduction in

Brazil dates from the 1920's, primarily in southern regions. Micropterus salmoides is already known to

have created a series of impacts in the ecosystems in which it is established. However, its parasite fauna in

Brazil is unknown. This opens the possibility of new interactions and potential impacts. Therefore, the

goal of the present study was to analyze the parasite fauna of M. salmoides in four reservoirs in southern

Brazil, measuring the prevalence and mean abundance in each reservoir. A total of 59 individuals of M.

salmoides were analyzed, 15 from each reservoir, except for the Capivari-Cachoeira Reservoir, with 14

individuals. Of the fish analyzed, 91.5% were parasitized by 1567 parasites belonging to four species,

three nematodes: larval Contracaecum sp. (86.4%), Procamallanus (Procamallanus) peraccuratus Pinto,

Fabio, Noronha & Rolas 1976 (6.7 %) and Hysterothylacium brachyurum Ward & Magath 1917 (6.7 %),

and one species of monogenean flatworm: Onchocleidus principalis (Mizelle, 1936) (57.6 %). From these

results we can conclude that the process of co-introduction and spillback is still in the early stages, mostly

by the low diversity of parasites. Therefore, monitoring and control actions are highly recommended in

order to both control the impacts of parasite infections as well as to promote mitigation of activities and

prevention campaigns.

Neotropical Helminthology

Volume14,Number1(jan-jun2020)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Auspiciado por:

doi:10.24039/rnh2020141610

INTRODUCTION

RESUMEN

Palabras clave: Parásitos no nativos – perca americana – ictioparasitología neotropical – Invasión biológica

La perca americana, Micropterus salmoides (Lacepéde, 1802), es un pez centrarchido de América del

Norte que ahora tiene una distribución global debido a introducciones extendidas por pesca deportiva. Su

introducción en Brasil data de 1920, principalmente en las regiones del sur. Sabemos que M. salmoides ha

generado una serie de impactos en los ecosistemas en que se ha establecido. Sin embargo, sus parásitos en

Brasil son desconocidos. Esto genera la posibilidad de nuevas interacciones y potenciales impactos. Por

tanto, el objetivo de este estudio fue analizar los parásitos de M. salmoides en cuatro reservorios de agua en

el sur de Brasil, midiendo la prevalencia y la abundancia media en cada reservorio. Analizamos un total de

59 individuos de M. salmoides, 15 en cada reserva, con excepción de la reserva Capivari-Cachoeira, con

14 individuos. De los peces analizados, 91,5% estaban parasitados por 1567 parásitos pertenecientes a

cuatro especies, tres nemátodos: Contracaecum sp. (86,4%) en larvas, Procamallanus (Procamallanus)

peraccuratus Pinto, Fábio, Noronha y Rolas 1976 (6,7%) y Hysterothylacium brachyurum Ward &

Magath 1917 (6,7%), y una especie de monogenoideo Onchocleidus principalis (Mizelle, 1936) (57,6 %).

De estos resultados podemos concluir que el proceso de co-introducción y “spillback” aún está en etapas

tempranas, en la mayoría de las veces por la baja diversidad de parásitos. Sin embargo, el monitoreo y las

acciones de control son altamente recomendadas para controlar los impactos de infecciones por parásitos

y promover actividades de mitigación y campañas de prevención.

Host-parasite interaction can influence community

structure in several ways (Price et al., 1986; Dunn

& Hatcher, 2015; Calhoun et al., 2018). A parasite

can interconnect a series of trophic levels through

its life cycle, modulating the population growth of

the host species and the apparent level of

competition in the ecosystem (Prenter et al., 2004).

When successfully co-introduced, a parasite

species can spillover to native hosts in the new

ecosystem, which may lead to a highly pathogenic

interaction due to the lack of co-evolutionary

history between the parasite and the new host.

Besides that, a nonnative host can also be infected

by native parasites, i.e. spillback, which can make

this new host a reservoir for the native parasite

species, increasing its prevalence in the ecosystem

(Kelly et al., 2009; Dunn, 2009; Dunn & Hatcher,

2015). These two possible impacts are influenced

by the encounter between susceptible and infected

hosts (Telfer & Brown, 2012).

The fish Micropterus salmoides (Lacépède 1802)

(Percifomes: Centrarchidae) is a species of great

importance in sport fishing because of its

characteristics as a top predator, including its large

size and voracity (Jackson, 2002; Brown et al.,

Biological invasions leads to novel interactions

and negative impacts in native ecosystems (Elton,

1958; Lockwood et al., 2007). Globalization and

its routes of transport and commerce plays a role as

vectors and pathways in introduction events and

large-scale dispersion of many invaders (Hulme,

2009). And this species never comes alone,

bringing with them new parasites and pathogens.

Which are responsible for changing the balance of

the community interactions in its new

environment. (Lockwood et al., 2007, 2009;

Cassey et al., 2018). The process of parasites co-

introduction is not yet contemplated in most of the

invasion frameworks, what is justified by the fact

that the forces which influence the invasion in free

living organisms is different than for parasites

(Taraschewski, 2006; Hulme, 2009; Carrete et al.,

2012; Blackburn & Ewen, 2017). For example, the

stages of introduction and establishment of

parasites depends on the prevalence rate in the

introduced host and the probability of finding

suitable hosts to complete its life cycle in the

environment (Hatcher et al., 2012).

Neotropical Helminthology, 2020, 14(1), ene-jun Lula-Costa et al.

Parasite fauna of Micropterus salmoides

Neotropical Helminthology, 2020, 14(1), ene-jun

2009; Estes et al., 2011). The species is native to

North America but is already established in more

than 50 countries, and is responsible for changes in

ecosystems around the world (Brown, 2009; Van

Der Walt et al., 2016; Froese & Pauly, 2016). The

impacts caused by M. salmoides have led its

inclusion in the list of the 100 worst invasive

species in the world, which makes its management

and control a priority (Lowe et al., 2000). In Brazil,

it was introduced in the 1920's and was originally

established in the southern region (Schulz & Leal,

2005; Ribeiro et al., 2015; Frehse et al., 2016).

The parasite fauna of M. salmoides is well known

in its native area, although there are few studies

where it has been introduced. Of those, none was

concerning the ecological impacts of co-

introduced parasites in the new environment

(Costa et al., 2018). Information concerning the

possible direct and indirect impacts of M.

salmoides in Brazil's native communities is

essential to ensure effective management and

control. The fact that M. salmoides is well

established and can be found in great abundance in

the south of Brazil increases the probability of co-

introduction and spillover of parasites, leading to

possible secondary impacts related to the invasion

by M. salmoides (Taraschewski, 2006). Therefore,

the present study aimed to provide an evaluation of

the helminth parasite fauna of M. salmoides in

Brazil and the possible impacts it may have on the

invaded ecosystems.

We sampled four reservoirs in South Brazil, on the

metropolitan region of Curitiba, Paraná, Brazil.

The reservoirs were chosen primarily by its abiotic

similarities, are in the same basin, and have a small

distance between each other. In the environmental

matter they are all categorized as moderately

degraded and are localized in the same basin with a

maximum distance of 78 km by each other

(Rodrigues et al., 2005; Brunkow et al., 2009;

Xavier et al., 2009; Seara, 2010; Da Conceição et

al., 2014).

The reservoirs sampled were: Piraquara I

(25°29'48.1"S 49°01'05.0"W), Passaúna

(25°27'41.2"S 49°22'58.4"W), Capivari-cachoeira

(25°11'39.1"S 48°52'35.2"W) and Vossoroca

(25°50'32.6"S 49°04'31.8"W).

The sampling effort was thought in a way that

maintained the same number of hosts (15 hosts by

reservoir) with similar average life stage, all adults.

Samples were all collected in the spring of 2015, to

decrease the influence of seasonality on the

parasite diversity between the reservoirs. All

individuals of M. salmoides were captured using

rod, hook, and artificial baits, in the period

necessary to reach the number of samples previous

stipulated (Parana, 2005). The fishes sampled were

anesthetized, killed by spinal section and taken to

the Zoology Laboratory of the Federal University

of Parana (Underwood et al., 2013). There, they

were numbered, measured (cm) (total and standard

length) and weighed (g). The gastrointestinal tract

and viscera were collect for endoparasite samples

and gills were separated for ectoparasite analyzes,

both were fixed in formol 5%. The parasites were

collected, quantified and preserved in ethyl alcohol

70% and prepared for identification following the

methods and protocols for which taxa described in

Eiras et al. (2006). The species of parasites were

identified using the classical studies of Margolis &

Kabata (1984), Moravec (1998) and Hoffman

(1999).

The parasite variables calculated were the parasite

richness of each reservoir class. Abundance,

prevalence and mean abundance of which parasite

species followed by Bush et al. (1997).

Ethic aspects: The authors point out that they

fulfilled all national and international ethical

aspects.

A total of 59 individuals of M. salmoides were

analyzed, 15 from each reservoir, except for

Capivari-Cachoeira Reservoir, with 14

individuals. The mean and SD of the hosts total

length analyzed was 31.41 ±3.50 cm in Passaúna

reservoir, 28.7 ±7.03 cm in Piraquara I reservoir,

31.75 ±2.58 cm in Vossoroca reservoir and 31.94

±7.19 cm in Capivari-cachoeira reservoir. All the

MATERIAL AND METHODS

RESULTS

The invasion of M. salmoides is responsible for

several disturbs in places where it was introduced,

although the impacts related to its parasite

community in Brazil were not known until the

present study (Ribeiro et al., 2015; Costa et al.,

2018). The native helminth fauna of the fish M.

salmoides is well studied, with more than 50

species of parasites recorded in its native region

(Hoffman, 1999; Costa et al., 2018). The

nematodes Contracaecum sp. and H. branchiurum

reservoirs sampled had 100% of the fishes

parasitized by some species of helminth, with

exception of Capivari-Cachoeira reservoir, that

had only 66.67 % of infected hosts. The parasites

sampled belong to four species, three nematodes:

Contracaecum sp. in their larval stage according to

Moravec, Kohn & Fernandes, 1993 found encysted

in the stomach external wall; Procamallanus

(Procamallanus) peraccuratus Pinto, Fabio,

Noronha and Rolas, 1976, and Hysterothylacium

brachyurum Ward & Magath, 1917, both found

inside the intestine of the hosts; and one species of

monogenean infecting the host's gills:

Onchocleidus principalis (Mizelle, 1936). Of

these, Contracaecum sp. and O. principalis were

recorded in all the reservoirs sampled, while P.

peraccuratus and H. branchiurum were found in

only one reservoir each. All the parasite variables

of prevalence, mean abundance, number of

parasite sampled by reservoir and number of

infected fish can be seen in Table 1.

Table 1. Helminth parasites of Micropterus salmoides by reservoir sampled, all located in the metropolitan region of

Curitiba, Paraná, Brazil. IF: Number of Infected Fish; NP: Number of Parasites; P%: Prevalence; MA±SD: Mean

Abundance ± Standard Deviation.

Reservoir Parasites IF

MA ±SD

Passaúna

(N=15)

P. peraccuratus

6.7

0.07 ±0.3

O. principalis

13.3

0.33 ±0.9

Contracaecum sp.

149

100

9.9 ±11.8

H. branchiurum

6.7

0.07 ±0.3

Piraquara (N=15)

O. principalis

237

100

15.8 ±15.3

Contracaecum sp.

394

100

26.7 ±15.2

Capivari-cachoeira

(N=14)

O. principalis

0.3 ±0.8

Contracaecum sp.

5 ±11.07

Vossoroca (=15)

Contracaecum sp.

387

21.7 ±19.7

O. principalis

319

100

25.8 ±14.2

Total

H. branchiurum

6.7

0.07 ±0.3

P. peraccuratus

6.7

0.07 ±0.3

O. principalis. 34 565 57.6 16.6 ±15.18

Contracaecum sp 51 1000 86.4 19.6 ±16.8

DISCUSSION observed during the present study have also been

noted parasitizing M. salmoides in its native

environment (Hoffman, 1999; Tavakol et al.,

2015). The same is true for the monogenean O.

principalis (Galaviz-Silva et al., 2016). However,

the nematode P. peraccuratus is a parasite native to

South America, which makes its infection in M.

salmoides a possible instance of parasite spillback

(Azevedo et al., 2006; Takemoto et al., 2009).

The helminth parasite fauna observed in the present

study showed low species diversity in comparison

with studies conducted in the native region (Costa

Neotropical Helminthology, 2020, 14(1), ene-jun Lula-Costa et al.

et al., 2018). It is known that most of the parasite

community are introduced with it host, although is

probably lost on the initial stages of introduction.

Mainly by its difficulty of adaptation in the

nonnative environment (MacLeod et al., 2010;

Carrete et al., 2012; Lymbery et al., 2014,

Blackburn & Ewen, 2017). Yet, highly stress

situation in the capture and transportation of

nonnative hosts can influence its immunologic

conditions, selecting more resistant propagules

(Carrete et al., 2012). The introduction of M.

salmoides in the reservoirs sampled during the

present investigation is still recent (the reservoirs

were constructed from the 1960's to the 1980's). So,

once M. salmoides are constantly introduced in

reservoir by multiple fonts (mostly fishermen) of

several distinguish life stage and local fonts, the

richness and prevalence of nonnative parasite may

increase with time, as its chances to establish in a

nonnative environment (e.g. Vitule et al., 2009;

Ribeiro et al., 2015).

In the present study only one specimen of both H.

brachyurum and P. peraccuratus was found. The

nematode H. brachyurum is commonly found

parasitizing the genus Micropterus. It has been

registered previously in the species M. dolomieu, in

Michigan, and in M. salmoides, also in the USA

(Amin & Minckley, 1996; Gopar-Merino et al.,

2005); this paper represents the first record of the

species in Brazil. As for P. peraccuratus, it has only

been recorded in Brazil, parasiting primarily

cichlids (Moravec et al., 1993; Azevedo et al.,

2006; Takemoto et al., 2009). According to

standard practice, a host-parasite relationship is

only considered to be effective if it results in at least

one other case of parasite infection, i.e. when the

rate of the parasite reproduction in the new host is

greater than one (Hatcher et al., 2012, Blackburn &

Ewen, 2017), or if the prevalence of infection is

greater than 10% (Bush et al., 1990). Although

more studies need to be done to confirm both

infections, we cannot discard the possibility of a

co- introduction event in the case of H. brachyurum

and a spillback event for P. peraccuratus (Kelly et

al., 2009). In relation to Contracaecum sp., its

larval stage is very generalist and are globally

distributed, once its final host are mainly

piscivorous birds (Madi & Silva, 2005; Takemoto

et al., 2009; Tavakol et al., 2015). This parasite has

a complex life cycle, and M. salmoides, among

other intermediary host, has its infection

influenced by its trophic level; i.e. top predators

typically have a higher probability of parasite

infection (Lafferty & Morris, 1996; Poulin &

Leung, 2011; Chen et al., 2008).

The species O. principalis has a high level of

specificity to the genus Micropterus, what makes it

presence an event of co-introduction (Maitland &

Price, 1969; Margolis & Kabata, 1984; Collins &

Janovy, 2003). Although, over the several

monogenean species that parasite M. salmoides

(Hoffman, 1999; Galaviz-Silva et al., 2016; Costa

et al., 2018), only one was found in this study. This

shows a clear example of enemy release, still the

high abundance of O. principalis in two of the

reservoirs sampled could be a compensation of the

poor parasite richness (Colautti et al., 2004; Roche

et al., 2010).

This study shows only a preliminary sample of the

parasite community of M. salmoides in Brazil,

what may increase in studies in other regions that

include seasonal samples. This allied to a constant

monitoring of the impacts made by these parasites

on the nonnative environments of M. salmoides.

However, we presented important information for

the introduction management and control for

nonnative hosts and its parasites. The parasite

fauna of M. salmoides can lead to multiple

scenarios of indirect impact. For example, the

increase in the prevalence of native parasites

caused by M. salmoides serving as a reservoir for

infection can facilitate the invasion success of the

host. The presence of M. salmoides can also lead to

a decrease in the prevalence and intensity of native

parasites in the cases where M. salmoides does not

serve as a proper host that can be included in the

parasite's life cycle. Furthermore, the co-

introduction of parasites may lead to emergent

diseases in the new environment because of the

lack of co-evolutionnary history in the host-

parasite relation, or because of the occurrence of

apparent competition, which may decrease the

population of native fishes in the ecosystem

(Strauss et al., 2012; Blackburn & Ewen, 2017;

Young et al., 2016). Finally, more than that, the

parasite community dynamics in a nonnative host

may suffer temporal variations (tend to increase its

richness over time), increasing the links of

connectance and nestedness in trophic networks, or

changing its patterns of predation and competition;

primordially in the early stages of the host

Parasite fauna of Micropterus salmoides

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Received November 2, 2019.

Accepted January 14, 2020.

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