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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica
Molluscicidal potential of Heterorhabditis baujardi (Rhabditida:
Heterorhabditidae), strain LPP7, on Lymnaea columella (Gastropoda:
Pulmonata): An alternative for biological control of fasciolosis
Victor Menezes Tunholi
a,
⁎
, P.O. Lorenzoni
a
, Ygor Henrique da Silva
a
,
Vinícius Menezes Tunholi-Alves
b,f
, Jankerle Neves Boeloni
a
, Maria Aparecida da Silva
c
,
Caio Oliveira Monteiro
d
, M.C.A. Prata
e
, J. Pinheiro
b,f
, Isabella Vilhena Freire Martins
a
a
Departamento de Medicina Veterinária, Centro de Ciências Agrárias e Engenharias, Universidade Federal do Espírito Santo—UFES, Alegre, ES, Brazil
b
Departamento de Ciências Fisiológicas, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
c
Departamento de Biologia, Centro de Ciências Exatas, Naturais e da Saúde, Universidade Federal do Espírito Santo—UFES, Alegre, ES, Brazil
d
Departamento de Microbiologia, Imunologia, Parasitologia e Patologia da Universidade Federal de Goiás, Rua 235, s/n, Setor Universitário, Goiânia, Goiás, CEP: 74605-
050, Brazil
e
Laboratório de Parasitologia da Unidade de Pesquisa da Embrapa Gado de Leite (Embrapa CNPGL), Juiz de Fora, MG, Brazil
f
Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
ARTICLE INFO
Keywords:
Reproductive biology
Parasitic castration
Snail-entomopathogenic nematode (EPN)
relationship
Microbial control
ABSTRACT
This study elucidated for the first time, under laboratory conditions, the susceptibility of Lymnaea columella to
infective juveniles of Heterorhabditis baujardi LPP7. Exposure to the nematodes induced an average mortality rate
of 66.66% in the population of L. columella, with the highest values attained from the second week after exposure
onward. In addition, all the reproductive parameters analyzed (total number of eggs, number of egg masses,
number of eggs laid/snail, embryo hatching rate and content of galactogen stored in the albumen gland) changed
as a result of the infection. The results indicate the occurrence of the phenomenon of parasitic castration in L.
columella infected by H. baujardi LPP7, probably through depletion of energy reserves such as galactogen,
necessary to meet the intense metabolic demands of the nematode’s larval stages. Finally, histopathological
analysis demonstrated an intense process of cell disorganization, characterized by the occurrence of
granulomatous inflammatory reactions in tissues of exposed snails, induced by the spoliative action of the
bacteria/nematode. The results suggest the use of H. baujardi LPP7 as an alternative for biological control of the
population of this intermediate host, and thus of the diseases in whose epidemiological chain it participates,
especially fasciolosis, in line with the recommendations of the World Health Organization (WHO).
1. Introduction
Lymnaea columella (Say, 1817) is an aquatic snail that is commonly
found in stagnant pools and slow-moving watercourses in Neotropical
regions. With both lungs and gills, adults and juveniles of Lymnaea have
amphibious behavior, with the ability to survive temporarily or even for
long periods out of their natural aquatic habitat (Jurberg et al., 1997).
These snails participate in the epidemiological chain of fasciolosis,
acting as the intermediate host in the life cycle of the etiological agent
of this parasitosis (Oakley et al., 1979). The disease is caused by two
trematode species: Fasciola hepatica (Linnaeus, 1758) and Fasciola
gigantica (Cobbold, 1855) (Mattos et al., 2009). Both are highly relevant
helminths in veterinary medicine and public health, by parasitizing the
biliary ducts and vessels of domestic ruminants, wild animals and
occasionally humans, so that the disease is classified as an important
anthropozoonosis (Oliveira and Spósito Filha, 2009; Mas-Coma, 2005).
The participation of snails of this genus as hosts in the cycle of
Fasciola sp. has been demonstrated by many researchers in studies
involving experimental infections, along with reports of the occurrence
of natural infection (Coelho et al., 2008, 2009; Pinheiro et al., 2009;
Farinazzo et al., 2001). The aim of these studies has been to clarify the
life cycle of Fasciola sp. and other trematodes, besides evaluating the
host’s behavior when infected, since modifications induced by the
parasite in the body of snails during infection cause a wide range of
responses, especially alterations in the reproductive pattern and growth
of the hosts (Tunholi et al., 2011; Dreyfuss et al., 1999; Jong-Brink,
http://dx.doi.org/10.1016/j.actatropica.2017.05.024
Received 5 March 2017; Received in revised form 15 May 2017; Accepted 20 May 2017
⁎
Corresponding author.
E-mail address: victortunholi@yahoo.com.br (V.M. Tunholi).
Acta Tropica 173 (2017) 23–29
Available online 22 May 2017
0001-706X/ © 2017 Elsevier B.V. All rights reserved.
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