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The development of Angiostrongylus vasorum (Baillet, 1866) in the freshwater snail Pomacea canaliculata (Lamarck, 1822)

Published online by Cambridge University Press:  29 December 2014

L.R. Mozzer ,
A.L. Coaglio ,
R.M. Dracz ,
V.M.A Ribeiro  and
W.S. Lima
L.R. Mozzer*
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
A.L. Coaglio
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
R.M. Dracz
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
V.M.A Ribeiro
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
W.S. Lima*
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
*
*Fax: +55 (31) 3499-2970 E-mails: wlima@icb.ufmg.br and lanuze@yahoo.com.br
*Fax: +55 (31) 3499-2970 E-mails: wlima@icb.ufmg.br and lanuze@yahoo.com.br
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Abstract

Angiostrongylus vasorum is a parasitic nematode that infects the heart and pulmonary artery and its branches of domestic and wild canids. The parasite can use several species of terrestrial and aquatic molluscs as intermediate hosts, although susceptibility varies. Pomacea canaliculata is a mollusc found in lakes, swamps and rivers in South America. In this study, we evaluated the susceptibility, parasite growth, oviposition and larval development of 282 P. canaliculata infected with 500 A. vasorum first-instar larvae (L1). From day 5 post-infection (pi) to day 30 pi, seven specimens per day were sacrificed to recover the larval instars. We compared 50 egg masses from infected and uninfected molluscs to determine the number of eggs per clutch, the hatching rate and the growth of the molluscs. The percentage of recovered larvae ranged from 39.17% to 67.5%. First-stage larvae (L1) were found until day 19 pi, second-stage larvae (L2) were found from days 11 to 25 pi, and third-stage larvae (L3) were recovered only after day 19 pi. Infected snails exhibited the most eggs during spawning, although the rate of hatching and shell size were lower in the infected snails compared with controls. This is the first report of an experimental infection of P. canaliculata with A. vasorum, and the results confirm the non-specificity of the nematode in relation to the intermediate host and indicate the importance of epidemiological surveys of this parasite and mollusc.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 6 , November 2015 , pp. 755 - 759
Copyright
Copyright © Cambridge University Press 2014 

Introduction

Angiostrongylus vasorum is a nematode that parasitizes the cardiorespiratory system of wild and domestic canids (Guilhon & Cens, Reference Barçante1969; Morgan et al., Reference Morgan, Shaw, Brennan, De Waal, Jones and Mulcahy2005; Helm et al., Reference Helm, Morgan, Jackson, Wotton and Bell2010). It has a worldwide distribution, having been reported in Europe, North America, South America and Africa, and can be found in tropical, subtropical and temperate regions (Lima et al., Reference Lima, Araujo Costa, Guimaraes and Leite1985.; Williams et al., Reference Williams, Lindemann, Padgett and Smith1985; Koch & Willesen, Reference Koch and Willesen2009).

The life cycle of A. vasorum includes both definitive and intermediate hosts, including terrestrial or aquatic gastropods that are infected through ingestion or by penetration by first-stage larvae (L1) from the faeces of canids. In the tissues of an infected invertebrate, first-stage larvae develop into second-stage (L2) larvae, and their development is complete when they reach the third stage (L3), which is infective for canids (Rosen et al., Reference Rosen, Ash and Wallace1970; Barçante et al., Reference Barçante, Barçante, Dias, Vieira, Lima and Negrão-Corrêa2003; Mozzer et al., Reference Mozzer, Montresor, Vidigal and Lima2011). Canids become infected after eating L3 larvae present in infected molluscs (Bessa et al., Reference Bessa, Lopes and Pinheiro1996; Morgan et al., Reference Morgan, Shaw, Brennan, De Waal, Jones and Mulcahy2005) or in a paratenic host, as demonstrated by Bolt et al. (Reference Bolt, Monrad, Koch and Jesen1993) who recovered adult A. vasorum from the canid Vulpes vulpes fed Rana temporaria that had been infected experimentally with A. vasorum. L3 larvae penetrate the wall of the digestive tract of a vertebrate host and migrate to the mesenteric lymph nodes, where they develop into fourth-stage larvae (L4) and then immature adults. Immature adults can reach the bloodstream and, after approximately 10 days, can be found in the right ventricle and pulmonary arteries (Guilhon & Cens, Reference Barçante1969; Helm et al., Reference Helm, Morgan, Jackson, Wotton and Bell2010).

The mollusc Pomacea canaliculata can be found in slow and stagnant water courses in the neotropical region and aestivates in the soil during dry periods (Lum-Kong & Kenny, Reference Lum-Kong and Kenny1989; França et al., Reference Koch and Willesen2007). It has been reported in Brazil, Argentina, Uruguay, Paraguay and Bolivia, and it is particularly abundant in the basins of the Plata, Uruguay and Paraguay Rivers (Thiengo, Reference Thiengo and Barbosa1995; Seuffert & Martin, Reference Seuffert and Martín2013). Pomacea canaliculata is naturally infected with A. cantonensis, the infectious agent of human eosinophilic meningitis in Asia and other parts of the world (Thiengo et al., Reference Thiengo, Fernandez, Boaventura and Stortti1998; Tsai et al., Reference Tsai, Liu, Kunin, Lee, Chen, Lin, Tsai, Lin, Huang, Yen and Yen2001; Lv et al., Reference Lv, Zhang, Liu, Hu, Yang, Steinmann, Chen, Wang, Utzinger and Zhou2009; Chen et al., Reference Chen, Tong, Zhang, Lou, Kong, Lv, Zhuo, Wen and Lu2011; Morrison & Hay, Reference Morrison and Hay2011; Qiu et al., Reference Qiu, Chan, Kwong and Sun2011).

The aim of this study was to evaluate the susceptibility of P. canaliculata to infection by A. vasorum and to analyse the biological changes resulting from this infection.

Materials and methods

Maintenance and experimental infection of molluscs

Specimes of Pomacea were collected from the edge of Pampulha Lagoon in the city of Belo Horizonte, Minas Gerais, Brazil (19°52′S, 43°58′W) and identified according to Rawlings et al. (Reference Rawlings, Hayes, Cowie and Collins2007). Eighty snails were maintained and reared in the laboratory, groups of eight specimens were placed in each of ten rectangular plastic containers (16 × 22 × 30 cm) with perforated lids (2-mm holes every 2 cm), containing chlorine-free water and bamboo culms. Each container was exposed to a photoperiod of 12 h light/12 h dark. Snails were fed lettuce and the water in the containers was changed every 7 days.

Each clutch was removed and transferred to a rearing container measuring 10 × 10 × 14 cm, and only molluscs that hatched from these clutches (designated first generation (F1), free from natural infection) were used during the experiment.

When these molluscs reached 30 mm (at approximately 60 days), 282 specimens were selected for further experiments. Of these specimens, 182 were placed in individual polypropylene vials (4 × 5 × 7 cm) containing 1 ml of water and 500 A. vasorum L1 larvae that had been recovered from the faeces of infected dogs. The molluscs were incubated in the vials at room temperature for 6 h and then transferred to a rearing container. The remaining contents of the infection vials were examined to quantify the larvae that had not penetrated the snails. From day 5 post-infection (pi) until day 30 pi, seven molluscs were randomly selected each day and sacrificed individually in Petri dishes, using a glass rod. The tissues and shells were macerated, wrapped in surgical gauze and filtered through a Baermann apparatus for 12 h to recover larvae. Larvae were then identified and counted according to Barçante et al. (Reference Barçante, Barçante, Dias, Vieira, Lima and Negrão-Corrêa2003).

To compare the biological characteristics, such as reproduction, growth and survival rate, of larvae from infected and uninfected snails, 100 specimens that were 30 mm in size were selected. Fifty snails were infected with 500 L1 larvae (as described above) and 50 snails were used as the uninfected control group. The molluscs were monitored for 120 days and the clutches from the infected and uninfected groups were separated and analysed to compare breeding throughout the experimental period. The number of eggs per spawning was quantified and the hatching rate was calculated based on the total number of eggs and the number of live molluscs that hatched. To compare growth, all molluscs from the infected and uninfected groups were measured with a pachymeter 120 days after hatching. The growth rate was calculated based on the initial and final sizes.

Data analysis

Pomacea canaliculata clutch size, hatching rate and growth were analysed with a one-way analysis of variance followed by a Tukey post-hoc text. Differences with P< 0.05 were considered statistically significant.

Results

Pomacea canaliculata molluscs were susceptible to infection with A. vasorum, as live larvae were recovered throughout the experimental period. Despite direct contact with A. vasorum larvae, the average rate of larval penetration per mollusc was 24% and ranged from 15.2 to 35% L1. The recovery of larvae from seven P. canaliculata specimens that were sacrificed each day ranged from 39.2 to 67.5%. Percentages were calculated assuming that the true rate of infection, i.e. the number of larvae that penetrated, averaged 120 L1 per mollusc.

The highest proportion of LI recovery was 50.31 ± 7.88% on days 5–10 pi, with no recovery after day 19. The peak of L2 recovery of 43.56 ± 7.95% occurred on days 11–19 pi and L3 peak of 60.86 ± 4.99% on days 26–30 pi. On day 19 pi all three developmental stages were recovered. Differences in the mean larval recovery of each of the larval stages were significant (P< 0.05), relative to days post-infection (table1).

Table 1

Mean recovery of Angiostrongylus vasorum larvae from seven specimens of Pomacea canaliculata each initially infected with 500 L1 of Angiostrongylus vasorum.

*Significant difference at P< 0.05.

Pomacea canaliculata clutches were collected from bamboo culms, and 50 clutches from the infected group and 50 clutches of the uninfected group were evaluated. The average number of eggs per clutch was significantly higher in the infected snails, 207 ± 18.12, than in the uninfected snails, 160 ± 12.14 (P< 0.0001). At an average environmental temperature of 27°C, the molluscs began hatching 12 days after the clutches were laid, and the hatching rate per clutch in uninfected molluscs, 68 ± 3.52%, was higher than that in infected molluscs, 55.8 ± 2.93%. The growth of the molluscs was affected by infection. Uninfected molluscs had significantly larger shells, measuring 56 ± 1.40 mm, than infected molluscs, 46 ± 1.77 mm (P< 0.0001), at 120 days after hatching. No significant difference in survival was observed between infected snails and uninfected snails (P= 0.74). At the end of the experiment, 41 of 50 specimens from the uninfected group survived, whereas 40 of 50 specimens from the infected group survived.

Discussion

The present study confirms that P. canaliculata is a valid intermediate host for A. vasorum. The rate of penetration by L1 larvae during infection ranged from 15.2 to 35% and was low compared with that found in other molluscs. This difference may be due to the presence of an operculum in P. canaliculata. This structure may act as a physical barrier to hinder the penetration of larvae, as molluscs that have no operculum show higher rates of larval penetration. For example, 95.2% of larvae have been shown to penetrate Omalonyx matheroni (Mozzer et al., Reference Mozzer, Montresor, Vidigal and Lima2011), and more than 80% of larvae have been shown to penetrate Biomphalaria tenagophila (Pereira et al., Reference Pereira, Martins-Souza, Coelho, Lima and Negrão-Corrêa2006). The results of this study also demonstrated the time required for P. canaliculata development. L1 larvae were observed until day 19 pi, L2 larvae were observed between days 11 and 25 pi, and L3 larvae were observed after day 19 pi. Based on our results, A. vasorum develops more slowly in P. canaliculata than in other mollusc species. Guilhon & Afghahi (Reference Guilhon and Afghahi1969) recovered L3 larvae starting on day 16 pi from several species of gastropods infected with A. vasorum. Sauerländer & Eckert (Reference Sauerländer and Eckert1974) recovered A. vasorum L3 larvae from Achatina fulica on day 17 pi. When Barçante (Reference Barçante2006) challenged Biomphalaria glabrata with A. vasorum, L2 larvae developed on day 5 pi, and L3 larvae developed on day 15 pi. Bessa et al. (Reference Bessa, Lima, Daemon, Cury and Araujo2000) infected Subulina octona with A. vasorum and observed L2 larvae on day 7 pi and L3 larvae on day 13 pi. Mozzer et al. (Reference Mozzer, Montresor, Vidigal and Lima2011) recovered A. vasorum L2 larvae from O. matheroni on day 5 pi and L3 larvae on day 10 pi. In the present study, the recovery rate of L3 larvae from P. canaliculata ranged from 39.17 to 67.5%. However, Barçante et al. (Reference Barçante, Barçante, Dias, Vieira, Lima and Negrão-Corrêa2003), also using the Baermann technique, recovered approximately 33% of L3 larvae from B. glabrata. In addition, Mozzer et al. (Reference Mozzer, Montresor, Vidigal and Lima2011) recovered between 78 and 95% of L3 larvae from infected O. matheroni. The development of the various larval stages of A. vasorum clearly requires more time in P. canaliculata than in other molluscs, but the mechanisms responsible for this delay are unknown. The progression between the different stages is delayed at lower temperatures (Gerichter, Reference Gerichter1948; Lv et al., Reference Lv, Zhou, Zhang, Liu, Zhu, Yin, Steinmann, Wang and Jia2006). However, in the present study, the average temperature was maintained at 27°C for the duration of the experimental period, which excluded any influence of temperature. A previous study reported that differences in the pattern of cellular responses and larval development in molluscs are dependent on the internal defence system of the molluscs (Iwanaga & Lee, Reference Iwanaga and Lee2005); however, further studies on the mollusc immune system are needed to elucidate the mechanism of this host–parasite interaction.

Regarding the biological aspects of the development of infected molluscs, we showed that the number of eggs per clutch was higher in the group infected with A. vasorum but that the hatching rate was lower. This result is consistent with trends known for other species of molluscs and trematodes, including B. glabrata infected with Echinostoma paraensei, Lymnaea stagnalis infected with Trichobilharzia ocellata and B. glabrata infected with Schistosoma mansoni (in which the number of clutches laid increased after cercariae were eliminated) (Brumpt, Reference Brumpt1941; Etges & Gresso, Reference Etges and Gresso1965; Schallig et al., Reference Schallig, Sassen and Jong-Brink1992; Tunholi et al., Reference Tunholi, Lustrino, Tunholi-Alves, de Mello-Silva, Maldonado, Rodrigues and Pinheiro2011). Most likely, infected molluscs spawn more often to compensate for losses caused by the stress of infection (Minchella, Reference Minchella1985). Tunholi et al. (Reference Tunholi, Lustrino, Tunholi-Alves, de Mello-Silva, Maldonado, Rodrigues and Pinheiro2011) have suggested that infected molluscs lay more clutches but that egg viability is lower due to reduced reproductive efficiency. This suggestion corresponds well with the results from our study, where a lower hatching rate was observed in the infected group. The results for the shell size of P. canaliculata infected with A. vasorum showed that the infected group developed smaller shells than the control group. This finding is similar to results obtained by Sauerländer & Eckert (Reference Sauerländer and Eckert1974), who infected A. fulica with 20,000 A. vasorum L1 larvae and observed growth retardation and shell deformation. In the present study, P. canaliculata exhibited low mortality rates over the course of the experiment. Nine of the 50 snails in the control group died, and ten of the 50 snails in the infected group died, indicating that this mollusc can survive while infected with A. vasorum. Sauerländer & Eckert (Reference Sauerländer and Eckert1974) reported a high rate of survival in A. fulica infected with A. vasorum, demonstrating that molluscs are resistant to this parasite; such resistance could promote the spread of the parasite.

The present study describes the first experimental infection of P. canaliculata with A. vasorum larvae and demonstrates that this mollusc can serve as an intermediate host for this parasite. Furthermore, our data underscore the non-specific nature of the A. vasorum parasite–intermediate host relationship.

Acknowledgements

The authors wish to thank Denis Aparecido Valério for his assistance with mollusc collection.

Financial support

This work was supported by CNPQ (Conselho Nacional de Desenvolvimento Científico e Tecnológico), grant number 2013-6.

Conflict of interest

None.

Ethical standards

This study was approved by the Research Ethics Committee of the Universidade Federal de Minas Gerais (CETEA/UFMG-147/2011).

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Figure 0

Table 1 Mean recovery of Angiostrongylus vasorum larvae from seven specimens of Pomacea canaliculata each initially infected with 500 L1 of Angiostrongylus vasorum.