Larval development of Aelurostrongylus abstrusus in experimentally infected Rumina decollata snails

Highlights

• Prospective role of R. decollata as A. abstrusus intermediate host was studied.

• Experimental infection was performed to study the larval development.

• High levels of infection in snails and fully development could be demonstrated.

Abstract

Aelurostrongylus abstrusus is a lungworm distributed worldwide that affects wild and domestic cats, causing bronchopneumonia of varying intensity. Snails serve as intermediate hosts. The aim of the present study was to assess the larval development of A. abstrusus in R. decollata snails and to investigate its potential as an intermediate host. For this purpose, first-stage larvae (L1) of A. abstrusus were obtained from the faeces of naturally infected cats. Doses of 500 L1/snail were given to 24 R. decollata snails, placed on the soil of the breeder chamber, and maintained under laboratory conditions. Three snails were killed at 8, 10, 12, 16, 22, 26, 45 and 55 days post-infection (dpi), and the muscular foot and visceral body were separately digested by an artificial digestion technique. The morphometric parameters of different larval stages were recorded. The mean number of larvae reaching the infective stage at the end of the study (L3) was 262 larvae/snail. The greatest development to L3 was recorded from days16 to 55 pi, during which the isolation was maximum. A. Abstrusus L3 were isolated from the viscera, but isolation from the snail foot was significantly higher. Our results showed for the first time the ability of A. Abstrusus larvae to develop in R. decollata, thus serving as a potential intermediate host.

Introduction

Aelurostrongylus abstrusus is a lungworm of cats distributed worldwide that causes bronchiolitis and interstitial pneumonia (Traversa et al., 2008). Cats can acquire the parasite by eating slugs and snails with infective third-stage larvae (L3) of A. abstrusus. Mice, birds and reptiles can act as paratenic hosts by the ingestion of infected snails (Giannelli et al., 2017; Hamilton, 1969; Hansen et al., 2017; Hobmaier and Hobmaier, 1935; Traversa and Di Cesare, 2016). In cats, L3 migrate to the lungs where they reach the adult stage and reproduce. The first-stage larvae (L1) are coughed up, swallowed and eliminated into host faeces where they can survive between 45 and 60 days (Dernegi and Turkish, 2010). When larvae reach the molluscs, they actively penetrate the foot integument and moult twice to L3 (Hobmaier and Hobmaier, 1935). Different species of gastropods have been reported as intermediate hosts for this nematode, including Agriolimax agrestis and A. columbianus, Helminthoglypta californiensis and H. nickliniana, Helicella spp. (Hobmaier and Hobmaier, 1935), H. aspersa (Di Cesare et al., 2013; Giannelli et al., 2013), Mesodonthyroidus, Triodopsis albolabris, Biomphalaria glabrata (Zottler and Schnyder, 2016), Cernuella virgata (López et al., 2005), Achatina fulica (Ohlweiler et al., 2010; Thiengo et al., 2008; Valente et al., 2017), and recently, R. decollata (Cardillo et al., 2014). L3have been demonstrated to survive for up to 2 years in H. aspersa snails (Hamilton, 1969), and transmission between two intermediate hosts (intermediesis) may occur (Colella et al., 2015) by shedding lungworm larvae within gastropod mucus in the environment (Giannelli et al., 2015).

R. decollata is a pulmonata land snail that belongs to the Subulinidae family (Rascop, 1960). This snail is native to and widely distributed in the countries around the Mediterranean Sea, southern Europe, northern Africa and western Asia (Batts, 1957; Neck, 1986), and it has been spread to other parts of the world (Matsukuma and Takeda, 2009; Prévot et al., 2015). In the 1970s, it was intentionally introduced into North America as a biological control agent of the garden snail H. aspersa, and then it was accidentally spread into the United States, Mexico, Bermuda, Cuba and Uruguay (Cowie, 2001; Selander and Kaufman, 1973). In Argentina, it has only been recorded in urban areas; it was first reported in 1988 in Buenos Aires province (Miquel, 1988) and then in La Pampa and Mendoza provinces (Francesco and Lagiglia, 2006). R. decollata is an omnivore and a detritivore, feeding on organic matter such as animal faeces (Batts, 1957, and cited by Tupen and Roth, (2001). It also preys upon other land snails, worms and insects (Batts, 1957, and cited by Mc Donnell et al. (2016)). R. decollata is a highly invasive snail adapted to arid conditions, extreme temperatures and low relative humidity (Rascop, 1960; Batts, 1957). Despite this, it does not reach long distances. However, human activities and the lack of natural predators could lead to their rapid dispersal (Francesco and Lagiglia, 2006). The increase in the stray cat population in public places of the Autonomous City of Buenos Aires (Sommerfelt et al., 2006) may contribute epidemiologically to the spread of A. abstrusus. Together with the increase in the population of R. decollata snail (Cardillo et al., 2014; Miquel, 1988), this raises the question about the snail as a possible transmitter of A. abstrusus for cats. Cardillo et al. (2014) previously reported a high infection rate of A. abstrusus (average of 93.89 L3/pool) in 80% (20/25) of the pools of three R. decollata snails collected from the environment of a place in Buenos Aires city inhabited by a stray cat population. The study of this gastropod species’ susceptibility as an intermediate host of metastrongyloids highlights its possible implication in the transmission and dispersion of parasites of medical and veterinary importance (Colella et al., 2015).

For this purpose, experimental infection of A. abstrusus in R. decollata was performed to study the infection rate and larval development, and therefore, elucidate the snaiĺs capability as an intermediate host in the parasités life cycle.