Distribution , feeding behavior and control strategies of the exotic land snail Achatina fulica ( Gastropoda : Pulmonata ) in the northeast of Brazil

The goal of this study was to document the distribution and establishment A. fulica such as their feeding preference and behavior in situ. The study was carried out at the city of Lauro de Freitas, Bahia state, Brazil, between November 2001 and November 2002. We used catch per unit effort methods to determine abundance, distribution, habitat choice and food preferences. The abundance and distribution of A. fulica was most representative in urban area, mainly near to the coastline. Lots and house gardens were the most preferred sites during active hours. The results indicated that A. fulica started their activity at the end of the evening and stopped in mid-morning. Their preferred food were vascular plants such as Hibiscus syriacus, Ricinus communis, Carica papaya, Galinsonga coccinea, Lippia alba, Ixora coccinea, Musa parasidisiaca, Mentha spicata and Cymbopogon citrates. Our results indicate that A. fulica are well adapted and established in this city and modified environments facilitate their establishment and dispersion. However, human perturbation, such as clearance of lots could be limiting for the persistence of A. fulica populations.


Introduction
The Giant African Snail (Achatina fulica Bowdich, 1822) promotes substantial ecological and economic impacts in areas where it has been introduced (Rauth and Barker, 2002).This snail is one of the most destructive pests affecting subtropical and tropical areas, causing large damages to farms, commercial plantations and domestic gardens.It can also be found on trees, de-caying material in decomposition and next to garbage deposits (Mead, 1995;Vansconcelos and Pile, 1999).Furthermore, A. fulica could be an intermediate host of Angiostrongylus costaricencis (Morera and Céspedes, 1971), the etiological agent of abdominal angiostrongylosis, and its dispersion could imply a possible risk of transmission of this disease (Teles et al., 1997).
One of the most important factors for the establishment and dispersion of A. fulica is human presence (De-Winter, 1989).In general, this snail is most abundant in sites with high human density (Takeda, 1988).Another important factor that may condition A. fulica population dynamics, growth rate, survival and fecundity is food preference (Ahmed and Rauth, 1991).Achatinidae species are generally regarded as herbivorous, feeding primarily on vascular plants (Rauth and Barker, 2002).Previous studies support that A. fulica is an important agricultural plague and causes substantial environmental loss (Hodashi, 1979;Egonmwan, 1991;Otchoumou et al., 1990).However, most of these studies deal with agricultural plant species.
Physical, biological and chemical strategies have been used to eradicate and manage A. fulica populations (Raut and Baker, 2002).Physical control strategies were used to collect and destruct snails and their eggs (Peterson 1957, Olson 1973).Invertebrate predators of terrestrial gastropods have also been used for biological control of A. fulica (Griffihs et al., 1993;Simberloff and Stiling, 1996;Takeuchi, 1997).Finally, a large number of toxicants have been used against A. fulica (Nair et al., 1968, Raut andGhose, 1984;Panigrahi and Raut, 1994).
It has been widely documented that A. fulica is welladapted and distributed around the world.However, information about A. fulica feeding preferences and behavior is still scarce in Brazil.Our main purpose was to describe A. fulica distribution in an area where it has been recently introduced, and identify its habitat and food preferences.We also examined the effects of scrub clearance on A. fulica abundance.To fulfill these goals, we addressed three basic questions: 1) what is the A. fulica distribution in areas where they have been recently introduced? 2) what are the main aspects of their behavior and feeding?and 3) what is the effect of lot clearance on their abundance?

Material and Methods
Distribution and abundance of Achatina fulica were recorded in a tropical area, Lauro de Freitas City (12° 54' S and 38° 19' W), Brazil.The study area covers of 60 Km 2 and was divided into urban area (residential and industrial areas) and forested area.The ur-ban area presented a population of 113,543 inhabitants (1,892.4hab/km 2 ) (IBGE, 2000).During the study, the annual average temperature was 25.7 °C, annual mean humidity was 78.6 and the annual precipitation was 2,000 mm (SEI, 2002).The map of Lauro de Freitas was digitalized and processed using ArcGIS 9.2 in a grid and comprised 60 quadrates of 1,000 x 1,000 m (Figure 1).
We carefully searched for A. fulica from November 2001 until November 2002 during different periods, including rainy days, to identify and quantify the occurrence of this snail in the city.Samples were taken monthly from forest and urban areas using catch per unit effort method (CPUE/hour) to collect the snails.The mean monthly abundance was then calculated.To identify the preferred sites into the urban areas, five 1.0 x 1.0 m quadrates were randomly thrown and the density of this snail was calculated.
Territorial and feeding behavior were monitored during December 2001 and November 2002.Observations were carried out during day and night times, recording location and behavior (Iglesias and Castillejo, 1998;Hatziioannou, et al., 1994;Lorenzi and Souza, 2001).For food plant preferences, 50 snails were placed in plastic jars (50 x 25 x 15 cm), with a screw cap and a small hole to allow respiration.Detached leaves of plant species presented in the study area (Hibiscus syriacus L., Ricinus communis L., Carica papaya L., Galinsonga coccinea, Lippia alba (P.Mill.), Ixora coccinea L., Musa parasidisiaca L., Mentha spicata L. and Cymbopogon citrates (DC.ex Nees)) were placed into these jars and observations of feeding behavior were performed at irregular intervals (Molgaard, 1986).
To identify possible control strategies, we monitored A. fulica abundance during August 2002 in 20 lots (10 cleared and 10 non-cleared) of approximately 500 m 2 , when Lauro de Freitas City Hall promoted the clearance of lots in the urban area.For this, we calculated the mean abundance before and after the clearance, using the catch per unit effort method.We also calculated the difference between these means, using the Student's t-test with a 95% confidence interval.

Results
Achatina fulica was mainly found in the urban area.The results show a different abundance pattern with distance from the coast line (see Figure 2).Mean monthly mean abundance value for forest and urban area is shown in Table 1.The distribution of A. fulica in the city showed different preferences among urban areas.High snail abundances were found outside houses.A. fulica was most abundant in lots.Also, 31.5% of the snails were also found inside stone walls, linear boundaries of houses and lots.As expected, only a low proportion (7.86%) was present on garden furniture and crawling on external house walls.No snails were found inside houses, although many specimens were found creeping onto windows (as shown in Table 2).
Achatina fulica is most active at dusk and dawn (Table 3), but on some cloudy and rainy days it was possible to observe them all day long.In general, A. fulica activity in Lauro de Freitas starts around 06:00 PM and the mean time for ceasing activities is 08:00 AM.
We found differences in food preferences.The preferred food were vascular plants such as Hibiscus syriacus, Ricinus communis, Carica papaya, Galinsonga coccinea, Lippia alba, Ixora coccinea, Musa parasidisiaca, Mentha spicata L and Cymbopogon citrates.Despite preferring herbaceous vegetation, we found saprophytic habits.A. fulica was found feeding on horse and bull feces.
We calculated the mean August abundance of A. fulica after and before the lot clearances.We noted that before clearance, abundance was 1,274 and at the end of the month, it was 378 snails.The mean snail abundance in non-cleared (3.2) and cleared lots (34.6) were significantly different with P < 0.001 (Figure 3).

Discussion
The data suggest that Achatina fulica is well-adapted and widely distributed in Lauro de Freitas City, and its population density was highest in the urban areas.Because of its low potential for active dispersal, Giant African Snail occupation is restricted to a few areas, but they can reach high densities (Aoki, 1978;De Winter, 1989;Takeuchi et al., 1991;Tomiyama, 1992).However, locally, this snail has a great potential to extend its distribution beyond the colonized area (Frankiel, 1989;Schotmamm, 1990).This pattern has also been observed in Rio de Janeiro (Brazil), around residential houses (Vasconcelos and Pile, 2001).In general, there is a tendency for this species to thrive in the presence of man, especially in urban sites (Barquet, 1950;Wolfenbarger, 1971;Takeuchi et al., 1991) and farms (Ahmed and Raut, 1991).Results show large fluctuations in snail population during September and November 2002.During August 2002 a notable decrease of this snail abundance was found.Also, there was a significant difference between cleared and uncleared lots.This may be a response to scrub clearance in lots.Such human perturbation can be a limiting factor for snail population growth.Similar oscillations in density due to human perturbation were found in Africa (Duah and Monney, 1999).
Another important aspect of the management of A. fulica pests is its cost.The cost of the eradication of A. fulica can be very expensive.In the USA, the elimination of this pest represented a very expensive process, varying from US$ 60,000 to US$ 700,000 (Muniappan 1987, Smith andFowler 2003).According to Lauro de Freitas City Hall, lot clearance cost is around US$ 3,300 per month.Consequently, we believe that lot clearance could be a good solution to eradicate A. fulica invasion in areas where its relative abundance was greater in lots, squares and streets.
Our results showed that A. fulica was most active from the beginning of the evening until the mid-morning.This result is similar to those obtained by Raut (1984) and Raut and Baker (2002).They found that A. fulica is a nocturnal snail and during the daytime it is quiescent and its activity begins at the end of the evening.Other important factors that affect the circadian cycle of these snails are sunlight and their physiological conditions (Takeda, 1986).
The feeding of A. fulica is dependent on plant community composition (Waterhouse and Noris, 1987), and varies according to quality and quantity (Rauth and Barker, 2002).Some studies suggest that this snail may be a generalist (Vinci et al., 1988).Similar feeding behavior was found in Lauro de Freitas, in that A. fulica fed on species such as Hibiscus spp., Hemigraphis colorata (Blume), Cymbopogon citratus, Carica papaya, Mentha spp.The location of food by A. fulica is powered by its sense of smell, being mainly attracted to garden crops (Farkas and Shorey, 1976;Gallois and Daguzan, 1989) and Urtica dióica L., a species typically used as refuge needs (Grimes and Blyte, 1969).We also found A. fulica feeding on bull feces.Many infections are spread by fresh water and terrestrial snails (Teles et al., 1997;Carvalho et al., 2003).Bearing in mind that this snail presents a possible public health risk regarding the spread of diseases, and even though we quantify the risk represented by its saprophytic habit, we believe that A. fulica could represent a threat to human health and its population must be controlled or eradicated.We also believe that further studies are still necessary to measure the degree of risk posed by A. fulica.
To conclude, although this species is a recent introduction to Brazil, and particularly in Lauro de Freitas City, A. fulica has become established successfully in this area because it presents favorable conditions.Our results suggest that human action could be an important population regulator, by influencing local distribution, or by increasing or decreasing its abundance.We believe that scrub clearance may represent a good and inexpensive solution to eradicate this pest on a small scale.

Figure 1 .
Figure 1.The 1,000 x 1,000 m grid covering the surface of Lauro de Freitas.Every Grid pixel is identified according to its use as urban area (dark gray) or forest area (light gray).

Figure 2 .
Figure 2. A map of mean abundance of Achatina fulica per 1,000 x 1,000 m in Lauro de Freitas during the sampling.

Figure 3 .
Figure 3. Abundance of Achatina fulica during August 2002.Data is represented by the abundance in cleared (dark gray) and uncleared (light gray) lots in the urban areas.

Table 1 .
Abundance of Achatina fulica in Forest and Urban areas of Lauro de Freitas from November (2001) until November (2002).

Table 2 .
Distribution, density and relative frequencies of Achatina fulica in urban sites in Lauro de Freitas city.

Table 3 .
Activity of Achatina fulica in Lauro de Freitas City.Data is represented by the start time of the activity of A. fulica such the last hour that this snail was found crawling elsewhere.During February and October, no snails were found in the field.