Variation in the population density of the Giant African Snail ( Lissachatina fulica ) in the Neotropical region Variación

The Giant African Snail ( Lissachatina fulica ) is one of the 100 world’s worst invasive species and has been recorded in the Neotropical region since the 1980s. Temperature and precipitation variables affect snail population density; however, these relationships have not been investigated for L. fulica on a regional scale. Here, we made the first description of variation in population density of L. fulica in the Neotropical region using a literature search, descriptive statistics, and a Principal Component Analysis (PCA). We found 22 studies covering 36 localities in six countries. The mean snail density was 11.55 ± 28.32 ind/m 2 , with the lowest value recorded in Cuba (0.0002 ind/m 2 ) and the highest value recorded in Venezuela (150 ind/m 2 ). These values were recorded between 21 % to 93 % of Human Footprint, 710 mm to 4438 mm of Annual Precipitation, 13 ºC to 27 ºC, Mean Temperature of the Coldest Quarter, and 3 ºC to 40 ºC of Temperature Seasonality. The PCA suggested that low densities can occur in various environmental conditions, whereas medium and high densities seem to appear in more specific climatic combinations. In conclusion, increased densities of Lissachatina fulica in the Neotropics seem to be influenced by climatic variations, especially the Mean Temperature of the Coldest Quarter and Annual Precipitation, supporting previous findings in the literature regarding the snail establishment. Future monitoring of this invasive species, performed at expanded spatial and temporal scales, may provide tools to establish a relationship between snail density values and impact.


INTRODUCTION
The Giant African Snail, Lissachatina fulica (Bowdich, 1822), is one of the 100 world's worst invasive species (Lowe et al. 2004, Thiengo et al. 2007). In the invaded areas, L. fulica can cause impacts on health, agriculture, and the economy. In health, the snail can act as an intermediate host for nematode species of the genera Angiostrongylus and Aelurostrongylus, which cause eosinophilic meningitis and abdominal angiostrongyliasis in humans, besides other diseases in domestic animals (Fischer et al. 2010).
L. fulica is recognized as a generalist herbivore that feeds on various cultivated plant species (Thiengo et al. 2007).
Finally, the presence of L. fulica entails an expense of the public herald for the potential consequences and control that must be carried out (Roda et al. 2018). Therefore, ecological research on L. fulica is necessary to mitigate the negative impacts of its presence through the construction of comprehensive management plans.
In the Neotropics, L. fulica was first recorded in the 1980s in Martinique and Brazil (Mead andPalaci 1992, Santana-Teles et al. 1997). By the beginning of the 21st century, it has already been recorded in Cuba (Vázquez and (Goldyn et al. 2017) and Argentina (Gutierrez-Gregoric et al. 2011). After recording L. fulica, some countries have established regulations to control and manage the snail, besides inciting research to provide baseline knowledge (MAVDT 2011). However, this control has been based on the manual collection and subsequent culling with chemical or physical means (Thiengo et al. 2007), which requires ecological knowledge of local populations. As the species is widely distributed in the Neotropics (Darrigran et al. 2020), a better understanding of the mollusk population dynamics in this region could help for enhancing control and management plans.
Density is one of the population parameters considered to assess whether an exotic population is established and the possible impact it produces. In L. fulica, it is postulated that a population density higher than 10 ind/m 2 is already a cause for concern as an established population ). This argument is because population density influences parameters related to fitness such as growth, fecundity, egg viability, and dispersal . Nevertheless, the relationship between population density and the impact of an invasive population is not linear (Jackson et al. 2015) and can be affected by other ecological factors such as the trophic level (Bradley et al. 2019). We would also expect that density is also affect-
Palabras clave: Achatina fulica, Caracol invasor, Ecología de poblaciones, Invasión biológica. ed by temperature and precipitation; however, as far as we know, these relationships have not been investigated for L. fulica on a regional scale. In heterogeneous environments, such as those found in the Neotropics, understanding the relationships between density and climate should contribute to modeling the link between density and impact.
Here and anthropic intervention where the species was recorded. We expect that this work will provide subsidies for decision-making for managing the giant African snail in the countries of the region.

RESULTS
In total, we found 22 papers estimating the population density of L. fulica in the Neotropics. These papers record snail density in 36 localities covering six countries: Argentina, Brazil, Colombia, Ecuador, Venezuela, and Cuba, from 2004 to 2020 (Fig. 1a). For these records, the mean density was 11.55 ± 28.32 ind/m 2 and the median was 4.03 ind/m 2 . The lowest and highest densities were reported in Cuba (Havana, 0.0002 ind/m 2 ) and Venezuela (Andres Bello, 150 ind/m 2 ). In most sites (80%) density values scored below 10 ind/m 2 (Table 1).
Regarding the relevant predictors for L. fulica establishment suggested by the literature, we found density records in the following ranges: Human Footprint from 21% to 93%, Annual Precipitation between 710 mm to 4438 mm, Mean Temperature of the Coldest Quarter between 13 ºC to 27 ºC, and Seasonality of Temperature between 3 ºC to 40 ºC. In general, we found no density pattern between low or high values of these variables (Fig. 1b).
The first two components of the PCA explained 63.5% of the variance of the environmental data (Supplementary material 2, Table S2). Mean Temperature of the Coldest Quarter (bio11) and Mean Temperature of the Driest Quarter (bio9) had the largest contributions to the first component. In contrast, Annual Precipitation (bio12) and Precipitation of the Wettest Month (bio13) had the largest contributions to the second component. Human Footprint was the least contributing variable for both components (Supplementary material 2, Table S3). The Cartesian space defined by PC1 and PC2 shows that sites presenting low snail densities are distributed across the two components, indicating that different climatic combinations can maintain L. fulica populations. On the other hand, most sites presenting medium snail densities show positive values of the first component, whereas most sites presenting high densities show negative values of the second component. This pattern suggests that density increase can be influenced by specific temperature and precipitation ranges (Fig. 2).

DISCUSSION
In this study, we found a high variation in the population density of L. fulica in six Neotropical countries. Low   densities of the species can be maintained in an array of environmental conditions, but density increase seems to be influenced by the Mean Temperature of the Coldest Quarter (bio11) and Annual Precipitation (bio12). The possible influence of bio11 on L. fulica density seems to be associated with establishment ) and survival . Annual Precipitation, in turn, may be related to physiological processes, like estivation (Rahman and Raut 2010), that influence population dynamics. However, the low number of localities with density records does not capture all the environmental conditions that could explain the variation in density of the invasive mollusk.
Our data did not show the clear effects of human intervention on snail population density. The human footprint did not contribute significantly to the principal components, and the highest population density (150 ind/m 2 ) was recorded in a site presenting the lowest value of human footprint (21%) (Supplementary material 1). In general, disturbed areas provide unique habitat opportunities and potential refugia for invasive alien species (Cadotte et al. 2017) and may even promote adaptation (Borden and Flory 2021). What is interesting in the case of L. fulica is its ability to maintain populations in low percentages of the human footprint, which would turn conservation units and rural areas of countries into refuges for the species (Fischer et al. 2010). Since L. fulica can occur from low to high human intervention, we call attention to direct management strategies in rural human populations.
According to the latest distribution model of the species in South America  In conclusion, the population density of Lissachatina fulica in the Neotropical region would be more influenced by climatic variables than by the degree of anthropogenic intervention. In this study, we postulate the Mean Temperature of the Coldest Quarter (bio11) and Annual Precipitation (bio12) as key climate variables influencing snail density, supporting the results found by Albuquerque et al. (2009) and Vogler et al. (2013) regarding L. fulica establishment. We call attention to the ability of the species to maintain low population densities over wide ranges of environmental variables. Since at high population densities, there is a greater perception of damage (Jackson et al. 2015), low-density localities are ignored when establishing control actions. In the future, a spatial and temporal expansion of local monitoring of this invasive species may provide sufficient tools to develop a relationship between density values and the impact produced by the species in the region.

PARTICIPATION OF AUTHORS
APM Conceived ideas, data analysis and writing; AG data analysis and writing; RT data analysis and writing.