Next Article in Journal
Invasive Aquatic Weeds Suppress Predator–Prey Cascades: Evidence from a Mesocosm Study
Previous Article in Journal
How Do Waterbird Communities Respond to Multi-Scale Environmental Variables in the Satellite Wetlands Surrounding a Ramsar Site, Shengjin Lake in China?
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 17
Issue 3
10.3390/d17030177
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Genetic Diversity of the Invasive Species Lissachatina fulica in the Urban Area of Cali, Colombia

by
Andres Castillo
1,2,*,
María C. Rodríguez
2,
Claudia M. Franco
2 and
Alan Giraldo
1
1
Grupo de Investigación en Ecología Animal, Departamento de Biología, Facultad de Ciencias Naturales y Exactas, Universidad del Valle, Cali 760032, Colombia
2
CiBioFi, Laboratorio de Técnicas y Análisis Ómicos TAO-Lab, Facultad de Ciencias Natrales y Exactas, Universidad del Valle, Cali 760032, Colombia
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(3), 177; https://doi.org/10.3390/d17030177
Submission received: 21 November 2024 / Revised: 18 December 2024 / Accepted: 20 December 2024 / Published: 28 February 2025
Browse Figures
Versions Notes

Abstract

:
The African giant snail, Lissachatina fulica (the Achatinidae family), is an invasive mollusk found in many countries across the Pacific, the Caribbean, Asia, and Latin America. Lissachatica fulica is known for its rapid dispersal and poses several ecosystem problems. It displaces native mollusk species and causes economic losses by damaging cultivated plants. This snail is also a public health concern as it can transmit the nematode Angiostrongylus cantonensis, leading to meningoencephalitis in humans. This study utilizes the 16S rRNA gene to examine the genetic variation in L. fulica in the city of Cali, located in southwestern Colombia. We identified two haplotypes, designated as C and D. Among the 578 samples analyzed, haplotype C was found in 11% of the samples, while haplotype D was present in 89%. Concerning demographic events in L. fulica, such as population expansions, contractions, and bottlenecks, the negative value of Tajima’s D index suggests that positive selection has favored certain alleles or haplotypes, reducing genetic variation. In conclusion, the clear dominance of haplotype D in most areas might indicate that haplotype D is either more prevalent or advantageous in these environments. However, further analysis would be needed to understand the reasons for this pattern (e.g., environmental, genetic, or social factors).

1. Introduction

The giant African land snail (Lissachatina fulica, Bowdich 1822) is a species native to West and Central Africa and is known for its large size and ecological adaptability [1]. However, it is recognized as an invasive species in many tropical and subtropical regions worldwide [2]. Its high fertility rate, ability to thrive in various environments, and economic appeal contribute to the giant African snail’s recognition as one of the 100 most dangerous invasive species in the world [3]. The primary means of its spread is through human activities, such as air and sea cargo transport and the trade of plant materials, pets, and food [4]. In addition to being a significant pest for tropical crops, L. fulica serves as an intermediate host for the rat lungworm, Angiostrongylus cantonensis, which can cause eosinophilic meningitis in humans [5].
The first recorded appearance of L. fulica outside its native range was in Madagascar in the 1760s [6]. From Madagascar, these snails were deliberately introduced to Mauritius in 1803, where they quickly became a widespread pest within twenty years. It is now distributed across Africa, the Indian subcontinent, Southeast Asia, the Pacific, the Caribbean, and North and South America. As of now, the total number of 16S haplotypes identified for L. fulica is 23. Among these, two have emerged from the Indian Ocean islands: haplotype C, which is predominant globally, and haplotype D, found in South America. Additionally, there are four non-African/Indian Ocean haplotypes derived from haplotype C: haplotype E from the Philippines, haplotype F from New Caledonia and Barbados, haplotype P from India, and haplotype Q from Ecuador. Haplotype H, which was previously exclusive to the Indian Ocean Islands, along with haplotypes S and W, found in India, are derived from haplotype H. All four other haplotypes in India also trace their origins back to the most common haplotype C [2,7,8]. Given the scale of global trade and the various haplotypes of L. fulica, it is crucial to investigate the presence and potential spread of these haplotypes outside Africa, particularly within the islands of the Indian Ocean, as well as to identify the source populations of newly emerging haplotypes.
The arrival of L. fulica in South America was first recorded in 1989 [9]. This species was imported from Indonesia to Brazil to evaluate its potential as an alternative source of meat for local consumption and international trade. From Brazil, its range expanded throughout the Neotropical region, with reports of its presence in Argentina, Paraguay, Peru, Ecuador, Colombia, and Venezuela [10,11]. In contrast, its introduction in Colombia was driven by a growing national demand for a cosmetic product known as “snail slime” [12].
The first recorded occurrence of the species in southern Colombia was between 2009 and 2010, and it reached the Caribbean region of Colombia by 2012 [13]. However, the demographic history of the giant African snail in southwest Colombia is not yet fully understood. It is believed that this species was introduced for commercial purposes about a decade ago [14]. In addition, Patiño et al. (2021) suggest that variations in the shell morphology of L. fulica in Colombia are influenced by environmental, management, or genetic differences between the cis- and trans-Andean regions [15]
This study aims to assess the genetic diversity of L. fulica in Cali, a city located in southwestern Colombia, by examining haplotype and nucleotide diversities. The findings will enhance our understanding of the species’ invasive potential in the region.

2. Materials and Methods

This study focuses on Cali City, the capital of the Valle del Cauca department in southwestern Colombia (Figure 1). The city has a population of around 2.5 million residents. It is divided into 6 localities, with 22 urban areas (communes) and 15 rural areas. Each locality features diverse environments influenced by human activities, including urban gardens and natural green spaces. Snails were collected from various sites across the city, including parks, gardens, and streets lined with vegetation. From May 2023 to July 2024, we analyzed 578 ADN snail samples over three different periods. To build a robust genetic dataset, we manually gathered at least 17 individuals from each site, ensuring minimal disruption to the local environment.
Approximately 30 mg of ethanol-preserved foot muscle tissue was utilized for DNA extraction, using a Blood/Cell/Tissue Genomic DNA Extraction Kit (ELK Biotechnology EP007®) according to the protocols provided with the kit. The isolated DNA was then used for the polymerase chain reaction (PCR) amplification and sequencing of the 16S rRNA gene fragment with two sets of primers: 16S1i (sense), 5′-TGA CTG TGC AAA GGT AGC ATA A-3′, and 16S_SSCP2i (anti-sense), 5′-CCT AGT CCA ACA TCG AGG TC-3′ [2]. PCR amplifications were performed in a final reaction mixture of 25 µL containing OneTaq buffer 1X, 0.2 μM of each primer, and 2 µL of template DNA. An Applied Biosystems Veriti Dx Thermal Cycler was used for PCR amplification, following the conditions outlined by [2]. This included an initial denaturation step at 94 °C for 30 s, followed by 35 cycles of denaturation at 94 °C for 30 s, annealing at 45 °C for 30 s, and extension at 68 °C for 1 min, concluding with a final extension at 68 °C for 5 min. The PCR products were visualized using a 1.2% agarose gel. The amplified PCR products were subsequently purified and sequenced using Sanger sequencing. We utilized a fragment of approximately 294 bp from the 16S rRNA gene, following the methods outlined by [2]. For our comparisons, longer sequences were adjusted using BioEdit 7.7 software [16]. The amplified sequences were aligned using Clustal W within MEGA 11 software [17]. In total, we generated 578 16S rRNA sequences for this study. Additionally, we included nineteen 16S rRNA haplotypes (labeled A to S) previously documented by [2,7], as well as four new haplotypes (T to W) identified by [8].
Nucleotide diversity (π) and haplotype diversity (h) were estimated using DNAsp v.6.12 [18]. To visualize the relationships among haplotypes in the Cali population, haplotype networks were constructed using Population Analysis with Reticulate Trees (PopART) [19]. Finally, Tajima’s D index was applied to investigate whether the populations had experienced recent demographic changes, such as a bottleneck or expansion [20].

3. Results

This study’s 578 Cali sequences generated a nucleotide diversity (π) of 0.00124, with 30 segregating sites and three parsimony-informative sites. Tajima’s D index was −2.41202. Two 16S rRNA haplotypes, designated as C and D, were identified (Figure 2). Each node in the haplotype network represents a distinct haplotype. In the left image, there are two large nodes. The node at the top corresponds to the most frequent haplotype, C. From urban area 3 (the dark-green portion), lines extend from this node, connecting it to several less frequent haplotypes: F, V, U, S, and T. On the other hand, the node at the bottom represents the second-most frequent haplotype, D. It is observed that from urban area 1 (the first light-green portion), a line connects this node to the less frequent haplotypes A and G. These results indicate that these nodes are similar, differing by only one or two molecular variants. Out of the 578 samples analyzed, haplotype C was present in 61 samples, accounting for 11% of the total, while haplotype D was found in 517 samples, representing 89%.
The haplotype distribution across the 22 urban areas of Cali, Colombia (Table 1) revealed significant variation in the proportion of individuals with haplotype C and haplotype D across different communes and localities. For instance, in Cali Aguacatal, 94% of individuals exhibited haplotype D, while only 6% had haplotype C. In Cauca Norte, 82% of individuals possessed haplotype D, whereas 18% had haplotype C. In urban area 20, 100% of individuals carried haplotype D, indicating complete homogeneity in the haplotype distribution within that locality. Most communes showed a predominance of haplotype D. For example, in urban area 4 (Cauca Norte), 91% of individuals exhibited haplotype D, and 9% exhibited haplotype C. Similarly, Pance Lili had a high percentage of individuals (96%) with haplotype D, while only a small percentage (4%) showed haplotype C. However, some communes, such as urban areas 3 and 5, demonstrated a more balanced distribution between the two haplotypes; in urban area 3, 65% of individuals had haplotype C, and 35% had haplotype D. In urban area 5, 43% exhibited haplotype C, compared to 57% with haplotype D. Additionally, several communes, including urban areas 16, 14, and 22, had individuals with haplotype D only (100%).
The proportion of individuals with haplotype D typically increased over time (Table 2). In the Cali Aguacatal locality, there was a significant shift from a higher percentage of haplotype C during the May–July period (33%) to a much lower percentage in the November 2023–April 2024 period (14%), while haplotype D showed a considerable increase during both periods. In the Cauca Norte locality, haplotype D remained dominant, though haplotype C showed a slight increase during the November–April period (19%) compared to earlier periods. Haplotype D continued to be overwhelmingly predominant throughout all time frames. The Cañaveralejo locality exhibited a similar pattern, with haplotype D being the dominant haplotype. The prevalence of haplotype C fluctuated slightly across the periods but remained relatively low overall. In the Pondaje locality, haplotype D was extremely dominant, especially in the August–October period (95%) and the November-April period (100%), with haplotype C nearly absent in the later period (0%). In the Cauca Sur locality, only haplotype D was found throughout the observed period, without any presence of haplotype C. This area demonstrated a complete dominance of haplotype D, particularly in the later months. Similarly, in the Pance Lili locality, haplotype D was the only haplotype present in the November–April period, with haplotype C existing only in very low percentages earlier. Ultimately, only haplotype D remained in this locality as well.

4. Discussion

Genetic studies of L. fulica populations provide valuable insights into the species’ evolutionary dynamics, including its adaptation to new environments, rapid population growth, and genetic structure in introduced regions identified by Vijayan et al. (2022) [8]. The haplotype network of L. fulica includes 23 distinct haplotypes, reflecting a considerable level of genetic diversity within the population. The network shows that most haplotypes are closely related, with a few distinct haplotypes branching off from the central, most frequent haplotype, suggesting recent evolutionary divergence. This pattern indicates that L. fulica may have undergone recent population expansion or gene flow, contributing to its current genetic structure.
In our study, we identified two 16S haplotypes, C (11%) and D (89%), for L. fulica in Cali, a city located in southwest Colombia, South America. Previous research on South American populations has also identified both haplotypes C and D in neighboring countries of Colombia [2]. In Ecuador, Bolivia, and Brazil, haplotype C was reported at frequencies of 69%, 50%, and 100%, respectively, while haplotype D was found in Ecuador at a 26% and in Bolivia at a 50% frequency. These findings suggest that the giant African snail population in Cali has likely resulted from multiple introduction events, possibly from these South American countries.
In a previous study, it was proposed that L. fulica arrived in southern Colombia from Brazil through the Amazon region. Subsequently, the giant African snail population migrated to the northeastern and southwestern regions of Colombia [21]. A study on the dispersion of L. fulica in Ecuador recorded this species in over a thousand locations distributed mainly in the coastal and Amazonian areas of the country [22]. Furthermore, the snail was not found above 2500 m above sea level, which is consistent with the negative correlation this species exhibits with altitude, likely due to the low temperatures in these regions [23]. In the present study, our results suggest a second possible spread of L. fulica to Colombia from Ecuador. In Ecuador, the first recorded sighting of this snail was in 2005. However, it is believed to have been introduced in the late 1990s through CORPEI, an organization that promotes productive competitiveness in the country to produce snail slime [24]. The snails were later marketed as pets in the city of Esmeraldas, and by 2010, they were recorded for the first time in the Galapagos, specifically on Santa Cruz Island. Trade between Cali (Colombia) and Esmeraldas (Ecuador) is quite active, facilitated by their geographical proximity. A direct flight between the two cities takes approximately 1 h and 6 min, while the distance by road is around 300 km. Esmeraldas is known for producing and exporting cocoa, bananas, seafood, and fish to Colombia. Additionally, the city exports wood, shrimp, and various agricultural products.
To investigate the population’s genetic consequences of the invasion of L. fulica in Cali, nucleotide diversity (π) and Tajima’s D index were estimated (Tajima 1989). A nucleotide diversity of 0.00124 suggested relatively low genetic diversity in the sites studied. In general, π values range from 0 (no variation) to 1 (high variation), and values below 0.01 are often considered low. This result indicates that, on average, there were 0.124% differences in the nucleotides between the randomly selected pairs of sequences from these samples. The relatively low number of segregation sites (30) further supports the notion of low genetic diversity in this dataset. This is typical of a population with limited genetic variation, possibly due to a recent bottleneck, inbreeding, or selection for alleles. Three parsimony-informative sites suggest that the data provide some phylogenetic or evolutionary information, but the low number indicates that the genetic variation in this study was not very complex in terms of phylogenetic signal. There were only three sites that provided significant information about the evolutionary history of the population. The negative Tajima’s D index (−2.41202) suggests an excess of low-frequency variants in the population, which can be indicative of population expansion, positive selection, or bottlenecks. This is because in a population with an expansion or selective sweep, rare alleles may increase in frequency more quickly than expected under neutrality. Also, a negative value such as −2.41202 points to a significant departure from the neutral equilibrium model, suggesting that the population has gone through a recent population expansion or may have undergone a selection event that affected allele frequencies.
Invasive species like L. fulica often undergo an initial genetic bottleneck when introduced to a new environment, resulting in a loss of genetic diversity. However, the evolutionary and genetic changes in invasive species can also be influenced by environmental factors, human-induced selection, or reproductive strategies, which complicate the interpretation of the Tajima’s D results. For example, L. fulica has a strong preference for hot climatic conditions. It tolerates altitudes ranging from 1 to 1000 m above sea level, thrives in rainfall between 350 and 5000 mm per year, and has a temperature tolerance that spans from 2 °C to 45 °C, with an optimal temperature range between 22 °C and 32 °C [3]. Cali, where this study was conducted, has a tropical climate significantly influenced by its proximity to the equator and its altitude, an ideal environment for the snail. The city is located approximately 1000 m above sea level, resulting in moderate humidity levels that usually range from 70% to 80%. Cali generally experiences warm weather, with a dry season that lasts from June to September and a rainy season occurring from March to May and again from October to November. Each year, the city receives an average of 1000 to 1500 mm of rainfall. However, during this study, conducted from May 2023 to April 2024, the city of Cali experienced the El Niño phenomenon, which resulted in a prolonged dry season. This made the climate hotter and drier than normal, severely impacting water resources and causing snails to enter estivation or become inactive until humidity levels became adequate again [25].
Estivation is a state in which a snail reduces its activity and metabolic rate to conserve energy [25]. So, the snail creates a protective barrier called the epiphragm, a calcified mucosal layer that seals its shell. This barrier helps prevent water loss through evaporation and forms over about 14 days from iron, calcium, and phosphorus [26]. During this time, the snail hides underground or behind rocks to avoid direct sunlight [27]. Also, this adaptation aids in the unintentional transport of snails over long distances. Juvenile snails often hide in shipments of plants, flowers, and fruits, making them hard to detect [28]. Another important factor is the level of humidity, critical for the survival of juvenile individuals [29]; low humidity or drought can lead to desiccation. So, rising temperatures and changing precipitation patterns can stress snail populations, especially those already living in sensitive environments, potentially altering their survival, reproductive success, and geographic distribution.
Regarding the haplotypes identified in Cali, we observed that haplotype D was overwhelmingly more common across most communes and localities, with some areas exhibiting a 100% representation of haplotype D. Haplotype C, on the other hand, was much less frequent overall, with certain communes showing a small percentage of individuals possessing it (often less than 20%). A few communes, such as urban areas 3 and 5, showed a more balanced distribution between haplotypes C and D. There was significant geographic variation in the distribution of haplotypes, with certain localities being homogenous (e.g., urban area 20, where 100% of individuals had haplotype D), while others showed more diverse distributions. Table 2 illustrates that haplotype D became more dominant over time in most localities, especially as haplotype C decreased. This shift in haplotype distribution may have been related to environmental factors such as temperature, humidity, and rainfall, which were stable or showed only slight variations. These results may have been influenced by several factors, including natural selection, genetic drift, changes in population size, and migration, all of which can lead to variations in haplotype frequencies. Environmental or climatic shifts can also affect selective pressures on haplotypes within a population. For example, if the climate changes (El Niño phenomenon) in a way that favors certain adaptations, haplotypes associated with those traits may become more prevalent. In this context, haplotype D may have shown greater tolerance to changing conditions, while haplotype C might have struggled during prolonged dry seasons, resulting in a significant decline in its frequency of occurrence and capture. It is important to note that a low frequency of observation does not imply that haplotype C has disappeared. During the dry season, haplotype C may enter a state of estivation until humidity levels improve. Additionally, L. fulica is most active at dusk and dawn, particularly on cloudy or rainy days [22]. However, our study had limitations, as the snails were collected during the daytime.
Another characteristic of L. fulica is its ability to thrive in urban areas, particularly due to human activity. In Brazil, this species has been found in locations such as outside homes, in vacant lots, and within walls [23]. Its preference for urban environments stems from the abundant food resources available in these areas. This snail feeds on diverse materials, including plant matter, lichens, algae, fungi [30], and even waste products [1]. Observations have shown that it consumes wet cardboard, dead animals, and other snails of its species. Notably, it has also been recorded feeding on horse and mouse feces. Illegal waste dumps are unauthorized sites where individuals dispose of waste, commonly found in vacant lots, riverbanks, and other public areas. These dumps are often concealed and can accumulate over time, contributing to environmental contamination and the spread of L. fulica populations. In Cali, the most central communes, such as urban areas 1, 2, and 3 in the locality of Cali Aguacatal, tend to have populations between 100,000 and 200,000 inhabitants each, due to their high density and concentration of services. In contrast, the peripheral and more rural communes, such as urban area 22 (Pance Lili), have much smaller populations, with often less than 50,000 inhabitants according to the most recent census and estimates from the National Administrative Department of Statistics (DANE) in Colombia (https://www.dane.gov.co/index.php/estadisticas-por-tema/demografia-y-poblacion/proyecciones-de-poblacion; accessed on 15 October 2024)
In conclusion, the clear dominance of haplotype D in most areas might suggest that haplotype D is either more prevalent or better suited in these environments. However, further analysis is needed to understand the reasons for this pattern (e.g., environmental, genetic, or social factors).

Author Contributions

Conceptualization, A.C. and A.G.; methodology, A.C. and A.G.; software, A.C., M.C.R. and C.M.F.; validation, A.C.; formal analysis, M.C.R. and C.M.F.; investigation, A.C., M.C.R. and C.M.F.; resources, A.G. and A.C.; data curation, A.C. and C.M.F.; writing—original draft preparation, A.C.; writing—review and editing, A.C. and A.G.; supervision, A.C.; project administration, M.C.R. and C.M.F.; funding acquisition, A.G. and A.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research and APC were funded by a special cooperation agreement between the University of Santiago de Cali and the University of Valle (Project CI 71330), associated with the project “Eco-epidemiological research of the African giant snail plague (L. fulica) and its potential impact on the environmental health of the Valle del Cauca”, approved by the SGR-FCTI under the code BPIN 2020000100194.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The animal study protocol was approved by the Institutional Research Ethics Committee of Universidad Santiago de Cali (CICBA-184, 11/19/2019). The haplotype sequences used in this study are available on the NCBI website (https://www.ncbi.nlm.nih.gov/; accessed on 15 July 2023). The data generated in this study are available from the corresponding author upon request.

Acknowledgments

We would like to express our sincere gratitude to Mario Garcés-Restrepo of Universidad del Valle and Rubén Varela of Universidad Santiago de Cali for their invaluable feedback on our research. We also extend our heartfelt appreciation to Claudia Medina for her administrative support throughout this project.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Fontanilla Ian Kendrich, C. Achatina (Lissachatina) Fulica Bowdich: Its Molecular Phylogeny, Genetic Variation in Global Populations, and Its Possible Role in the Spread of the Rat Lungworm Angiostrongylus cantonensis (CHEN). Ph.D. Thesis, University of Nottingham, Nottingham, UK, 2010. [Google Scholar]
  2. Fontanilla, I.K.C.; Maria, I.M.P.S.; Garcia, J.R.M.; Ghate, H.; Naggs, F.; Wade, C.M. Restricted genetic variation in populations of Achatina (Lissachatina) fulica outside of East Africa and the Indian Ocean Islands points to the Indian Ocean Islands as the earliest known common source. PLoS ONE 2014, 9, e105151. [Google Scholar] [CrossRef] [PubMed]
  3. Rekha Sarma, R.; Munsi, M.; Neelavara Ananthram, A. Effect of climate change on invasion risk of giant African snail (Achatina fulica Férussac, 1821: Achatinidae) in India. PLoS ONE 2015, 10, e0143724. [Google Scholar] [CrossRef] [PubMed]
  4. Brenton-Rule, E.C.; Barbieri, R.F.; Lester, P.J. Corruption, development and governance indicators predict invasive species risk from trade. Proc. R. Soc. B Biol. Sci. 2006, 283, 20160901. [Google Scholar] [CrossRef]
  5. Kliks, M.M.; Palumbo, N.E. Eosinophilic meningitis beyond the Pacific Basin: The global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc. Sci. Med. 1992, 34, 199–212. [Google Scholar] [CrossRef]
  6. Barquet, J.C. Studies on the Achatinidae, a group of African Land Snail. Bull. Mus. Comp. Zool. 1950, 105, 1–216. [Google Scholar]
  7. Ayyagari, V.S.; Sreerama, K. Evaluation of haplotype diversity of Achatina fulica (Lissachatina) [Bowdich] from Indian sub-continent by means of 16S rDNA sequence and its phylogenetic relationships with other global populations. 3 Biotech 2017, 7, 252. [Google Scholar] [CrossRef] [PubMed]
  8. Vijayan, K.; Suganthasakthivel, R.; Naggs, F.; Fontanilla, I.K.; Soorae, P.S.; Sajeev, T.V.; Wade, C.M. Fine-scale geographical sampling and molecular characterization of the giant African land snail in its invasive range in Asia shows low genetic diversity, new haplotypes and the emergence of another haplotype from the Indian Ocean Islands. Biol. J. Linn. Soc. 2022, 137, 421–433. [Google Scholar] [CrossRef]
  9. Pollard, G.V.; Fields, A.; Taylor, B. Giant African Snail in the Caribbean sub-region. In Proceedings of the Caribbean Food Crops Society, Miami, FL, USA, 13–17 July 2008; Volume 44, pp. 126–134. [Google Scholar] [CrossRef]
  10. Thiengo, S.C.; Faraco, F.A.; Salgado, N.C.; Cowie, R.H.; Fernandez, M.A. Rapid spread of an invasive snail in South America: The giant African snail, Achatina fulica, in Brasil. Biol. Invasions 2007, 9, 693–702. [Google Scholar] [CrossRef]
  11. Darrigran, G.; Agudo-Padrón, I.; Baez, P.; Belz, C.; Cardoso, F.; Carranza, A.; Collado, G.; Correoso, M.; Cuezzo, M.G.; Fabres, A.; et al. Non-native mollusks throughout South America: Emergent patterns in an understudied continent. Biol. Invasions 2020, 22, 853–871. [Google Scholar] [CrossRef]
  12. Aquino, M. Achatina fulica in Brazil. REDVET Rev. Electrónica De Vet. 2010, 11, 1–7. [Google Scholar]
  13. De la Ossa-Lacayo, A.; De la Ossa, J.; Lasso, C. Registro del caracol africano gigante Achatina fulica (Bowdich 1822) (Mollusca: GastropodaAchatinidae) en Sincelejo, Costa Caribe de Colombia. Biota Colomb. 2012, 13, 247–252. [Google Scholar]
  14. Giraldo, A.; Bolívar-García, W.; Cantera, J.; Restrepo, M.G.; Colorado, A.G.; Gómez, M.; Cordoba, D.; Prado, A.; Patiño, A.; Garzón, C.G. Aspectos generales de la historia natural del caracol gigante africano (Achatina fulica Bowdich, 1822) en el Valle del Cauca. Innovaciencia 2017, 5, 3–4. [Google Scholar] [CrossRef]
  15. Patiño-Montoya, A.; Murillo-García, O.; Giraldo, A. Allometry and geographic variation of the morphology of Achatina fulica (Achatinidae) in Colombia. Molluscan Res. 2021, 41, 57–63. [Google Scholar] [CrossRef]
  16. Hall, T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser 1999, 41, 95–98. [Google Scholar]
  17. Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
  18. Rozas, J.; Ferrer-Mata, A.; Sánchez-DelBarrio, J.C.; Guirao, R.S.; Librado, P.; Ramos-Onsins, S.E.; Sánchez-Gracia, A. DnaSP6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 2017, 34, 3299–3302. [Google Scholar] [CrossRef]
  19. Leigh, J.W.; Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 2015, 6, 1110–1116. [Google Scholar] [CrossRef]
  20. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA Polymorphism. Genetics 1989, 123, 585–595. [Google Scholar] [CrossRef]
  21. Montoya, A.P.; López, A.G. Diez años del caracol gigante africano en Colombia: Revisión de la investigación y divulgación desarrollada entre 2008–2017. Ecol. Austral. 2020, 30, 125–133. [Google Scholar] [CrossRef]
  22. Albuquerque, F.; Peso-Aguiar, M.; Assunção-Albuquerque, M. Distribution, feeding behavior, and control strategies of the exotic land snail Achatina fulica (Gastropoda: Pulmonata) in the northeast of Brazil. Braz. J. Biol. 2008, 68, 837–842. [Google Scholar] [CrossRef]
  23. Gołdyn, B.; Guayasamín, P.R.; Sanchez, K.A.; Hepting, L. Note on the distribution and invasion potential of Achatina fulica Bowdich, 1822 (Gastropoda: Pulmonata: Achatinidae). Folia Malacol. 2016, 2, 85–90. [Google Scholar] [CrossRef]
  24. Correoso, M.; Coello, M. Modelación y distribución de Lissachatina fulica (Gastropoda, Achatinidae) en Ecuador. Potenciales impactos ambientales y sanitarios. Rev. Geoespacial 2009, 6, 79–90. [Google Scholar]
  25. Rahman, M.S.; Raut, S.K. Factors inducing aestivation of the giant African land snail Achatina fulica Bowdich (Gastropoda: Achatinidae). Proc. Zool. Soc. 2010, 63, 45–52. [Google Scholar] [CrossRef]
  26. Ademolu, K.O.; Fantola, F.O.; Bamidele, J.A.; Dedeke, G.A.; Idowu, A.B. Formation and composition of epiphragm in three giant African land snails (Achatina marginata, Achatina fulica and Achatina achatina). Ruthenica 2016, 26, 165–169. [Google Scholar]
  27. Fagbuaro, O.; Oso, J.A.; Edward, J.B.; Ogunleye, R.F. Nutritional status of four species of giant land snail in Nigeria. J. Zhejiang Univ. Sci. B 2006, 7, 686–689. [Google Scholar] [CrossRef] [PubMed]
  28. Gutiérrez Gregoric, D.; Beltramino, A.; Vogler, R.; Rumi, A. Expansión del rango de distribución de Achatina fulica Bowdich, 1822 (Gastropoda) en la Argentina y su concordancia con modelos predictivos. Amici Molluscarum 2013, 21, 17–21. [Google Scholar]
  29. Chase, R.; Croll, R.P.; Lubin Zeichner, L. Aggregation in Snails, Achatina fulica. Behav. Neural Biol. 1980, 30, 218–230. [Google Scholar] [CrossRef]
  30. Vogler, R.E.; Beltramino, A.A.; Sede, M.M.; Gregoric, D.E.G.; Núñez, V.; Rumi, A. The giant African snail, Achatina fulica (Gastropoda: Achatinidae): Using bioclimatic models to identify South American areas susceptible to invasion. Am. Malacol. Bull. 2013, 31, 39–50. [Google Scholar] [CrossRef]
Diversity 17 00177 g001
Figure 1. A base map showing the location of Cali, Colombia. Cali is situated in the southwestern region of Colombia (highlighted in the red box). Its geographic coordinates are approximately 3.4516° N latitude and 76.5320° W longitude. Sources: http://www.maphill.com/colombia/valle-del-cauca/cali/location-maps/physical-map/?most-similar-to=maps/physical-map/ (accessed on Day 15 October 2024) and https://liderando.co/wp-content/uploads/2020/08/image-1.jpg./ (accessed on Day 15 October 2024).
Figure 1. A base map showing the location of Cali, Colombia. Cali is situated in the southwestern region of Colombia (highlighted in the red box). Its geographic coordinates are approximately 3.4516° N latitude and 76.5320° W longitude. Sources: http://www.maphill.com/colombia/valle-del-cauca/cali/location-maps/physical-map/?most-similar-to=maps/physical-map/ (accessed on Day 15 October 2024) and https://liderando.co/wp-content/uploads/2020/08/image-1.jpg./ (accessed on Day 15 October 2024).
Diversity 17 00177 g001
Diversity 17 00177 g002
Figure 2. The median-joining haplotype network of L. fulica (23 haplotypes) based on 16 sRNA gene sequences (255 bp). The size of each circle indicates the frequency of the corresponding haplotype, while the colors of the circles represent the 22 urban areas (communes) in the city of Cali where each haplotype was recorded. Additionally, the frequencies of haplotypes C and D are shown across the three time intervals during which the snails were collected.
Figure 2. The median-joining haplotype network of L. fulica (23 haplotypes) based on 16 sRNA gene sequences (255 bp). The size of each circle indicates the frequency of the corresponding haplotype, while the colors of the circles represent the 22 urban areas (communes) in the city of Cali where each haplotype was recorded. Additionally, the frequencies of haplotypes C and D are shown across the three time intervals during which the snails were collected.
Diversity 17 00177 g002
Table 1. The distribution of the 16S rRNA haplotype frequencies of L. fulica by urban area (commune) and locality in Cali, Colombia. The table presents the number of individuals collected during three distinct time intervals: 1. from May 2023 to July 2023; 2. from August 2023 to October 2023; and 3. from November 2023 to April 2024. The last interval lasted for six months instead of three due to an unexpectedly prolonged dry season in Cali caused by the El Niño phenomenon, which affected the observation and collection of snails. Most communes exhibited a predominance of haplotype D.
Table 1. The distribution of the 16S rRNA haplotype frequencies of L. fulica by urban area (commune) and locality in Cali, Colombia. The table presents the number of individuals collected during three distinct time intervals: 1. from May 2023 to July 2023; 2. from August 2023 to October 2023; and 3. from November 2023 to April 2024. The last interval lasted for six months instead of three due to an unexpectedly prolonged dry season in Cali caused by the El Niño phenomenon, which affected the observation and collection of snails. Most communes exhibited a predominance of haplotype D.
Urban Area (Commune)Num. of Ind. per Time IntervalTOTALHaplotype LocalitiesTOTALHaplotype
123C (%)D (%)C (%)D (%)
11697322 (6)30 (94)Cali Aguacatal7618 (24)58 (76)
212411275 (19)22 (81)
38631711 (65)6 (35)
41175232 (9)21 (91)Cauca Norte11320 (18)93 (82)
59682310 (43)13 (57)
6695203 (15)17 (85)
71086243 (12)21 (88)
810103232 (9)21 (91)
91224186 (33)12 (67)Cañaveralejo969 (9)87 (91)
101177252 (8)23 (92)
191289291 (3)28 (97)
201011324024 (100)
1114113287 (25)21 (75)Pondaje12510 (8)115 (92)
1211109301 (3)29 (97)
13141111362 (5)34 (95)
161171331031 (100)
141514837037 (100)Cauca Sur961 (1)95 (99)
1514811331 (3)32 (97)
211110526026 (100)
17873182 (11)16 (89)Pance Lili723 (4)69 (96)
18121113361 (3)35 (97)
2274718018 (100)
TOTAL24418015457861 (11)517 (89)
Table 2. The distribution of haplotype C and D in different localities of Cali, Colombia, for three distinct time intervals show that haplotype D became increasingly dominant over time, while haplotype C declined. This shift was likely associated with stable environmental factors such as temperature, humidity, and rainfall. Cali’s tropical climate features high humidity and moderate precipitation, although there was a significant decrease in rainfall from November 2023 to April 2024, likely due to El Niño. This suggested that if the dry season continued to be prolonged, local conditions might favor the ongoing dominance of haplotype D in the region.
Table 2. The distribution of haplotype C and D in different localities of Cali, Colombia, for three distinct time intervals show that haplotype D became increasingly dominant over time, while haplotype C declined. This shift was likely associated with stable environmental factors such as temperature, humidity, and rainfall. Cali’s tropical climate features high humidity and moderate precipitation, although there was a significant decrease in rainfall from November 2023 to April 2024, likely due to El Niño. This suggested that if the dry season continued to be prolonged, local conditions might favor the ongoing dominance of haplotype D in the region.
LocalitiesMay 2023–July 2023August 2023–October 2023November 2023–April 2024
Hap C (%)Hap D (%)Hap C (%)Hap D (%)Hap C (%)Hap D (%)
Cali Aguacatal12 (33)24 (67)4 (21)15 (79)2 (14)19 (86)
Cauca Norte10 (22)36 (78)5 (13)35 (87)5 (19)22 (81)
Cañaveralejo4 (9)41 (91)2 (7)26 (93)3 (13)20 (87)
Pondaje8 (16)42 (84)2 (5)37 (95)036 (100)
Cauca Sur040 (100)032 (100)1 (4)23 (96)
Pance Lili2 (7)25 (93)1 (5)21 (95)023 (100)
Cali Weather conditions *
Average maximum temperature30 °C30 °C30 °C
Average minimum temperature21 °C21 °C21 °C
Average monthly rainfall80–130 mm per month80–130 mm per month50–100 mm per month
Average monthly humidity80–85%80–85%80–85%
* https://bart.ideam.gov.co/cliciu/cali/cali.htm (accessed on 15 October 2024).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Castillo, A.; Rodríguez, M.C.; Franco, C.M.; Giraldo, A. The Genetic Diversity of the Invasive Species Lissachatina fulica in the Urban Area of Cali, Colombia. Diversity 2025, 17, 177. https://doi.org/10.3390/d17030177

AMA Style

Castillo A, Rodríguez MC, Franco CM, Giraldo A. The Genetic Diversity of the Invasive Species Lissachatina fulica in the Urban Area of Cali, Colombia. Diversity. 2025; 17(3):177. https://doi.org/10.3390/d17030177

Chicago/Turabian Style

Castillo, Andres, María C. Rodríguez, Claudia M. Franco, and Alan Giraldo. 2025. "The Genetic Diversity of the Invasive Species Lissachatina fulica in the Urban Area of Cali, Colombia" Diversity 17, no. 3: 177. https://doi.org/10.3390/d17030177

APA Style

Castillo, A., Rodríguez, M. C., Franco, C. M., & Giraldo, A. (2025). The Genetic Diversity of the Invasive Species Lissachatina fulica in the Urban Area of Cali, Colombia. Diversity, 17(3), 177. https://doi.org/10.3390/d17030177

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop