Life cycle and food consumption potential of the invasive terrestrial slug Meghimatium pictum (Stoliczka, 1873)

Ciclo de vida e potencial de consumo alimentar da lesma terrestre invasora Meghimatium pictum(Stoliczka, 1873)

ABSTRACT:

The invasive chinese slug Meghimatiumpictum (Stoliczka, 1873) (Stylommathophora: Philomycidae) is originally from Asia, and it has been introduced in Latin American countries like Argentina and Brazil, where it is considered a critical horticultural pest. This species also became an intermediate host for the nematode AngiostrongyluscostaricensisMorera&Cespedes, 1971(Strongylida: Metastrongylidae), which can cause abdominal angiostrongyliasis in humans when ingested molluscs or their mucus containing larvae released on fruit and vegetables. This research aimed to investigate the biological parameters of the life cycle of M. pictum and evaluate its food preference to understand the species’ behavior and provide information on the choice of safer pest management and control methods. We observed that 68 and 75% of the grouped and isolated slugs, respectively, survived 26 weeks (180 days) under laboratory conditions. In addition, the individuals kept isolated had higher body mass (2.8 ± 0.6 g), length (3.3 ± 0.8 cm), and width (0.37 ± 0.3 cm) than grouped specimens. We also found that M. pictum has indeterminate growth and an annual reproductive cycle. Concerning food preference, slugs better accepted lettuce at different developmental stages (neonate, juvenile, and adult). Our study presents the first description of the M. pictum life cycle. We concluded that M. pictum has undefined biological parameters, which hampers its laboratory rearing. However, we also demonstrate its potential as a pest for different horticultural crops, which will require the development of management strategies.

Key words:
Philomycidae; terrestrial gastropod; reproduction; growth.

RESUMO:

A lesma invasora Meghimatium pictum (Stoliczka, 1873) (Stylommathophora: Philomycidae) é originária da Ásia e foi introduzida em países latino-americanos como Argentina e Brasil, onde é considerada uma praga hortícola severa. Esta espécie também se tornou um hospedeiro intermediário do nematoide Angiostrongylus costaricensis Morera & Céspedes, 1971 (Strongylida: Metastrongylidae), que pode causar a infecção angiostrongilíase abdominal em humanos quando ingerido o molusco ou frutas e vegetais contendo o seu muco contaminado com larvas. Esta pesquisa teve como objetivo investigar os parâmetros biológicos do ciclo de vida de M. pictum e avaliar sua preferência alimentar para entender o comportamento da espécie e fornecer informações sobre a escolha futura de métodos mais seguros de manejo e controle desta praga. Observamos que 68 e 75% das lesmas agrupadas e isoladas, respectivamente, sobreviveram 26 semanas (180 dias) em condições de laboratório. Além disso, os indivíduos mantidos isolados apresentaram maior massa corporal (2,8 ± 0,6 g), comprimento (3,3 ± 0,8 cm) e largura (0,37 ± 0,3 cm) do que os espécimes agrupados. Também descobrimos que M. pictum tem crescimento indeterminado e ciclo reprodutivo anual. Com relação à preferência alimentar, a alface foi bem aceita pelas lesmas em diferentes estágios de desenvolvimento (recém-nascido, juvenil e adulto). Nosso estudo apresenta a primeira descrição do ciclo de vida de M. pictum. Concluímos que M. pictum possui parâmetros biológicos indefinidos, com ciclo de vida longo o que dificulta sua criação em laboratório. No entanto, também demonstramos seu potencial como praga para diferentes culturas hortícolas, o que exigirá o desenvolvimento de estratégias de manejo.

Palavras-chave:
Philomycidae; gastrópode terrestre; reprodução; crescimento

INTRODUCTION:

Mollusca is considered the second-largest Phylum in the animal kingdom. This group stands out for the ability of its species to occupy the most varied environments, whether aquatic or terrestrial (THIENGO et al., 2007). Approximately 700 species of terrestrial mollusks have been recorded in Brazil, of which 42 occur in the state of Paraná (COLLEY, 2012). Most species of terrestrial mollusks belong to Stylommatophora, with two pairs of invaginable eyes and hermaphroditism as common characteristics (STURM et al., 2006). Furthermore, some species of terrestrial gastropods introduced in Brazil may be associated with zoonoses. Some of these species are AchatinafulicaBowdich, 1822; Bradybaenasimilaris (Férussac, 1821); Deroceraslaeve (Muller, 1774), Limacusflavus (Linnaeus, 1758); Limax maximus (Linnaeus, 1758); Helix aspersa Muller, 1774 (THIENGO et al., 2007), and Meghimatiumpictum(Stoliczka, 1873) (GOMES et al., 2011; RODRIGUEZ et al., 2019; THIENGO et al., 2022). Another negative factor is the mucus left by gastropods on food during locomotion, making the products unfeasible for human consumption (LANDAL et al., 2019).

Philomycidae includes terrestrial gastropod species that can feed on different plants, also causing severe injuries, and affecting crop productivity (BARONIO et al., 2014; WHITE-MCLEAN & CAPINERA, 2014; CAPINERA & RODRIGUES, 2015; LANDAL et al., 2019). In Brazil, there is only one species of this family, represented by M. pictum, where it is reported damaging vineyards (Vitislabrusca L.; Vitaceae) (BARONIO et al., 2014; RODRIGUEZ et al., 2019) and strawberry crops (Fragaria × ananassaDuch.;Rosaceae) (LANDAL et al., 2019). It was possibly accidentally introduced in Brazil through mushroom importation from Asiatic countries (GOMES et al., 2011).

In Brazil, since its first record by GOMES et al. (2011), the slug M. pictum has spread its occurrence, reaching a widespread distribution throughout the southern region (BARONIO et al., 2014; LANDAL et al., 2019), showing that it has high adaptability to environments with different edaphoclimatic conditions. This species also became an intermediate host for the nematode AngiostrongyluscostaricensisMorera&Cespedes, 1971 (Strongylida: Metastrongylidae), which can cause abdominal angiostrongyliasis in humans when ingested. Recently, the risk of infection associated with grape consumption infested by M. pictum was confirmed (RODRIGUEZ et al., 2019).

Despite its potential as an agricultural pest and the possible risk of human infection, there are no studies on the behavior, biology, and food preferences of M. pictum in the places where it has been introduced. Consequently, there are no protocols for the mass rearingof M. pictum in the laboratory, hindering the establishment of management strategies for this species. Thus, this study aimed to evaluate the biological parameters of M. pictum under laboratory conditions to understand its behavior, life cycle, and food preference.

MATERIALS AND METHODS:

Collection procedures

Mass rearing in the laboratory began by collecting specimens of juvenile and adults of M. pictum in native forests close to production areas of mushrooms (Agaricusbisporus (JE Lange) Imbach; Agaricaceae) in the municipality of São José dos Pinhais, state of Paraná (25º34’S - 49º06’W). We collected the slug samples manually, using gloves, between January and March 2019, seeking under trunks, senescent plant material, and debris. Then, we placed the slugs in plastic containers with moistened paper sheets and soil from the collection points to keep samples alive during transport. Species identification was carried out at the Laboratory of Malacology of FIOCRUZ, Rio de Janeiro, Brazil. Subsequently, voucher specimens were listed in the Malacology Collection of the Oswaldo Cruz Institute (CMIOC), Rio de Janeiro, Brazil, under the registration code CMIOC 10.784.

Mass rearing

The methodology for rearing M. pictum was adapted from CAPINERA & RODRIGUES (2015). We sorted the collected specimens into groups of four to five individuals, which were kept in 250 mL plastic containers (7.25 cm in height, 8.75 cm in diameter, with a base of 6.65 cm) and sealed with plastic wrap. Each container had a 3 cm layer of sterilized vegetable soil (Riga snikers^® - organic compound, mineral fertilizer, poultry manure, earthworm humus) at the bottom, moistened with 10 mL of distilled water every 48 h. Slugs were fed ad libitum with formulated rabbit food (Supra Coelho Agro^® - Alisul Alimentos S.A.). Food replacement occurred at 48-hour intervals. Laboratory conditions for slug rearing were 25 ± 2 °C, 70 ± 10% relative humidity (RH), and 14 h photoperiod. We also introduced specimens of juveniles and adults collected between February and April 2020 from the same sampling points mentioned above to sustain the mass rearing and keep the population’s genetic variability.

Bioassays

Life cycle

Two treatments were conducted for lifecycle description, one consisting of 30 Petri dishes (9 cm in diameter × 1.5 cm height) containing one slug each, and the other with 30 Petri dishes containing four slugs each (grouped slugs). The biological stages were observed and photographed with a Sony DSC-H300 camera, and the linear measurements were taken using a 150 mm plastic caliper. Life cycle observations occurred daily for 26 weeks (180 days), recording the modification in color onset time of sexual maturity, rearing season, total number of eggs produced per reproductive event, hatchability, and periods of the egg, neonate, juvenile, and adult stages.

Biological parameters ofMeghimatiumpictum

The biological experiment was developed under laboratory conditions (25 ± 2 °C, 70 ± 10% RH, and 14 h photoperiod). Egg masses removed from the slugs’ mass rearing were stored in Petri dishes (9 cm in diameter × 1.5 cm height), lined with filter paper (weight of 80 g/m² and 0.2 mm thick), moistened with distilled water every 48 h, and sealed with plastic wrap. After the eggs hatched, the neonate slugs were counted and sorted into two treatments with 50 replicates (slugs) each. The first treatment comprised grouped slugs (four specimens per replicate), and the second comprised isolated slugs (one specimen per replicate). Slug feeding consisted of discs of mature lettuce leaves with 2 cm in diameter, which were replaced every 48 h. The life cycle was assessed by daily observations for 26 weeks (180 days), during which we recorded the survival rate (%), laying period (days), and duration of developmental stages (days). From the first week of life and every 15 days, measures of slug mass (g) and size (length and width in cm) were recorded using an electronic analytical scale (0.0001g) (Gehaka, São Paulo) and a 150 mm plastic caliper, respectively. The specimens were placed on filter paper moistened with distilled water to prevent dehydration and facilitate locomotion, waiting for the slug’s body to be fully extended during locomotion to measure its length and width (STURM et al., 2007).

Consumption potential on different hosts

The consumption potential was assessed on 360 M. pictum slugs from the maintenance rearing, based on their body mass. Therefore, the slugs were divided into neonates (0.7 ± 0.2 g), juveniles (1.6 ± 0.3 g), and adults (3.3 ± 0.4 g). Six types of food were evaluated as a feeding source for each mass body category: [Japanese cucumber (Cucumissativus L.; Cucurbitaceae), beetroot (Beta vulgaris L. var. esculenta L.; Amaranthaceae), carrot (Daucuscarota L. subsp. sativus L.; Apiaceae), chayote (Sechiumedule Sw.; Cucurbitaceae), lettuce cultivar Veronica (Lactuca sativa L.; Asteraceae), and Italian zucchini cultivar Caserta (Cucurbita pepo L.; Cucurbitaceae)]. For each category of body mass, 30 replicates per treatment were used. The foods were cut into 2 cm diameter discs and placed in Petri dishes (9 cm diameter × 1.5 cm height) on filter paper (80 g/m² weight and 0.2 mm thick), which was moistened with distilled water every 48 h. Food consumption was evaluated considering the difference between the initial and final food mass after 72 h of consumption. The slugs fasted for 48 h before feeding in all treatments (aonaga cucumber, beetroot, carrot, chayote, lettuce, and zucchini).

Statistical analysis

A completely randomized design was carried out. Generalized linear models with a Poisson distribution and a log link function were used to evaluate the leaf consumption and survival variables over the weeks (NELDER et al., 1972). Data regarding differences in length, width, survival, and weight of specimens, when reared isolated, and grouped for the same evaluation week, were submitted to the t-test with a significance level of 5%. After detecting significant differences between treatments, data were analyzed by the Tukey test at a 5% significance level. All analyses were performed using the statistical software R version 2.15.1 (R CORE TEAM, 2018).

RESULTS:

Our study presents the first description of the M. pictum life cycle, including eggs, neonate, juvenile, and adult stages (Figure 1). Concerning the egg stage, we identified mass-like laying containing an average of 67.29 ± 10.65 eggs each (Figure 1A). Slugs laid these egg masses on the substrate surface. Interestingly, rearing slugs showed a slower locomotion behavior than usual, spending more time resting close to the container walls. These slugs presented a swelling in the anterior dorsal region, which shriveled soon after oviposition.

Figure 1
Meghimatiumpictum (Gastropoda: Philomycidae) specimens at different life cycle stages: oviposition (A) showing the respiratory opening, pneumostome (black arrow), and an egg cluster (Ec); eggs (B) and a one-day-old neonate (C) with the dorsal stripe already formed in the embryo and well visible in the neonate (white arrow); 1.6 cm long juvenile (D) and 3.2 cm long adult (E), showing the lateral stripes already formed (white arrow with red border).

Eggs hatch 18 ± 3 days after laying on average. During oviposition, the eggs are translucent and have a gelatinous appearance. A mid-dorsal stripe of the mantle becomes evident when the hatching time is near (Figure 1B). As the hatching time approaches, this stripe becomes darker, constituting the first formed feature during individual development.

Subsequently, the neonatal stage shows slugs with reduced tentacles, eyes close to the anterior region, and the black mid-dorsal stripe from the middle of the anterior region to the end of the posterior region (Figure 1C). This is the most critical stage for individual survival, as the mantle is poorly developed, translucent, and sensitive to moisture. The radula in the mouth apparatus is also underdeveloped. This characteristic relates to the preference for soft foods with high moisture content, such as lettuce.

After a week of development, the color pattern changes. The mantle varies from translucent to the light pink color characteristic of the species, and the mid-dorsal stripe becomes dark brown (Figure 1D). Two lateral stripes arose after a month and a half of development, appearing in the right and left side of the head each (anterior region) and advancing laterally to the posterior end, where they meet the mid-dorsal stripe. The ocular tentacles develop during the transition from the neonate to the juvenile stage. Therefore, Meghimatiumpictum reaches the juvenile form when its external morphological features are well developed.

The adult stage is marked by the beginning of reproductive life and occurs when M. pictum individuals reach a mean body mass of approximately 1.6 ± 0.3 g. We observed individuals growing even after their first reproductive event, indicating indeterminate growth (Figure 1E). Under climatic conditions similar to the present study, M. pictum can show an annual reproductive cycle, with more than one oviposition that would coincide between August and December, from the winter end until the spring in the southern hemisphere.

Under the laboratory conditions, grouped individuals of M. pictum showed a mortality rate of 32% over the first 11 weeks. From the 11^th week, survival was 68% and remained constant until the last week of evaluation (Figure 2). Isolated individuals showed 78% survival until the 25^th week, slightly dropping to 75% approximately at the 26^th week (Figure 2). A significantly higher survival for isolated than grouped slugs was observed by the t-test of specimens reared on lettuce leaves (Figure 2).

Figure 2-
Survival rate (%) of Meghimatiumpictum specimens kept isolated and in groups under 26 weeks (180 days). ^*Asterisks indicate significant differences between treatments (within the same week) according to Student’s t-test (P < 0.05).

Isolated specimens had significantly higher measurements of body mass (Figure 3A), length (Figure 3B), and width (Figure 3C) than individuals kept in groups over the 180 days of evaluation. After assessing the consumption of potential host plants by M. pictum slugs, we obtained variable results about neonate, juvenile, and adult life stages (Table 1). However, for all evaluated developmental stages, the most consumed food by M. pictum was lettuce, followed by aonaga cucumber, chayote, zucchini, carrot, and beetroot (Table 1). There was a significant increase in the consumption of zucchini, beetroot, carrot, chayote, and aonagacucumber during the adult stage. For beetroot and carrot, specifically, there was a statistical difference in consumption only for adult slugs, with less consumption of these foods by neonates and juveniles.

Figure 3
- Mean body mass (g), length (cm), and width (cm) of isolated and grouped individuals of Meghimatiumpictum evaluated over 26 weeks (180 days). ^*Asterisks indicate significant differences between treatments (within the same week) according to Student’s t-test (P < 0.05)

Table 1
Consumption (g) (mean ± standard error) of aonaga cucumber, beetroot, carrot, chayote, lettuce, and zucchini by Meghimatiumpictum slugs classified in three developmental stages.

Food	------------------------------------------------Slug developmental stages----------------------------------------------
	Neonate	Juvenile	Adult
Aonaga cucumber	79.86 ± 1.10 Bb*	78.08 ± 1.21 Bb	84.07 ± 1.36 Ba
Beetroot	3.03 ± 0.20 Db	4.78 ± 0.21 Db	8.18 ± 0.30 Ea
Carrot	6.97 ± 0.68 DC	11.49 ± 0.50 Db	22.11 ± 0.46 Da
Chayote	54.67 ± 0.61 Cb	65.19 ± 0.08 Bab	76.33 ± 0.61 BCa
Lettuce	92.54 ± 1.11 Aa	93.40 ± 0.57 Aa	96.64 ± 0.23 Aa
Zucchini	55.25 ± 0.13 Cb	58.27 ± 0.82 Cb	64.22 ± 0.39 Ca

• ^*Means followed by the same uppercase letter in the same column and lowercase letter in the same row do not differ significantly (generalized linear model with an almost binomial distribution followed by Tukey’s post hoc test: P <0.05).

DISCUSSION:

Meghimatiumpictum has an annual reproductive cycle, with more than one oviposition over the winter end (August-September) extending until spring (October-December) in the southern hemisphere. SLOTSBO et al. (2013) also showed an annual reproductive cycle for the slug Arion lusitanicus J. Mabille 1868 (Gastropoda: Arionidae), although with an oviposition period from the end of spring with eggs hatching before the winter, in the northern hemisphere. The behavior of both species suggests a life cycle strategy of eggs hatching outside the critical winter period, which increases the chances of neonates’ survival.

The beginning of the reproductive life of M. pictum occurs in the juvenile stage, characterized by a body mass of approximately 1.6 ± 0.3 g. In addition, we observed a growth continuity after the first reproductive cycle, indicating that individuals were under indeterminate development. This same pattern was reported for B. similarisby CARVALHO et al. (2008), who described a slow growth in the adult stage, indicating that energy resources are preferentially allocated for reproduction after sexual maturity. In contrast, energy is mostly expended on the individual’s development in immature juveniles. ALMEIDA & BESSA (2001) also observed differences in the shell size of B. similaris, with isolated individuals showing larger shell sizes.

The energy expenditure ratio is also influenced by population density, as observed for the most significant growth in length and width for the isolated individuals concerning all analyzed specimens of our study. The more significant mass gain of isolated individuals can result from the lack of competitive pressure for space and food suffered by grouped individuals.

The reproductive stage commenced earlier for grouped individuals than for the isolated ones, indicating that the energy resources were used to reach sexual maturity instead of growth. In contrast, isolated specimens used energy resources to grow, waiting to find a mate to prioritize cross-fertilization. Similar results were observed by ALMEIDA & BESSA (2001) for B. similaris; in their study, isolated individuals reached sexual maturity one month after the grouped individuals.

Grouped specimens of M. pictum had lower longevity and survival rates than isolated individuals throughout the evaluation period of our research, as previously observed by HOMMAY et al. (2001) for LimaxvalentianusFérussac, 1822. The authors detected a high rate of cannibalism in the grouped individuals due to competition for space and food, resulting in a low survival rate. In the present study, although lower percent survival was observed in the grouped specimens, no cannibalism was observed, suggesting that this is not a common behavior of the species.

Meghimatiumpictum showed more potential for consumption of lettuce leaves than other food sources considering all developmental stages evaluated (neonate, juvenile, and adult). Similar results on the leaf consumption pattern were reported by CAPINERA & RODRIGUES (2015) for the land slug Leidyulafloridana (Leidy, 1851) (Gastropoda: Veronicellidae), who found that leaf consumption was higher as species body mass increased. Likewise, leaf consumption decreased when L. floridana specimens reached 8 g of body mass. Thus, considering that adult individuals of M. pictum used in our study had 3.3 ± 0.4 g, the detected increase in leaf consumption is in line with CAPINERA & RODRIGUES (2015).

In the present study, moisture (water content in the food) was the determining factor influencing consumption regarding food preference. Hence, neonate, juvenile, and adult slugs showed higher consumption of lettuce leaves than other food sources. Aonaga cucumber was the second most consumed food source, followed by zucchini and chayote, all with higher moisture content than carrot and beetroot, the less consumed food sources. Moisture need for the species’ survival was also observed in other studies. SILVA et al. (2009) found that substrate moisture affected the energy investment of Bulimulustenuissimus (d’Orbigny, 1835) (Gastropoda: Bulimulidae). This way, under unfavorable moisture conditions, B. tenuissimus allocates energy resources for growth rather than investing in reproduction as a survival strategy. In the present study, as specimens of M. pictum were subjected to a low moisture unfavorable environment, the slugs consume considerable amounts of leaves with high moisture contents. Less moist and hard foods, like carrots and beetroots, would lead to moisture loss during digestion, diminishing chances of survival.

Our results can be a basis for further studies on M. pictum behavior. In addition, we have established a protocol for the species’ collection and laboratory rearing to further evaluations on biological development, such as the influence of temperature, humidity, type of substrate, and photoperiod. Regarding pest management, we must consider the poor control of the few commercially available molluscicides (BARONIO et al., 2014), which represents an environmental concern (GALL & TOOKER, 2017). Thus, presenting ecological bases through the combination of the biology and food preferences of M. pictum can mitigate losses from agricultural damage. In addition, reducing agricultural damage by this slug can also diminish the risks of contamination with helminths. We also highlight that the species’ oviposition behavior differs from that in the field, with egg masses deposited below the soil surface, in crevices, and under stones. This behavioral change may be due to the controlled laboratory conditions, as the eggs must be protected from environmental variations and predators in the field.

CONCLUSION:

Our study presents the first description of the M. pictum life cycle, including eggs, neonate, juvenile, and adult stages. A protocol for the species’ collection and laboratory rearing is proposed. The slug M. pictum has indeterminate growth and an annual reproductive cycle. Meghimatiumpictum had a higher potential for consuming lettuce leaves compared to other vegetables at all stages of development. Different life cycle stages were characterized: mass oviposition; a one-day-old neonate, juvenile, and adult with different size and color patterns.

ACKNOWLEDGEMENTS

We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their financial support. We are also grateful to the FundaçãoAraucária for providing a research grant to the last author.

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• CR-2023-0101.R1

Edited by

Editor: Leandro Souza da Silva (0000-0002-1636-6643)

Publication Dates

• Publication in this collection
  23 Feb 2024
• Date of issue
  2024

History

• Received
  20 Feb 2023
• Accepted
  03 Oct 2023
• Reviewed
  13 Dec 2023