Growth parameters of the invasive gastropod Melanoides tuberculata (Müller, 1774) (Gastropoda, Thiaridae) in a semiarid region, Northeastern Brazil

Abstract

Melanoides tuberculata has invaded several aquatic ecosystems in the Neotropical region. This species shows high adaptive capacity and plasticity, establishing itself in several basins, promoting negative impacts on environments and native species. Here, we determine the growth parameters and the population structure of this species, in a semi-arid environment, in Northeast Brazil (Pernambuco state). Monthly captures were conducted at three types of substrate: site 1: soft bottom with macrophytes, site 2: soft bottom without macrophytes, and site 3: gravel and rocks. Shells were classified as occupied or empty, and their shell length (SL) and opening width (SW) were measured. The growth parameters of the von Bertalanffy’s model were estimated from the size-length frequency distribution using the ELEFAN I. Also, the maturity was verified, through the size at onset of maturity (SOM - 14.85 mm SL) proposed in the literature. A total of 1,013 individuals were collected, with shells varying from 7 to 39 mm SL and mean density of 84.42 (±3.86) individuals m-2. The substrate with the largest number of mollusks was the site 1. Largest amount of empty shells was detected at site 3. Growth of M. tuberculata indicates rapid increment, with k = 0.56, L∞ = 42 mm and t0 = -0.26 years. The mean estimated age for the species was 0.95 years. According to the SOM, 86% of individuals sampled were considered mature.

Full text

Acta Scientiarum
http://periodicos.uem.br/ojs/acta
ISSN on-line: 1807-863X
Doi: 10.4025/actascibiolsci.v41i1.45720
ZOOLOG
Y
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
Growth parameters of the invasive gastropod Melanoides
tuberculata (Müller, 1774) (Gastropoda, Thiaridae) in a semi-
arid region, Northeastern Brazil
Cicero Diogo Lins de Oliveira1* and Carlos Yure Barbosa de Oliveira2
1Laboratório de Dinâmica de Popu lações Aquáticas, Universidade Federal Rural de Pernamb uco, Rua Dom Manuel de Medeiros, s/n, 52171-900 Recife, Pernambuco,
Brazil. 2Laboratório de Cultivo de Algas, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil. *Author for correspondence. E-mail:
linsdiogoc@gmail.com
ABSTRACT. Melanoides tuberculata has invaded several aquatic ecosystems in the Neotropical region.
This species shows high adaptive capacity and plasticity, establishing itself in several basins, promoting
negative impacts on environments and native species. Here, we determine the growth parameters and the
population structure of this species, in a semi-arid environment, in Northeast Brazil (Pernambuco state).
Monthly captures were conducted at three types of substrate: site 1: soft bottom with macrophytes, site 2:
soft bottom without macrophytes, and site 3: gravel and rocks. Shells were classified as occupied or
empty, and their shell length (SL) and opening width (SW) were measured. The growth parameters of the
von Bertalanffy’s model were estimated from the size-length frequency distribution using the ELEFAN I.
Also, the maturity was verified, through the size at onset of maturity (SOM - 14.85 mm SL) proposed in
the literature. A total of 1,013 individuals were collected, with shells varying from 7 to 39 mm SL and
mean density of 84.42 (± 3.86) individuals m-2. The substrate with the largest number of mollusks was the
site 1. Largest amount of empty shells was detected at site 3. Growth of M. tuberculata indicates rapid
increment, with k = 0.56, L∞ = 42 mm and t0 = -0.26 years. The mean estimated age for the species was 0.95
years. According to the SOM, 86% of individuals sampled were considered mature.
Keywords: invasive mollusk; population structure; growth curve.
Received on December 7, 2018.
Accepted on April 1, 2019.
Introduction
Biological invasions are one of the most serious threats to global biodiversity, second only to the
destruction of habitats, can cause substantial changes to biotic communities and abiotic (Everett, 2000;
Mack, Simberloff, Mark Lonsdale, Evans, Clout, & Bazzaz, 2000; Ricciardi & Simberloff, 2009). In almost all
of the environments colonized by human, there were introductions of invasive organisms, often followed by
total or partial extinction of native species (Rocha, 2003). Due to this threat, the invasion of mollusks has
been studied long ago because of its economic losses (Mead, 1979), their impacts on native fauna (Civeyrel
& Simberloff, 1996) and its role in transmitting parasites to humans (Malek, 1980). In particular, South
America is severely affected by the invasion of limnic mollusks, such as: Corbicula fluminea (Müller, 1774)
(Cyrenidae, Bivalvia), Limnoperna fortunei (Dunker, 1857) (Mytilidae, Bivalvia) and Melanoides tuberculata
(Müller, 1774) (Thiaridae, Gastropoda) (Santos et al., 2012).
Melanoides tuberculata is a native species in Eastern and Northern Africa, Southeast Asia, China and the
Indo-Pacific islands, with a wide distribution in these areas (Santos et al., 2012). In Brazil, it was reported
for the first time in the Santos city (São Paulo state), around 1967, and since then it has spread to all regions
of the country (Vaz, Teles, Correa, & Leite, 1986; Santos, Miyahira, & Lacerda, 2007; Santos et al., 2012).
This parthenogenetic species forms large population aggregates and tolerates high amplitudes of
temperature, salinity, pH, and other parameters (Pointier, 2001; Duggan, 2002; Santos et al., 2007).
The reports indicate that the gastropod M. tuberculata had extensively invaded aquatic ecosystems in the
Neotropical region, because it has a high adaptive and migratory capacity, establishing itself in diverse
substrates, besides indicative of active dispersion (Pointier, Théron, & Borel, 1993; Supian & Ikhwanuddin,

Page 2 of 9 Oliveira and Oliveira
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
2002). Melanoides tuberculata has common characteristics to many invasive species: high growth rate,
capacity of migration and territorial expansion, and can be established on different types of substrates
(Miyahira, Lacerda, & Santos 2009, Santos et al., 2012).
The variation in the growth rate of the individuals can affect the survival and reproduction chances and
has been an important component to be analyzed in population dynamics studies (Paschoal, Andrade, &
Darringran, 2015). Therefore, is fundamental importance to establish patterns of growth for the species, in
order to try to explain the relationship between the growth of individuals and the environment where they
live (Darrigran, Damborenea, & Greco, 2007; Paschoal et al., 2015). In this sense, the growth patterns of M.
tuberculata, as well as its population structure were determined, in a reservoir located in the semi-arid
region, Northeast Brazil.
Material and methods
The collections were carried out between August and November 2016 at the Cachoeira II reservoir,
located in Serra Talhada, Pernambuco state, Brazil (Figure 1). This reservoir is an important source of
drinking water supply and income, for artisanal fishermen, for this region. Although it has 21,031,000 m³ of
water capacity, an extreme drought season has been gradually affected the volume of water of this body
(Oliveira, Oliveira, Almeida, Gálvez, & Dantas, 2019).
Figure 1. The study area of the Cachoeira II reservoir, located in Serra Talhada, Pernambuco state, Brazil.
In each month, three samples, with the aid of a fishing net (0.5 mm) were taken, in different sites with an
area of 1 m² each and depth between 20-30 cm. The site 1 was characterized by the soft bottom substrate
and the macrophytes presence, site 2, the soft bottom substrate without macrophytes, and site 3, the
substrate contained gravel and rock.
To assess the distribution of organisms over the time and collection sites, normality and homoscedasticy
by the Shapiro-Wilk and Barlett tests, respectively, were evaluated. One-way analysis of variance (ANOVA),
followed by the Tukey’s test, was applied using a significance level of 0.05 (Zar, 2009).
Each captured specimen was identified according to Fernandez, Santos, Miyahira, Gonçalves,
Ximenes, and Thiengo (2012) and the shell length (SL) and opening width (SW) were measured with
analog caliper (0.05 mm) (Figure 2). Then, it was then identified whether the shell was empty or
occupied, through presence or absence of operculum and soft mass. The t-student test was performed to
compare the lengths per month to verify if there was a significant difference between months (Zar,

Growth of invasive gastropod Melanoides tuberculata Page 3 of 9
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
2009). In addition, the proportion of empty and full shells sampled by site and collection months was
verified.
Figure 2. General scheme for shell size dimensions used in the morphometric analysis of Melanoides tuberculata. SL - shell length and;
SW - shell opening width.
A linear regression was adjusted, relating SL and SW, in order to evaluate if these two measures grow at
the same proportion. The equation was classified according to the values of the slopes (b), such as: negative
allometric when b < 1, positive allometric when b > 1 and isometric when b = 1 (Gould, 1966).
The growth parameters of the Von Bertalanffy (1938) curve were estimated to complete (Equation 1):
  ∞  1   (1)
at where:
L
t
= length at age t,
L
∞
= asymptotic or theoretical maximum length,
K = growth coefficient, and
t
0
= theoretical age at birth.
The growth coefficient (K) and maximum asymptotic length (L
∞
), was determined by the ELEFAN I
method (Pauly & David, 1981), inserted in the computational package FISAT II (FAO ICLARM Stock
Assessment Tools), which is based on the modal shift of time sequences of length distributions (Gayanilo Jr.,
Sparre, & Pauly, 1997).
For the calculation of the theoretical age parameter at zero length (t
0
), the equation of Pauly (1981) was
used (Equation 2):
log0 0.3922  0.2752  log∞ 1.038  log  (2)
The proportion of mature and immature individuals was carried out, considering the size at the onset of
morphometric maturity (SOM: 13.20 mm) proposed by Work and Mills (2013). It was then tested whether
there was a significant difference between the proportions by chi-square (χ²) method, with significance level
of 5% (Zar, 2009).
Results
A total of 1,013 snails were collected, with shells varying from 7 to 39 mm SL, the mean total density was
84.42 ± 3.86 individuals m
-2
(Table 1). The place with the largest amount of mollusk was the soft bottom
substrate with the macrophytes presence in the four months sampled, followed by the soft bottom
environment. However, there was no difference between sites (p-value = 0.673). Regarding the number of
empty shells, the highest account was for the rocky environment, with average 17.56%, while the lowest
account was for the soft bottom with macrophytes presence with only 2.82%.

Page 4 of 9 Oliveira and Oliveira
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
Table 1. Number of individuals of Melanoides tuberculata collected each month and each type of substrate during the study.
Aug Sep Oct Nov Total Average
(mm)
Density
(ind m²)
Empty shells
N (%)
Site 1 95 89 85 85 354 17.4 ± 8.9 88.5 ± 4.7 10 (2.83%)
Site 2 90 85 81 85 341 19.1 ± 7.3 85.3 ± 3.7 16 (4.69%)
Site 3 85 72 79 82 318 18.4 ± 8.1 79 ± 5.6 56 (17.61%)
Grouped sites 270 246 245 252 1013 18.3 ± 8.6 84.4 ± 5.8 82 (8.10%)
The number of empty shells registered at the three sites showed significant differences in its
composition (F = 38.03 p-value = 0.01), with site 3 showing higher quantity of shells when compared to the
others. The shell length of the mollusks ranged from 7 to 39 mm SL, with a modal peak at the class of 10- 15
mm (> 300 individuals). Small (5-10 mm SL) and large (35-40 mm SL) size snails showed low frequency of
occurrence (Figure 3D). According to the SOM, 66.1% of the sampled individuals were considered mature,
showing a significant difference (p-value = 0.021) between the maturation phases.
Figure 3. Length frequency distribution of Melanoides tuberculata. A: Site 1; B: Site 2; C: Site 3; and D: grouped sites.
The morphometric relationship SW vs. SL showed a high correlation (r² = 0.99), the b value showed a
negative allometry (b < 1) (Figure 4).
Figure 4. Relationship between width opening and length shell of Melanoides tuberculata.

Growth of invasive gastropod Melanoides tuberculata Page 5 of 9
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
The cohort analyses showed six age groups for M. tuberculata in the Cachoeira II reservoir (Figure 5),
these groups were continuous over the months occasioned to the low sampled period.
Figure 5. Cohorts of Melanoides tuberculata verified during the study.
Melanoides tuberculata showed a rapid growth, with k = 0.56, L
∞
= 42 mm e t
0
= -0.26 years (Figure 6). The
highest growth rate was recorded in the first year of life, and the species can reach 21.31 mm. Between the
first and second year, the growth rate is 8.87 mm, while in later years the species tends to grow less than 1
mm per year.
Figure 6. Von Bertalanffy (1938) growth curve for Melanoides tuberculata.
The mean estimated age for M. tuberculata in the present study was 0.95 years, with a minimum age of
0.1 and a maximum of 4.45 years (53.4 months). The maximum theoretical estimated age was 11 years,
assuming that the maximum length that the species could reach is 42 mm.
Discussion
The substrate and aquatic vegetation are important conditioners for distribution and occurrence of
mollusks in different biotopes (Pip, 1987). In the present study, the percentage of empty shells (17.6%) was
significant higher for the substrate composed of gravel and rocks. In relation to the macrophytes presence,
there were no significant differences between the three sites. However, the number of individuals caught in
soft bottom substrate with macrophytes presence was higher during the four months. Abílio et al. (2007)
also observed in water bodies of the Paraíba state (Northeast Brazil). That the potential of M. tuberculata
(and other gastropods) were directly associated with the aquatic macrophytes presence, showing that the
presence of vegetation may also influence the abundance of gastropod.
Melanoides tuberculata showed high density with aggregated distribution at the sampling sites. The
population density registered in the present study, was higher than that reported in 2009 at the same

Page 6 of 9 Oliveira and Oliveira
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
reservoir by Almeida, Nascimento Filho, and Viana (2018). These authors reported the highest average
density of 63 individuals m-2. This increase can be justified by the dominance of the species in the study area
over the years. In addition, other studies also indicated high density of M. tuberculata in Brazil. Suriani,
França and Rocha (2007) reported a maximum density of 5,503 individuals m-2 in the Ibitinga dam in São
Paulo state (Southeast Brazil), and Santos and Eskinazi-Sant'Anna (2010) recorded a sample of 134,381
individuals m-2 in the Piranhas-Assu river basin in Rio Grande do Norte state (northeast Brazil).
In relation to the size class, Santos and Eskinazi-Sant'Anna (2010) also reported data like the present
study, being found most of the individuals with less than 15 mm. However, Murray (1975) reported that in a
lake in Texas (USA), shell lengths of Melanoides tuberculata with 70-80 mm SL, yet, Thompson (1983)
pointed that this species typically reaches 30-36 mm SL. These differences in lengths were directly related
to environmental factors, especially temperature, oxygen, pH, which may limit shell formation, and organic
materials such as diatoms (Madsen, 1992; Souza, Drummond, Silva, Queiroz, Guimarães, & Rocha, 1998;
Oliveira & Viana, 2019). Thus, M. tuberculata can present different lengths depending on where it is.
The SL vs. SW relationship was negative allometric, showing that the length of the shell increases faster
with which shell opening. Other studies also find close values such as Chagas, Barros, and Bezerra (2018)
that verified a negative allometric relation of b = 0.26. This relationship may be linked to the degree of
establishment of the species in the environment, since when well established, it can reduce or even
eliminate other species of the same trophic level (Ricciardi & Simberloff, 2009), thus possessing space and
food without competition and growing more rapidly.
The high growth rate of M. tuberculata registered in the present study, corroborated the potential of
invasive species. Elkarmi and Ismail (2007) also recorded rapid growth for the species in the Arabian
Peninsula, with K = 0.245, L∞ = 28 mm and t0 =0.837. Here, we verified that the highest growth occurs in the
first year, reaching about 21 mm, similar to Supian and Ikhwanuddin (2002) that observed, maximum value
of length of 25 mm in Sabah, Borneo for the first year of life. Due to this highly rapid growth, the species
may have advantages over other mollusks, a striking characteristic observed in invasive species (Santos et
al., 2012). This pattern of growth was also verified in some terrestrial gastropods (for this statement see
Table 2). When compared to other invasive species, growth rates were similar, as C. fluminea (Müller, 1774)
that had K = 0.65, L∞ = 32 mm and t0= 0.5 (Cataldo & Boltovskoy, 1999).
Table 2. Growth parameters of the von Bertalanffy(1938) model for other mollusk species. (N.I. = Not informed).
Species K (years) L∞ (mm) t0 Reference
Biomphalaria straminea 0.21 7.75 0 Ituarte, 1989
Biomphalaria glabrata 0.27 19.9 N. I. Puga, Pointier, Cong, & Lopez,,1991
Simpulopsis ovate 0.36 14.86 0 Gomes, Silva, Gil, & Thomé, 2004
In relation birth size, according to Dudgeon (1986) M. tuberculata born with 2.2-3.4 mm. In opposition,
the present study showed a higher value, being the size at birth of 5.5 mm. According to Ben-Ami and
Hodgson (2005), the differences in size of the newborns were related to the fact that the embryos can
remain inside the reproductive pouch of the females, for three to five months before being released.
Melanoides tuberculata shows rapid growth and early maturation. As the maturation of snails was
anticipated (approximately 0.41 years, 13.20 mm) the species is already able to reproduce at reduced sizes,
being capable of structure itself faster in the environment than native species. Invasive species may, thus,
displace native species, due to the characteristics cited above (Paschoal et al., 2015). The high proportion of
adults in the study area was also observed in other reservoirs of Brazil (Suriani et al., 2007; Santos &
Eskinazi-Sant'Anna, 2010), highlighting the ecological risks that this species can play in environments.
The population of M. tuberculata was well established at the Cachoeira II reservoir, semi-arid
Pernambuco state (Northeast Brazil). This was not a good news, once this invasive species is capable of repel
native species, modify aquatic habitats and alter environment scenario (Santos et al., 2012), such as other
invasive species: C. fluminea (Paschoal et al., 2015) and L. fortunei (Darrigran & Damborenea, 2006;
Darrigran et al, 2007).This result could be related both to the environment aspects, since the species
tolerates different substrates (having more affinity to the soft bottom substrate with the macrophytes
presence), as well as to the biology of the species, characterized by rapid growth, early maturation and
population composed mainly by adults.

Growth of invasive gastropod Melanoides tuberculata Page 7 of 9
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
Conclusion
Therefore, it was observed that Melanoides tuberculata presented fast growth, had preference for
environment soft bottom with macrophytes presence. In addition, it was observed that, during this study,
the population was predominantly adult.
Mitigating measures should be implemented in the study area and surveys should be carried out
continuously to verify the increase (or not) of the M. tuberculata populations and possible decreases or
changes in the benthic community of the analyzed reservoir.
References
Abílio, F. J. P., Melo Ruffo, T. L., Souza, A. H. F. F., Silva Florentino, H., Oliveira Júnior, E. T., Meireles, B. N.,
& Santana, A. C. D. (2007). Benthonic macroinvertebrates as bioindicators of environmental quality from
water bodies of Caatinga. Oecologia Australis, 11(3), 397-409.
Almeida, P. R. D. S., Nascimento Filho, S. L. D., & Viana, G. F. S. (2018). Effects of invasive species snails in
continental aquatic bodies of Pernambucano semiarid. Acta Limnologica Brasiliensia, 30(1), e103. doi:
10.1590/s2179-975x10616
Ben-Ami, F., & Hodgson, A. N. (2005). Ovoviviparity and the structure of the brood pouch in Melanoides
tuberculata (Gastropoda: Prosobranchia: Thiaridae). Journal of Morphology, 263(3), 322-329. doi:
doi.org/10.1002/jmor.10307
Cataldo, D., & Boltovskoy, D. (1998). Population dynamics of Corbicula fluminea (Bivalvia) in the Paraná
river delta (Argentina). Hydrobiologia, 380(1-3), 153-163. doi: 10.1023/A:100342872
Chagas, R. A., Barros, M. R. F., & Bezerra, A. M. (2018). Morfometria da concha do gastrópode invasor
Melanoides tuberculata (Müller, 1774) (Gastropoda, Thiaridae). Acta of Fisheries and Aquatic Resources,
6(1), 10-16. doi: 10.2312/Actafish.2018.6.1.10-16
Civeyrel, L., & Simberloff, D. (1996). A tale of two snails: is the cure worse than the disease? Biodiversity &
Conservation, 5(10), 1231-1252. doi: 10.1007/BF00051574
Darrigran, G., & Damborenea, C. (2006). Bio-invasión del mejillón dorado em el continente americano. La Plata,
AR: Editorial de la Universidad de La Plata.
Darrigran, G., Damborenea, C., & Greco, N. (2007). Freshwater invasive bivalves in man-made
environments: a case study of larvae biology of Limnoperna fortunei in a Hydroelectric Power Plant in
South America. AMBIO: A Journal of the Human Environment, 36(7), 575-579.
Dudgeon, D. (1986). The life cycle, population dynamics and productivity of Melanoides tuberculata (Muller,
1774) (Gastropoda: Prosobranchia: Thiaridae) in Hong Kong. Journal of Zoology, 208(1), 37-53. doi:
10.1111/j.1469-7998.1986.tb04707.x
Duggan, I. C. (2002). First record of a wild population of the tropical snail Melanoides tuberculata in New
Zealand natural waters. New Zealand Journal of Marine and Freshwater Research, 36(4), 85-89. doi:
10.1080/00288330.2002.9517135
Elkarmi, A. Z., & Ismail, N. S. (2007). Growth models and shell morphometrics of two populations of
Melanoides tuberculata (Thiaridae) living in hot springs and freshwater pools. Journal of Limnology, 66(2),
90-96. doi: 10.4081/jlimnol.2007.90
Everett, R. A. (2000). Patterns and pathways of biological invasions. Trends in Ecology & Evolution, 15(5),
177-178. doi: 10.1016/S0169-5347(00)01835-8
Fernandez, M. A., Santos, S. B., Miyahira, I. C., Gonçalves, I. B., Ximenes, R. D. F., & Thiengo, S. C. (2012).
Gastrópodes límnicos invasores: morfologia comparada. In M. C. D. Mansur, C. P. Santos, D. Pereira, I. C.
P. Paz, M. L. L. Zurita, M. T. R. Rodriguez, ... P. E. A. Bergonci (Eds.), Moluscos límnicos invasores no
Brasil: biologia, prevenção e controle (p. 25-50). Porto Alegre: RS: Redes Editora.
Gayanilo Jr., F. C., Sparre, P., & Pauly, D. (1997). The FAO-ICLARM stock assesment tools (FISAT) user's guide
(Vol. 8, FAO Computerized information Series -Fisheries). Rome, IT: FAO.
Gomes, S. R., Silva, R. S. D., Gil, G. M., & Thomé, J. W. (2004). Biological cycle of Simpulopsis ovata
(Gastropoda, Bulimulidae) in São Francisco de Paula, Rio Grande do Sul, Brazil. Iheringia. Série Zoologia,
94(3), 253-259. doi: 10.1590/S0073-47212004000300005

Page 8 of 9 Oliveira and Oliveira
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
Gould, S. J. (1966). Allometry and size in ontogeny and phylogeny. Biological Reviews Cambridge
Philosophical Society, 41(1), 587-638. doi: 10.1111/j.1469-185X.1966.tb01624.x
Ituarte, C. F. (1989). Growth dynamics in a natural population of Biomphalaria straminea (Dunker, 1848)
from Bella Unión, Artigas, Uruguay. Studies on Neotropical Fauna and Environment, 24(1), 35-40. doi:
10.1080/01650528909360773
Mack, R. N., Simberloff, D., Mark Lonsdale, W., Evans, H., Clout, M., & Bazzaz, F. A. (2000). Biotic invasions:
causes, epidemiology, global consequences, and control. Ecological applications, 10(3), 689-710. doi:
10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
Madsen, H. (1992). Food selection by freshwater snails in the Gezira irrigation canals, Sudan. Hydrobiologia,
228(3), 203-217. doi: 10.1007/BF00006587
Malek, E. A. (1980). Snails transmitting parasitic diseases (Vol. 1 & 2). Boca Raton, FL: CRC Press.
Mead, A. R. (1979). Economic malacology with particular reference to Achatina fulica, Volume 2. London,
UK: Academic Press.
Miyahira, I. C., Lacerda, L. E. M., & Santos, S. (2009). Dispersão ativa de Melanoides tuberculatus (Müller,
1774) e sua influência no processo de invasão. Informativo SBMa, 40(167), 3-5.
Murray, H. D. (1975). Melanoides tuberculata (Müller), Las Morras Creek, Bracketville, Texas. Bulletin of the
American Malacological Union, 43(1), 11-19.
Oliveira, C. D. L., & Viana, G. F. S. (2019). Influência dos parâmetros abióticos na abundância de
Biomphalaria straminea (Basommatophora: Planorbidae) em uma lagoa temporária no semiárido de
Pernambuco, Brasil. Oecologia Australis, 23(1), 90-98. doi: 10.4257/oeco.2019.2301.08
Oliveira, C. Y., Oliveira, C. D., Almeida, A. J., Gálvez, A. O., & Dantas, D. M. (2019). Phytoplankton
responses to an extreme drought season: A case study at two reservoirs from a semiarid region,
Northeastern Brazil. Journal of Limnology, 78(1), 1-18. doi: 10.4081/jlimnol.2019.1869
Paschoal, L. R. P., Andrade, D. P., & Darrigran, G. (2015). How the fluctuations of water levels affect
populations of invasive bivalve Corbicula fluminea (Müller, 1774) in a Neotropical reservoir? Brazilian
Journal Biology, 75(1), 135-143. doi: 10.1590/1519-6984.09113
Pauly, D. (1981). The relationships between gill surface area and growth performance in fish: a
generalization of von Bertalanffy’s theory of growth. Meeresforschung, 28(4), 251-282.
Pauly, D., & David, N. (1981). ELEFAN I, a BASIC program for the objective extraction of growth parameters
from length-frequency data. Meeresforschung, 28(4): 205-211.
Pip, E. (1987). Species richness of freshwater gastropod communities in central North America. Journal of
Molluscan Studies, 53(2), 163-170. doi: 10.1093/mollus/53.2.163
Pointier, J. P. (2001). Invading freshwater snails and biological control in Martinique Island, French West
Indies. Memórias do Instituto Oswaldo Cruz, 96(suppl.), 67-74. doi: 10.1590/S0074-02762001000900009
Pointier, J. P., Théron, A., & Borel, G. (1993). Ecology of the introduced snail Melanoides tuberculata
(Gastropoda: Thiaridae) in relation to Biomphalaria glabrata in the marshy forest zone of Guadeloupe,
French West Indies. Journal of Molluscan Studies, 59(4): 421-428. doi: 10.1093/mollus/59.4.421
Puga, G. P., Pointier, J. P., Cong, M. Y., & Lopez, J. R. F. (1991). Comparación del crecimiento de 2 especies
de Pomacea del área antillana, útiles como agente de control de enfermedades tropicales. Revista Cubana
Medicina Tropical, 43(1), 36-38.
Ricciardi, A., & Simberloff, D. (2009). Assisted colonization is not a viable conservation strategy. Trends in
Ecology & Evolution, 24(5), 248-253. doi: 10.1016/j.tree.2008.12.006
Rocha, O. (2003). Águas doces (versão preliminar). Avaliação do estado do conhecimento da diversidade
biológica do Brasil. Brasília, DF: COBIO/MMA–GTB/CNPq– NEPAM/UNICAMP.
Santos, C. M., & Eskinazi-Sant'Anna, E. M. (2010). The introduced snail Melanoides tuberculatus (Muller,
1774) (Mollusca: Thiaridae) in aquatic ecosystems of the Brazilian semiarid northeast (Piranhas-Assu
River basin, State of Rio Grande do Norte). Brazilian Journal of Biology, 70(1), 1-7. doi: 10.1590/S1519-
69842010000100003
Santos, S. B. D., Miyahira, I. C., & Lacerda, L. E. M. D. (2007). First record of Melanoides tuberculatus (Müller,
1774) and Biomphalaria tenagophila (d´ Orbigny, 1835) on Ilha Grande, Rio de Janeiro, Brazil. Biota
Neotropica, 7(3): 361-364. doi: 10.1590/S1676-06032007000300037

Growth of invasive gastropod Melanoides tuberculata Page 9 of 9
Acta Scientiarum. Biological Sciences, v. 41, e45720, 2019
Santos, S. B., Thiengo, S. C., Fernandez, M. A., Miyahira, I. C., Gonçalves, I. B., Ximenes, R. D. F., ... Pereira,
D. (2012). Espécies de moluscos límnicos invasores no Brasil. In M. C. D. Mansur, C. P. Santos, D. Pereira,
I. C. P. Paz, M. L. L. Zurita, M. T. R. Rodriguez, ... P. E. A. Bergonci (Eds.), Moluscos límnicos invasores no
Brasil: biologia, prevenção e controle (p. 25-50). Porto Alegre, RS: Redes Editora.
Souza, C. P., Drummond, S. C., Silva, C. J. E., Queiroz, L. A., Guimarães, C.T., & Rocha, R. S. 1998.
Investigação sobre a transmissão da esquistossomose no complexo turístico da Serra do Cipó, MG.
Informe Epidemiológico do Sus, 6(4), 43-51. doi: 10.5123/S0104-16731998000400005
Supian, Z., & Ikhwanuddin, A. M. (2002). Population dynamics of freshwater molluscs (Gastropod:
Melanoides tuberculata) in crocker range park, Sabah. ASEAN Review of Biodiversity and Environmental
Conservation (ARBEC), 1(1), 1-9.
Suriani, A. L., França, R. S., & Rocha, O. (2007). A malacofauna bentônica das represas do médio rio Tietê
(São Paulo, Brasil) e uma avaliação ecológica das espécies exóticas invasoras, Melanoides tuberculata
(Müller) e Corbicula fluminea (Müller). Revista Brasileira de Zoologia, 24(1), 21-32. doi: 10.1590/S0101-
81752007000100003
Thompson, R. J. (1983). The relationship between food ration and reproductive effort in the green sea
urchin, Strongylocentrotus droebachiensis. Oecologia, 56(1), 50-57. doi: 10.1007/BF00378216
Vaz, J. F., Teles, H. M. S., Correa, M. A., & Leite, S. P. S. (1986). Ocorrência no Brasil de Thiara (Melanoides
tuberculata) Müller, 1974) (Gastropoda, Prosobranchia), primeiro hospedeiro intermediário de Clonorchis
sinensis (Cobbold, 1875) (Trematoda, Plathyhelmintes). Revista Saúde Pública de São Paulo, 20(4), 318-322.
doi: http://dx.doi.org/10.1590/S0034-89101986000400008
Von Bertalanffy, L. (1938). A quantitative theory of organic growth (inquiries on growth laws. II). Human
biology, 10(2): 181-213.
Work, K., & Mills, C. (2013). Rapid population growth countered high mortality in a demographic study of
the invasive snail, Melanoides tuberculata (Müller, 1774), in Florida. Aquatic Invasions, 8(4), 417-425. doi:
10.3391/ai.2013.8.4.05
Zar, J. H. (2009). Biostatistical Analysis (5th Ed.). Englewood Cliffs, NJ: Prentice Hall.