ORIGINAL ARTICLE /ARTÍCULO ORIGINAL
ENVIRONMENTAL INFLUENCE ON THE ABUNDANCE OF TWO POPULATIONS OF
PHYSELLA ACUTA (PULMONATA: PHYSIDAE) FROM CAMAGÜEY (CUBA)
INFLUENCIA AMBIENTAL EN LA ABUNDANCIA DE DOS POBLACIONES DE
PHYSELLA ACUTA (PULMONATA: PHYSIDAE) DE CAMAGÜEY (CUBA)
1 2,3* 4 5,6
Raisa Vázquez-Capote ; Lorenzo Diéguez-Fernández ; Rigoberto Fimia-Duarte & José Iannacone
1Unidad Provincial de Vigilancia y Lucha Antivectorial de Camagüey, Cuba.
2 3
Departamento de Control de Vectores. Unidad Municipal de Higiene y Epidemiología. Camagüey, Cuba.
4Facultad de Tecnología de la Salud “Julio Trigo López”. Universidad de Ciencias Médicas
“Dr. Serafín Ruiz de Zárate Ruiz” de Villa Clara, Cuba.
5Facultad de Ciencias Naturales y Matemática (FCNNM). Universidad Nacional Federico Villarreal (UNFV). El Agustino,
Lima, Perú.
6Facultad de Ciencias Biológicas. Universidad Ricardo Palma (URP). Santiago de Surco, Lima, Perú.
*Correo electrónico: lfdieguez@finlay.cmw.sld.cu
Neotropical Helminthology, 2015, 9(2), jul-dec: 243-252.
ABSTRACT
Keywords: Ecological studies - ecology - environmental factors - freshwater snail - Physidae - seasonal variation.
Physella acuta Draparnaud is a species extremely abundant in places where they appear to carry
out a certain controlling action on other undesirable species of mollusks. The influence of some
abiotic factors on two populations of this species from Camagüey, Cuba was determined by a
canonical correspondence analysis. The samples were taken once a month using a sieve, as well
as, the strata of vegetation in a time unit (15 min) without repositioning the specimen. The
mollusks were classified into 10 classes of shell height. In the Tínima River, only the larger-sized
classes were influenced by weather conditions. In the Canal Palomino, the only classes that
proved sensitive to climatic changes were the larger-size ones. The above consideration indicates
that this widely distributed species perhaps by its capacity of tolerating of great variability of the
chemical quality of water, successfully facing extreme values in the physical and chemical
parameters. This situation undoubtedly has permitted this species to colonize with success very
unstable habitats, similar to those analyzed in the present studies that were carried out in the
eastern region of Cuba.
243
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
INTRODUCTION
244
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015
The family Physidae is very controversial in
reference to the species that compose it (Yong
et al., 1994; Iannacone & Caballero, 2002;
Ibáñez & Alonso, 2003) and for this reason; it
has received some attention in Cuba.
Moreover, the bladder snail Physella acuta
Draparnaud 1805 (synonymy of P. cubensis) is
wrongly considered the Fasciola hepatica
(Linnaeus, 1758) a snail host, as laboratory
investigations have demonstrated that this is
not possible (Morales et al., 1987). This
species is reported as the commonest
freshwater mollusk in Cuba (Aguayo, 1938).
Furthermore, it is present in Bahamas,
Jamaica, Puerto Rico, West Indies, Honduras
and the Florida peninsula, with worldwide
distribution (Burch, 1989; Ibáñez & Alonso,
2003; Semenchenko et al., 2008; Banha et al.,
2014).
Physella acuta is described as colonizing
different habitats with a wide spectrum of
organic matter (Ibáñez & Alonso, 2003). This
species is extremely abundant in places where
they appear to carry out a certain controlling
action on other undesirable species of
mollusks (Perera et al., 1995). P. acuta lives in
all types of freshwater environments,
especially in low current places, and can
survive in polluted water (Ibáñez & Alonso,
2003). This makes it possible to carry out auto-
and demo-ecological studies in natural
conditions to enrich the knowledge existing on
this species.
The aim of this paper is to show the
environmental influence on the abundance of
two populations of P. acuta (Pulmonata:
Physidae) from Camagüey (Cuba) that could
be used as biological control agent.
RESUMEN
Palabras clave: caracoles de agua dulce - ecología - estudios ecológicos - factores ambientales - Physidae - variación estacional.
Physella acuta Draparnaud 1805 es una especie muy abundante en los lugares donde parece
llevar a cabo una determinada acción de control sobre otras especies indeseables de moluscos. Se
determinó mediante un análisis de correspondencia canónica la influencia de algunos factores
abióticos en dos poblaciones de esta especie en Camagüey, Cuba. Las muestras se tomaron una
vez al mes usando un tamiz para remover los estratos y la vegetación por unidad de esfuerzo (15
min) sin reposición. Los moluscos fueron clasificados en 10 clases de altura de la concha. En el
río Tínima, las clases de mayor tamaño fueron influenciadas por las condiciones climáticas, no
así las clases medianas; pero en El Canal Palomino, las únicas clases que resultaron sensibles a
los cambios climáticos fueron las de mayor tamaño. La consideración anterior indica que esta
especie con una amplia distribución tal vez por su capacidad de tolerar de gran variabilidad de la
calidad química del agua, enfrenta con éxito valores extremos en los parámetros físicos y
químicos, esta situación, sin duda, ha permitido a esta especie colonizar con éxito hábitats muy
inestables, similares a los analizados en el presente estudio llevado a cabo en la región oriental de
Cuba.
Vázquez-Capote et al.
Canal Palomino: With approximately 100m of
length, its water is very turbid and receives the
liquid waste from numerous neighboring
houses. The stream speed is approximately
-1
0.60 m·sec and the aquatic vegetation is
represented by Cyperus rotundus L. and
gramineous. The bottom is muddy. The
deepest part has a depth of 30cm.
The samples were taken once a month using a
sieve covering the bottom; as well as, the strata
of vegetation in a time unit (15 min) during the
morning and always by the same person
without repositioning the specimen.
The studies were conducted in two habitats
from the capital of Camagüey province (Fig. 1)
from January 2014 to January 2015 (21°20'N;
78°00'W).
Tínima River: In the studied section, the water
is very clear, the aquatic vegetation is mainly
composed of Eichornia crassipes (Mart.)
Solm., whose individuals cover 10% of the
-1
area. The stream speed was of 4 m·sec . The
deepest part has a depth of 2m.
245
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Physella acuta in Camagüey, Cuba
MATERIAL AND METHODS
1:18000
Figure 1. Map of Cuba showing the Camagüey province and its capital with the same name (*).
The following factors were measured:
temperature (T) in situ, pH, calcium (Ca),
chlorides (Cl), nitrates (NO ), nitrites (NO ),
3 2
total hardness (HAR), magnesium (Mg) and
dissolved oxygen (O ) by spectrophotometer
2
in the chemical laboratory from the Provincial
Center of Hygiene and Epidemiology in
Camagüey, Cuba.
The live mollusks were measured with a
micrometer caliper with a 0.01 mm allowance
to determine the maximum height of the shell.
The mollusks were classified into 10 classes of
shell height: class 1 (<3.9 mm), class 2 (4-4.9
mm), class 3 (5-5.9 mm), class 4 (6-6.9 mm),
class 5 (7-7.9 mm), class 6 (8-8.9 mm), class 7
(9-9.9 mm), class 8 (10-10.9 mm), class 9 (11-
11.9 mm) and class 10 (>12 mm) (Vasileva,
2011).
Specimens of P. acuta were identified
according to Nuñez (2011). Voucher
specimens have been deposited in the
Malacological Collection of the “Provincial
Unit of Surveillance and Antivectorial Fight”
in Camagüey, Cuba.
The ordinating diagram of the canonical
correspondence analysis was performed to
show the relation between the abiotic
influences on the monthly variation of the
abundance of P. acuta in both habitats studied,
considering that in Cuba there are two climatic
seasons: the dry season (November-April) and
the rainy season (May-October) (Samek &
Travieso, 1968).
The abundance of higher classes of P. acuta, as
well as the abiotic factor values in the Tínima
River and Canal Palomino, respectively is
shown in the Table 1 and 2.
246
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Vázquez-Capote et al.
RESULTS
Table 1. Values of abundance of classes of shell height of Physella acuta and the abiotic factors measured in the
Tínima River, during the period studied. The shell height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9 mm), 4 (6-6.9 mm), 5
(7-7.9 mm), 6 (8-8.9 mm), 7 (9-9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics factors: T=
0 -1 -1 -1
temperature ( C), pH= pH, Cl= chlorides (mg·L ), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O = dissolved
2
-1 -1 -1 -1
oxygen (mg·L ), HAR= total hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg·L ). Months:
3 2
JAN1=January 2014 and JAN2= January 2015.
Months
Classes of shell height Abiotics factors
1 2 3 4 5 6 7 8 9 10 TOTAL HAR Cl
pH T O2Ca Mg NO3NO2
JAN1 0 6 6 10 19 17 9 6 1 4 78 356 6 0.12 19.4 7.2 0 42.1 90 30.3
FEB 1 1 1 2 0 3 4 5 6 17 40 261.5 3.7 0.08 21.1 7 0 49.4 52.5 43.2
MAR 26 13 17 13 14 19 21 18 2 2 145 450 2.8 0.02 21.1 6.9 0 72.3 95 51.7
APR 0 1 3 4 5 4 3 2 2 2 26 352 7.2 0.51 24 7.1 0 54 183 52.1
MAY 1 2 0 1 5 4 12 7 3 1 36 274 8.6 0.4 25.5 6.9 0.66 69.1 72 46.9
JUN 0 2 8 22 18 17 7 2 0 0 76 338 2.8 0.14 24.6 7.1 0.25 63.2 91 66.4
JUL 2 2 0 27 32 70 60 20 0 2 215 351 5.5 0 24.1 7 0 40.8 87.5 30.3
AGO 0 0 0 1 2 12 42 51 52 4 164 409 6.65 0.65 24.7 7.3 0.28 60.1 113 53.6
SEP 32 2 22 34 84 54 32 10 1 2 273 266 3.7 1.13 24.7 7.1 0 52.1 97.5 40.1
OCT 2 7 6 16 30 26 23 4 0 0 114 272 4.7 3.35 22.6 6.7 0 58.4 76 57.5
NOV 0 2 1 2 12 6 2 1 0 0 26 407 4.3 0.18 23.4 7.4 0 71.2 112 55
DEC 93 4 2 32 85 82 52 22 7 3 382 303 8.75 0.01 23,6 7.1 0.005 56.1 161.5 48.1
JAN2 0 1 0 0 0 4 8 2 3 4 22 256 4,8 0.01 23.5 6.5 0 57.6 72 26.8
247
The ordinating diagram of the canonical
correspondence analysis performed in the
Tínima River is shown in Fig. 2. For classes 8
and 9, the highest scores were reached by NO
3
and HAR, but not so for class 1, which is not
favored in order of importance by NO , HAR,
3
pH, Ca and T.
The individuals with sizes between 4-4.9 mm
(Class 2) and 7-9.9 mm (class 5, 6 and 7) are
indifferent to the increase of the values
analyzed. However, class 10 is strongly
influenced by O , Mg and NO .
2 2
Table 2. Values of abundance of shell height classes of Physella acuta and the abiotic factors measured in the Canal
Palomino, during the period studied. The shell height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9 mm), 4 (6-6.9 mm), 5 (7-
7.9 mm), 6 (8-8.9 mm), 7 (9-9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics factors: T=
0 -1 -1
temperature ( C), pH= pH, Cl= chlorides (mg·L-1), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O = dissolved
2
-1 -1 -1 -1
oxygen (mg·L ), HAR= total hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg·L ). Months:
3 2
JAN1=January 2014 and JAN2= January 2015.
Months
Classes of shell height Abiotics factors
1 2 3 4 5 6 7 8 9 10 TOTAL HAR Cl pH T O2Ca Mg NO3NO2
JAN1 0 3 0 12 17 0 6 0 2 17 57 103 60 7 21 14,5 40.1 51.4 0 0
FEB 3 25 1 54 80 4 15 11 23 16 232 251 76.5 6.85 21.9 2.1 45.1
57.3
0,05 0
MAR 2 28 1 62 132 205 179 112 115 152
988 230 100 7 21.8 21 52.1
66.3
0.8
0
APR 1 9 1 17 34 23 53 29 18 40 225 220 142 7 23.7 12.7 61 42.9
0.33 0
MAY 28 94 8 102 70 0 7 1 1 28 339 360 107 6.9 24.2 4.3 48.1
64.4
0.05 0
JUN 8 82 6 135 133 4 56 38 13 79 554 275 150 7.2 24.7 8 55.9
55.6
0.28 0.01
JUL 9 38 15 109 138 22 56 30 109 58 584 260 105 7 24.8 7.7 56.1
60 0 0.15
AGO 10 24 2 89 57 65 6 24 35 28 340 230 66.7 7.2 25.1 3.3 51.8
52.8
0 0.1
SEP 13 4 0 34 52 0 4 0 1 34 142 282 75 7.4 25.2 6.8 56.8
59.2
0.06 0.25
OCT 2 11 0 85 28 48 14 17 18 29 252 290 85 7.1 23.8 6.9 50.4
85.4
0 0
NOV 1 6 0 43 64 1 4 3 3 33 158 303 60 7.3 23.7 4.9 38.4
49.7
0 0
DEC 0 6 0 40 55 12 4 9 6 27 159 250 87.5 6.9 25.9 14.9 49.7
25.6
0.08 1.9
JAN2 0 7 0 32 37 28 8 16 6 39 173 260 82 6.8 24.1 4.4 59.2 26.8 0.01 0
Figure 2. Ordination diagram of the canonical correspondence analysis performed in the Tínima River with the 10
classes shell height of Physella acuta (o) and abiotic factors (—). The shell height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9
mm), 4 (6-6.9 mm), 5 (7-7.9 mm), 6 (8-8.9 mm), 7 (9-9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics
° -1 -1 -1
factors: T= temperature ( C), pH= pH, Cl= chlorides (mg·L ), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O =
2
-1 -1 -1 -1
dissolved oxygen (mg·L ), HAR= total hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg·L ).
3 2
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Physella acuta in Camagüey, Cuba
The abiotic influence on the abundance of the
10 classes of higher shells of P. acuta in the
Canal Palomino can be observed in Fig. 3,
where the variables Mg, NO , pH and T
3
influenced negatively on the smaller classes
(classes 1,2 and 3), while T favored the
presence of classes 6 and 7, principally the last
one. In the second quadrant is observed the
favorable influence of O and NO on the
2 2
intermediate classes and inverse on those of
HAR in higher values and the Cl in the lower
values. The first factor is strongly associated
with the presence of classes 8 and 9 in a lower
degree with classes 7 and 10. Ca exhibits a
positive relation with classes smaller than of
6.9 mm, because in proportion with the
increase of this ion, the presence of the number
of individuals of these classes also increases.
248
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Vázquez-Capote et al.
In the Figure 4 we can see the ordination of
canonical analysis performed to show the
temporal dispersion in the Tínima River. The
highest abundance of smaller mollusks was at
the end of the dry season (March and April)
while the intermediate classes were
represented indistinctly during all the year
studied. Nevertheless, the highest quantity of
individuals with larger size was strongly
associated with the end of the dry season
(February) and the start of the rainy season
(May).
Figure 3. Ordination diagram of the canonical correspondence analysis performed in the Canal
Palomino with the 10 classes shell height of Physella acuta (o) and abiotic factors (—). The shell
height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9 mm), 4 (6-6.9 mm), 5 (7-7.9 mm), 6 (8-8.9 mm), 7 (9-
0
9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics factors: T= temperature ( C),
- 1 - 1
pH= pH, Cl= chlorides (mg·L-1), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O = dissolved
2
-1 -1 -1 -1
oxygen (mg·L ), HAR= total hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg·L ).
3 2
249
The situation in the Canal Palomino is
presented in Fig.5. The individuals smaller
than 9.9 mm. of shell height were represented
all the year round, but the classes 8 and 9 had
preference for the rainy months. The mollusks
with sizes higher than 12 mm presented a
strong positive association with the months at
the end of the dry season.
Figure 4. Ordination diagram of the canonical correspondence analysis performed in the Tínima
River showing the temporal dispersion of 10 classes of shell height of Physella acuta. The shell
height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9 mm), 4 (6-6.9 mm), 5 (7-7.9 mm), 6 (8-8.9 mm), 7 (9-
0
9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics factors: T= temperature ( C),
- 1 - 1 - 1
pH= pH, Cl= chlorides (mg·L ), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O = dissolved
2
- 1 - 1 - 1 - 1
oxygen (mg·L ), HAR= total hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg·L ).
3 2
Months: JAN1=January 2014 and JAN2= January 2015.
Figure 5. Ordination diagram of the canonical correspondence analysis performed in the Canal Palomino showing the temporal
dispersion of 10 classes of shell height of Physella acuta. The shell height: 1 (<3.9 mm), 2 (4-4.9 mm), 3 (5-5.9 mm), 4 (6-6.9 mm),
0
5 (7-7.9 mm), 6 (8-8.9 mm), 7 (9-9.9 mm), 8 (10-10.9 mm), 9 (11-11.9 mm) y 12 (>12 mm). Abiotics factors: T= temperature ( C),
-1 -1 -1
pH= pH, Cl= chlorides (mg·L-1), Ca= calcium (mg·L ), Mg= magnesium (mg·L ), O = dissolved oxygen (mg·L ), HAR= total
2
-1 -1
hardness (mg·L ), NO = nitrate (mg·L ) y NO = nitrite (mg/l). Months: JAN1=January 2014 and JAN2= January 2015.
3 2
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Physella acuta in Camagüey, Cuba
250
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Vázquez-Capote et al.
to the distribution, reproduction and growth of
mollusks in general (Appleton, 1976; Sturrock
& Sturrock, 1972; Perera & Yong, 1991;
Iannacone et al., 2003; Semenchenko et al.,
2008 & Pino et al., 2010). Although the higher
intermediate classes did not receive a strong
abiotic influence, we can explain this because
according to Margalef (1977) these classes
have the capacity to tolerate extremely adverse
environmental conditions.
The largest classes were strongly influenced by
T, pH, NO , Mg and Ca. Boycott (1934),
2
Hubendick (1958), Diéguez et al. (1992) and
Okland (1983) said that the Ca ion has a
positive influence on mollusks, because it
favors the shell formation.
The analysis of the spatial and seasonal
variations of the malacological communities
has shown the importance of environmental
factors. In Cuba some investigations have
indicated that there are two climatic seasons,
but malacological populations depend mainly
on the dry periods, which can be extremely
variable in frequency and duration (Perera,
1996; Vasileva, 2011).
In the population studies, in the Canal
Palomino the seasonal influence was
practically null except on the highest classes,
but in the Tínima River the smaller and the
larger mollusks received climatic influence
(Vasileva, 2011).
The above consideration indicates that P. acuta
is a species with a wide distribution perhaps by
its tolerance capacity of great variability of the
chemical quality of water, successfully facing
extreme values in the physical and chemical
parameters (Semenchenko et al., 2008;
Vasileva, 2011; Banha et al., 2014), this
situation undoubtedly has permitted this specie
to colonize with success very unstable habitats,
similar to those analyzed in the present studies
carried out in the central region of Cuba.
In Cuba there are studies carried out about the
environmental influence in the presence and
distribution of freshwater mollusks (Perera &
Yong, 1984; Yong et al., 1987; Diéguez et al.,
1992, 1997; Gómez, 1995; Fimia-Duarte et al.,
2014a, b). In some cases we can observe the
favorable or limiting influence of some
species. Other authors have indicated that the
quality of water exerts a marked influence, due
to the sensitivity of some species to the
changes that occur in numerous aquatic
ecosystems (Vasileva, 2011).
According to Yong et al. (1987) and Diéguez et
al. (1992) in studies performed on Tarebia
granifera (Lamarck, 1822), more population
density has been found in aquatoriums without
running water in comparison to those that have
it, because it produces a drag of nutriment and
therefore the availability of food is smaller. In
the Tínima River (1597 individuals) the water
stream was stronger than in Canal Palomino
(4203 individuals); moreover this last habitat
received the liquid wastes from numerous
neighboring houses, therefore this canal has
better conditions for the reproduction and
development of P. acuta in comparison with
the Tínima River, due to a greater presence of
organic material in decomposition.
Some authors have demonstrated that this
species colonizes contaminated water bodies
with notable success (Pino & Morales, 1982;
Ferrer et al., 1985, 1989; Perera & Yong, 1991;
Fernández, 1994; Diéguez et al., 1997;
Semenchenko et al., 2008), an aspect which
corroborates the present study.
The abiotic factors can favor, limit or exclude
some species of mollusks, in our case the
undesirable influence of pH and T in both
habitats was proved mainly with the smaller
individuals. These results coincide with other
authors since these variables are greatly related
DISCUSSION
Ferrer, JR, Perera, G & Yong, M. 1985.
Estudios de los moluscos fluviatiles de
una localidad afectada por un brote de
Fascioliasis. Revista Cubana de
Medicina Tropical, vol. 37, pp. 155-160.
Ferrer, JR, Perera, G, Yong, M & Amador, O.
1989. Estudios de la densidad de
ho sp ed er os i nt er me di ar io s d e
enfermedades tropicales en las berreras.
Revista Cubana de Medicina Tropical,
vol. 41, pp. 341-354.
Fimia-Duarte, R, Iannacone, J, Argota-Pérez,
G, Cruz-Camacho, L, Diéguez-
Fernández, L, López-Gómez, EJ &
Á l v a r e z - Va l d é s , R . 2 0 1 4 a .
Epidemiological and zoonotic risk of the
malacofauna fluvial and terrestrial in
Capitan Roberto Flieites Healthy Area,
Cuba. Neotropical Helminthology, vol.
8, pp. 313-323.
Fimia-Duarte, R, Iannacone, J, Roche-
Fernández, D, Cruz-Camacho, L &
L ó p e z - G r i m a r d i t , E . 2 0 1 4 b .
Epidemiological risk and zoonotic
diseases in Urban communities from the
Municipality of Santa Clara, Cuba. The
Biologist (Lima), vol. 12, pp. 225-239.
Gómez, M. 1995. Influencia de los factores
abióticos en la distribución, diversidad y
abundancia de moluscos dulceacuícolas
en diferentes cuerpos de agua de la
provincia de Camagüey. Tesis para optar
por el grado de maestro en Entomología
Médica y Control de Vectores. Instituto
de Medicina Tropical “Pedro Kourí” La
Habana, 65 pp.
Hubendick, B. 1958. Factors conditioning the
habitat of freshwater snails. Bulletin
WHO, vol. 18, pp. 1072-1080.
Iannacone, J & Caballero, C. 2002. Empleo del
caracol de agua dulce Physa venustula
G o u l d c o m o h e r r a m i e n t a
ecotoxicológica para la evaluación de
riesgos ambientales por plaguicidas.
Agricultura Técnica, vol. 62, pp. 212-
225.
Iannacone, J, Mansilla, J & Ventura, K. 2003.
251
Aguayo, CG. 1938. Los moluscos fluviatiles
cubanos. Parte II. Memorias Sociedad
Cubana de Historia Natural, vol. 12, pp.
203-242.
Appleton, CC. 1976. Observation on the
thermal regime of a stream in the
Eastern Transvaal with reference to
certain aquatic pulmonata. South
African Journal of Science, vol. 72, pp.
20-23.
Banha, F, Monica Marques, M & Anastácio,
PM. 2014. Dispersal of two freshwater
i n v a s i v e m a c ro i n v e r t e b r a t e s ,
Procambarus clarkii and Physella acuta,
b y o f f -ro a d v e h i cl e s. Aquatic
Conservation: Marine and Freshwater
Ecosystems, vol. 24, pp. 582-591.
Boycott, AE. 1934. The habitat of land
mollusca in Britain. Journal Ecologycal,
vol. 12, pp. 1-38.
Burch, JB. 1989. North American Freshwater
Snails. Malacological Publications,
Hamburg, Michigan, USA, 65 p.
Diéguez, L, Escalante, A, Martínez, A &
Verdecia, M. 1992. Estudio preliminar
de la variación de Tarebia granifera
(Lamarck), Río Hatibonico, Camagüey.
Revista Cubana de Medicina Tropical,
vol. 44, pp. 66-70.
Diéguez, L, Hernández, R, Perera, G,
Vázquez, R & Escalante, A. 1997.
Presencia de Corbicula fluminea
(Müller, 1774) y estudios estacionales
sobre su abundancia en el lago artificial
L a J í a d e C a m a g ü e y, C u b a .
Malacological Reviews, vol. 30, pp. 93-
100.
Fernández, JA. 1994. Ecología de los
moluscos fluviátiles de importancia
médica de la Región Central de Cuba.
Tesis para optar por el grado de maestro
en Entomología Médica y Control de
Vectores. Instituto de Medicina Tropical
“Pedro Kourí” La Habana. 44 p.
BIBLIOGRAPHIC REFERENCES
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Physella acuta in Camagüey, Cuba
252
Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Vázquez-Capote et al.
Macroinvertebrados en las lagunas de
Puerto Viejo, Lima-Perú. Ecología
aplicada, vol. 2, pp. 116-124.
Ibáñez, M & Alonso, MR 2003. Physella
(Costatella) acuta (Draparnaud, 1805) in
the Canary Islands (Pulmonata
Basommatophora: Planorboidea:
Physidae). Vieraea, vol. 31, pp. 133-144.
Margalef, R. 1997. Ecología. Ed. Omega.
Barcelona. España. 951 p.
Morales, G, Pino, L & Angulo, N. 1987.
Resistencia de Physa cubensis a la
infección con Fasciola hepatica. Revista
de la Facultad de Ciencia Veterinarias de
Venezuela, vol. 34, pp. 43-55.
Núñez, V. 2011. Revisión de dos especies de
Physidae. Revista Mexicana de
Biodiversidad, vol. 82, pp. 93-108.
Okland, J. 1983. Factors regulating the
distribution of freshwater snails
(Gastropoda) in Norway. Malacologia,
vol. 24, pp. 277-288.
Pino, AL & Morales, AG. 1982. Habitat de
Lymnaea cubensis (Pfeiffer, 1839),
hospedero intermediario detectado en el
Estado de Trujillo, Venezuela. Acta
Científica Venezolana, vol. 33, pp. 61-
65.
Pino, J, López, F & Iannacone, J. 2010.
Impacto ambiental en la proporción de
especímenes machos en poblaciones
partenogenéticas de Melanoides
t u b e r c u l a t a ( M u l l e r 1 7 7 4 )
(Prosobranchia: Thiaridae) en el Perú.
The Biologist (Lima), vol. 8, pp. 139-
149.
Perera, G. 1996. L'Ecole Practique des hautes
etudes sciences de la Vie et de la Terre.
Thesé présentée dans le laboratoire de
Biologie Marine et Malacologie. Centre
de Biologie et d'Ecologie Tropicale et
Méditerranéenne. Ecole Practique des
Hautes Etudes, Université de Perpignan.
105 p.
Perera, G & Yong, M. 1984. The influence of
some abiotic factors on the distribution
of freshwater mollusks on the Isle of
Young (Isle of Pines), Cuba. Walkerana,
vol. 2, pp. 131-139.
Perera, G, Yong, M. 1991. Seasonal studies on
Pomacea paludosa in Cuba. Walkerana,
vol. 5, pp. 19-23.
Perera, G, Yong, M, Ferrer, JR, Gutiérrez, A &
Sánchez, A. 1995. Ecological structure
and factors regulating the population
d y na m ic s o f f res h w a t e r s n ai l
populations in hanabanilla lake, Cuba.
Malacological Review, vol. 28:63-69.
Samek, E & Travieso, A. 1968. Climas y
regiones de Cuba. Revista de la
Agricultura Cubana, vol. 3:1.
Semenchenko, V, Laenko, T & Razlutskij, V.
2008. A new record of the North
American gastropod Physella acuta
(Draparnaud, 1805) from the Neman
River Basin, Belarus. Aquatic Invasions,
vol. 3, pp. 359-360.
Sturrock, RF & Sturrock, BM. 1972. The
influence of temperature on the biology
of Biomphalaria glabrata (Say),
intermediate host of Schistosoma
mansoni in St. Lucia, West Indies. Annals
of Tropical Medicine and Parasitology,
vol. 66, pp. 385-390.
Vasileva, SY. 2011. Shell size of the freshwater
snail Physella acuta (Draparnaud,
1805) collected from water vegetation: A
case study from South-East Bulgaria.
Ecologia Balkanica, vol. 3, pp. 61-64.
Yong, M, Ferrer, JR & Perera, G. 1994.
Anatomía y morfología de Physa
cubensis Pfeiffer, 1839 (Pulmonata:
Physidae) en Cuba. Revista Cubana de
Medicina Tropical, vol. 46, pp. 158-163.
Yong, M, Sánchez, R, Perera, G, Ferrer, JR &
Amador, O. 1987. Seasonal studies of
two populations of Tarebia granifera
(Lamarck). Walkerana, vol. 2, pp. 158-
163.
Received May 28, 2015.
Accepted August 5, 2015.
