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Biology and individual growth of Milax gagates

(Draparnaud, 1801) (Pulmonata: Stylommatophora)
a a a
NATALIA LILIANA CLEMENTE , ARIEL JESÚS FABERI , CARLA SALVIO & ALICIA NOEMÍ
a
LÓPEZ
a
Facultad de Ciencias Agrarias , Universidad Nacional de Mar del Plata, Estación
Experimental del Instituto Nacional de Tecnología Agropecuaria (INTA) , Cc 276, 7620,
Balcarce, Buenos Aires, Argentina E-mail:
Published online: 01 Dec 2010.

To cite this article: NATALIA LILIANA CLEMENTE , ARIEL JESÚS FABERI , CARLA SALVIO & ALICIA NOEMÍ LÓPEZ (2010) Biology
and individual growth of Milax gagates (Draparnaud, 1801) (Pulmonata: Stylommatophora), Invertebrate Reproduction &
Development, 54:3, 163-168, DOI: 10.1080/07924259.2010.9652328

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 Invertebrate Reproduction and Development, 54:3 (2010) 163–168 163
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0168-8170/10/$05.00 © 2010 Balaban

Biology and individual growth of Milax gagates (Draparnaud,

1801) (Pulmonata: Stylommatophora)

NATALIA LILIANA CLEMENTE *, ARIEL JESÚS FABERI, CARLA SALVIO and

ALICIA NOEMÍ LÓPEZ
Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Estación Experimental del Instituto Nacional de
Downloaded by [University of Georgia] at 18:56 17 December 2014

Tecnología Agropecuaria (INTA), Cc 276, 7620 Balcarce, Buenos Aires, Argentina

email: nataliaclemente@hotmail.com

Received 14 April 2010; Accepted 16 July 2010

Abstract
In the southeast of Buenos Aires Province, Argentina, Milax gagates (Draparnaud, 1801) causes
reductions in yields of soybean, sunflower and oilseed rape under no tillage by damaging seeds and
seedlings. Whilst there are some studies of the damage caused by M. gagates to sunflower and
soybean crops, and the control of slugs in soybean, there is little information on the biology and
ecology of this species of slug. The aim of the present study was to analyze the biology and
individual body growth of M. gagates. The study was carried out at 20ºC and a 16/8 h light/dark
regime. The egg stage took about 23 days (SD = 2.7 days) and viability was 75.4%. The slugs
reached maximum fecundity between the 19th to 29th week with values of 4 and 9 eggs/slug/week,
respectively. The net reproductive rate varied considerably among cohorts, 7.2 to 33.2, but the
generation time was similar, 181 to 206 days. The growth pattern was well described by the three
parameter logistic model. The slugs reach half of their maximum weight at about 150 days old
(inflection point of the growth curve), 22 to 43 days before the start of oviposition. The maximum
mean body weight of the adult slugs was 2149.6 mg, but in the population maximum body weight
varied between 991.2 mg to 3308.0 mg (±2×579.2 mg) among slugs. The biological parameters and
individual growth of M. gagates from Argentina were consistent with that of an annual reproductive
cycle of a semelparous species.

Key words: “Keeled slug”, Mollusca, Gastropoda, life cycle, reproduction, growth

Introduction
other parts of the world, for example New Zealand,
In Argentina, slugs are represented by the families Australia and North and South America (South, 1992).
Veronicellidae, Succineidae, Milacidae and Limacidae The “keeled slug”, Milax gagates, is associated with
(Manetti et al., 2005). Within the Milacidae, species of man-made environments such as gardens and agricultural
Milax and Tandonia occur mainly in the Mediterranean land. This species may attain a length of 60 mm, is gray
region through to the Balkan peninsula and in Western or black, has an oval groove on the center of the mantle,
Europe, although they have also been introduced into and a prominent keel running from the posterior border

*
Corresponding author.
 164 N.L. Clemente et al. / IRD 54 (2010) 163–168

of the mantle to the end of the body. This keel is individually in plastic boxes (9.5 cm diameter × 6.4 cm
especially conspicuous when the body is contracted high) and reared under the same conditions as the adults.
(South, 1992). Boxes were cleaned, and food changed, weekly. Slugs
Milax gagates, as well as slugs of the family were weighed at one month intervals on an electronic
Limacidae, Deroceras reticulatum and D. leave, are balance accurate to 0.001 g.
important macrofaunal organism of the no tillage crops in For the reproductive study, 38 hatched juveniles (five
the southeast of Buenos Aires Province, Argentina. cohorts, i.e., slugs born on the same day) were selected
These slugs cause reductions in yield by killing seeds and randomly and placed individually in plastic boxes. Slugs
seedlings, and by grazing on the young shoots of were examined weekly to determine the presense of eggs.
soybean, sunflower and oilseed rape (Aragón, 2003; At the same time food and soil were changed. The life
Clemente et al., 2007; Larsen et al., 2007). Increases in history parameters determined were time till hatching
area of crops under no tillage would result in more (days), viability (% of eggs hatched), time from hatching
favorable agricultural land for slugs and potentially more to oviposition (weeks; i.e. the period between hatching
crop damage and yield losses. and the production of the first egg clutch), fecundity
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Although there have been some studies on the (number of eggs/slug), number of eggs per clutch and
damage caused by different sized M. gagates to sun- longevity (weeks). Data were recorded until slugs died.
flowers (Tambascio, 2007), and a recent description of Survival and fecundity curves were constructed. The
its damage and control in soybean (Salvio et al., 2008a), survival rate (lx) is the percentage of slugs living at time
biological and ecological information of the species is x from the initial number of slugs at x0. The age-specific
scarce. The aim of this study was to examine the biology fecundity (mx) is the number of eggs produced per slug at
and individual body growth of M. gagates in order to week x. The net reproduction rate (R0), which is the rate
provide some basic parameters of population dynamics, of multiplication in one generation, and the generation
which will be required for evaluation and future time (T), which is the time required for the population to
successful management of this pest in no tillage crops. increase R0 times were estimated (Birch, 1948).
Body weight was fitted with a logistic curve with
three-parameters: Y = A/{1 + e[(B!x)/C]} where Y = weight
Materials and Methods
(mg) at time x (days); A = the asymptotic weight at adult
To start the study and to ensure egg production, age; B = the x value at the inflection point of the curve,
40 specimens of M. gagates were collected on October 5, the time at which the slugs reaches half of this
2007, from a pasture located at the Experimental Station asymptotic weight; C = a numeric scale parameter
of the National Institute of Agricultural Technology (Pinheiro & Bates, 2000). Growth parameters were esti-
(INTA) in Balcarce, Buenos Aires Province (37º45NS, mated with the nlme procedure of R 2.9.1 (R Develop-
58º18N W), Argentina. Taxonomic identification was ment Core Team, 2009). The nlme procedure fits non-
accomplished using Grossu (1983) and Rodriguez & linear mixed models, that is, models in which both fixed
Hermida (1993). The adult slugs were placed on moist and random effects (cohort and slug) are permitted to
soil in plastic boxes (23 cm × 23 cm × 12 cm high) with have a nonlinear relationship to the response variable.
holes made in the lid to allow air circulation whilst
ensuring a moist atmosphere. The slugs were fed with
Results
dry rabbit food. The rearing boxes, each containing
10 slugs, were placed in controlled temperature chambers The eggs of Milax gagates were sub-spherical or
at 20ºC. The light/dark regime during the experiment was ellipsoidal with a maximum diameter of 3.5 mm. They
16/8 h. were normally laid in clutches of 13–18 eggs. The egg
On October 12, slugs were placed individually in stage took about 23 days (SD = 2.7 days), after which
plastic boxes (9.5 cm diameter × 6.4 cm high) and main- 156 slugs were obtained; viability was 75.4%. The first
tained at 20ºC for egg production. Eggs from each clutch laid eggs of slugs were at 169 to 193 days (5.5 to
were counted, and then each clutch was placed on damp 6.5 months) (Table 1) and the maximum total fecundity
filter paper in a box (9.5 cm diameter × 6.4 cm high) and was 146 eggs/slug. The oviposition period extended until
incubated at 20ºC. A total of 207 eggs were collected for 273 days, after which slugs did not lay eggs. Longevity
the determination of the time till hatching and egg was approximately one year and varied between 287 and
viability. 330 days.
To study slug growth, 139 hatched juveniles (five The slugs reached maximum fecundity between the
cohorts, i.e., slugs born on the same day) were placed 19th to 29th week among cohorts, and the values were
 N.L. Clemente et al. / IRD 54 (2010) 163–168 165

Table 1. Mean ± standard deviation of life history parameters of Milax gagates in five different cohorts

Cohort n Time from hatching to Fecundity Number of eggs Longevity R0 T

oviposition (days) (eggs/slug) per clutch (days) (days)

1 13 172 ±38 20 ±35 13 ±7 330 ±19 19.8 181

2 6 181 ±29 36 ±55 14 ±6 330 ±63 33.2 206
3 5 169 ±27 21 ±16 18 ±5 287 ±15 21.0 177
4 6 193 ±18 11 ±13 17 ±10 327 ±32 7.2 206
5 8 193 ±4 11 ±9 12 ±8 329 ±38 7.2 203

between 4 to 9 eggs/slug/week respectively (Fig. 1). The Table 2. Estimated parameters for the logistic growth curve
age-specific survival was similar to the convex Type I of Milax gagates and asymptotic standard error
curve and reached 50% (lx = 0.50) at 280 – 329 days for Parameter Estimated SE
different cohorts (Fig. 1). The net reproductive rate (R0)
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varied considerably among cohorts, from 7.2 to 33.2, but A (mg) 2149.6412 55.76228
the generation time (T) was similar, 181 to 206 days. B (days) 147.2901 0.97352
C 28.945 0.77997
The individual weight data (Fig. 2) show a more or
less uniform initial growth of all slugs. However, there
was considerable variation in the asymptotic weight
were relatively rare. This was also found in our study. At
among slugs (random effect), but the same overall
birth the animals are still almost transparent. Focardi &
S-shaped pattern was observed for all slugs. Fig. 2 also
Quattrini (1972) found that the intensely dark pigmen-
shows that differences in asymptotic weight of slugs
tation that distinguished the adults occurs much later and
were not related with the time of their deaths. In this
gradually, after slugs are about 2 months old.
species, body weight increased, reached the maximum
Milax gagates reproduction began at the age of 5–6
value and then decreased or was maintained until
months. Galangau (1964) determined that not all the
mortality.
animals reach gonad maturity at the same time of the year
The growth pattern was well described by the three
and thus each of their reproductive cycles can fall within
parameter logistic model (Table 2). The slugs reached
varying periods of time. According to Duncan (1975, in
half of their maximum weight at approximately 150 age
South, 1992), M. gagates, Limax cinereoniger, Vagi-
days (inflection point), 22 to 43 days before the start
nulus borellianus and Laevicaulis alte self fertilize. Chen
to oviposition. The asymptotic weight of the model
(1994) showed that the fecundity of Deroceras agreste
(Table 2) represents maximum mean weight in the
with self-fertilization was two to four times greater than
population and random effects of the slugs represent the
that of normal reproduction. The growth rate of the
deviations of their mean values among slugs. There was
young slugs was higher and the life span longer than for
no variation in asympotic weight among cohorts (SD =
slugs produced by sexual reproduction. In this study,
0.08 mg) but there was great variation among individuals
total fecundity was low. Clemente et al. (2008) found low
(standard deviation = 579.20 mg). Maximum mean
fecundity of Deroceras reticulatum at the same experi-
weight of adult slugs was 2149.6 mg, but in the popu-
mental conditions, two eggs per slug. In other species
lation maximum body weight varied between 991.2 mg
introduced into Argentina, such as D. leave, the fertility
to 3308.0 mg (± 2 x 579.2 mg) among slugs.
after self-fertilization was high, slugs producing 353 eggs
per slug at 20ºC (Faberi et al., 2006).
According to Focardi & Quattrini (1972), the life
Discussion
cycle of M. gagates finishes with the end of oviposition
The eggs of Milax gagtes were laid in small groups and usually death occurs 15–20 days after laying the last
and were never united by mucous masses or cords as clutch of eggs. However, this period can be reduced to a
found in other gastropods, for example in Veronicellidae couple of days or exceed one month. By contrast, in this
(Lanza & Quattrini, 1964). Focardi & Quattrini (1972) experiment the slugs lived for several weeks after ovi-
observed that a greater mass of eggs was formed by position and longevity was about 1 year. Among the
various albumen layers covered externally by a mucous Milacidae, M. gagates and T. sowerbii, have a life span
capsule. These authors found that hatching occurs about of 12–14 months in New Zealand. Many populations
1 month after oviposition at 18–25ºC and aborted eggs exhibit both autum and spring periods of recruitment but
 166 N.L. Clemente et al. / IRD 54 (2010) 163–168
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Fig. 1. Survival (lx)

and fecundity (mx) of
Milax gagates (a–e)
corresponding cohort
1–5, respectively.
 N.L. Clemente et al. / IRD 54 (2010) 163–168 167
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Fig. 2. Individual growth curves of Milax gagates at 20ºC.

individual slugs contribute to one generation only determined three distinct phases of growth; an initial
(Barker, 1986). phase of rapid growth (infantile phase), followed by a
The growth data showed a generic logistic curve, but slower growth (juvenile phase), and finally a phase with
only studying individuals can produce a valid pattern of little growth during which slugs laid eggs (adult phase).
animal growth. Similar results were demonstrated by In this laboratory study we determined biological
Zotin (2007) in the growth curve of D. reticulatum. In parameters and described several aspects of individual
this study M. gagates exhibited a great variation of growth of M. gagates from Argentina that were consis-
maximum weight among slugs. In D. reticulatum there is tent with an annual reproductive cycle and semelparity.
considerable variation in the body weight of slugs with This information of M. gagates biology and the
hermaphrodite glands in the spermatozoon and oocyte knowledge of biological, cultural and chemical control of
stages (Barker, 1991). The gland increased rapidly in size slugs (Salvio et al., 2008b; Tulli et al., 2009) should
to reach maximum weight with sexual maturation of the enable integrated slug management in agricultural crops.
animal (Gomez, 2001). However, Hommay et al. (2001)
observed that weight variation of Limax valentianus
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