DISTRIBUTION OF ARION HORTENSIS S.S. AND
ARION DISTINCTUS IN NORTHERN SWITZERLAND
J. IGLESIAS1 AND B. SPEISER2
1
Department of Animal Biology, Faculty of Biology, University of Santiago de Compostela, 15706 Santiago de Compostela, Spain.
E-mail: [email protected].
2
FiBL, Research Institute of Organic Agriculture, Ackerstrasse, CH-5070 Frick, Switzerland.
(Received 4 July 2000; accepted 19 September 2000)
ABSTRACT
The distribution of the sibling slug species Arion hortensis s.s. and Arion distinctus in Northern Switzerland is described. In the sampled area, both species were almost equally abundant and their distributions overlapped. Most of the sampled sites contained both species. Arion hortensis s.s. is more common
in Switzerland than previously known, and its range extends more towards the east of Switzerland.
Arion hortensis s.s. was more abundant in gardens than in the other habitats sampled. At sites where
only A. distinctus occurred, the form with a bipartite oviduct prevailed. At sites where both species were
present, the form of A. distinctus with a tripartite oviduct was more common than the form with a bipartite oviduct. In captivity, one specimen of A. distinctus mated with one A. hortensis s.s., as indicated by a
spermatophore of A. distinctus that was found within the atrium of one A. hortensis s.s. A majority of
the specimens could by assigned to the correct species by their colouration, but a safe distinction
between A. hortensis s.s. and A. distinctus is only possible using characters of the reproductive system.
INTRODUCTION
Species of the Arion hortensis aggregate are among the
most important slug pests of field crops in the UK (Port
& Port, 1986), France (Chabert, Guinot & Tisseur,
1997), and elsewhere in continental Europe (Godan,
1979; South, 1992). Arion hortensis Férussac, 1819 and
Arion distinctus Mabille, 1868 are sibling species which
were considered as a species complex under the denomination Arion hortensis s.l. for a long time. Davies
(1977, 1979) divided the complex into three species: A.
hortensis s.s., A. distinctus and Arion owenii Davies,
1979. As they have only recently been distinguished and
as they can only be identified reliably based on internal
anatomy (Kerney, Cameron & Jungbluth, 1983; Backeljau & Van Beeck, 1986), the distribution of the individual species is not well known. Arion owenii has been
recorded on the British Isles only (South, 1992), but the
distribution of A. hortensis s.s. and A. distinctus is much
less well known. De Winter (1984) described A. distinctus
as common all over Western and Central Europe
(including Germany and Poland), and A. hortensis s.s.
as a more Atlantic species. In the Mollusca Atlas of
Switzerland and Liechtenstein (Turner, Kuiper, Thew,
Bernasconi, Rüetschi, Wüthrich & Gosteli, 1998), a
single record of A. hortensis s.s. in Switzerland is given,
in the extreme west of the country, while A. distinctus
occurs throughout Switzerland (records from 100
sites).
Corresponding author: J. Iglesias
J. Moll. Stud. (2001), 67, 209–214
In the literature, several characteristics for distinguishing A. hortensis s.s. from A. distinctus are described, but
some characters are known to be less reliable than
others. Therefore, we studied the correlation between
genital features and the colour and banding pattern.
MATERIAL AND METHODS
Sampling and processing of animals
Slugs were collected by sight or attracted with traps baited
with cucumber slices. Lowland habitats in Northern Switzerland and a few sites in Germany close to the Swiss border
were sampled. Samples of 10 or more animals that were large
enough to be identified were included in the study. Collection
sites, together with their UTM coordinates, habitat type and
sampling method, are given in Table 1. Collections were
made in March and April 2000. The habitats sampled included
gardens, wildflower strips, field margins, grassland, strawberry
and vegetable fields. In the laboratory, the animals were
drowned in water for 24 h and then transferred to 70% ethanol,
in which they were kept for at least 24 h prior to dissection.
Slugs were dissected according to the method described by
De Wilde (1983) and observed under a stereomicroscope. For
every animal, the following characters were noted: (i) whether
the right mantle band ran over or through the pneumostome;
(ii) whether the oviduct was composed of two or three parts
[types A and B of A. distinctus respectively, according to the
terminology used by De Winter (1984)]; (iii) the presence or
absence of a ligula-like structure inside the oviduct; and (iv)
the morphology of the structure associated with the outlet
of the epiphallus in the atrium. This last character was the
© The Malacological Society of London 2001
J. IGLESIAS & B. SPEISER
criterion used to determine the specific allocation of the animals, since it is the only one by which the species can be safely
distinguished (Backeljau & Van Beeck, 1986). In a subsample
of 100 specimens of A. hortensis s.s. and 90 A. distinctus, the
overall colour was noted before killing the animals. When a
spermatophore was found within the atrium, its morphology
was also noted. Contingency tables and 2 tests were undertaken to investigate differences between A. hortensis s.s. and
A. distinctus in relation to habitat type, and differences
between the frequencies of the bi- and tripartite forms of A.
distinctus at sites where only this species occurred or at sites
where both species coexisted. All the biological material used
in this study is stored at the Research Institute of Organic
Agriculture (FiBL) in Frick, Switzerland. UTM coordinates
were obtained using the facilities of the internet site http://
www.dmap.co.uk.
As Davies (1977) reported attempts for courtship between
members of different species of the A. hortensis aggregate, we
kept 10 A. hortensis s.s.–A. distinctus pairs, and five conspecific pairs of each species in boxes with moist soil and
lettuce as food, and observed them at least once daily for 40
days.
RESULTS
The distribution map presented in Figure 1 is based on
394 animals, coming from 31 different sites (Table 1).
Overall, 48% of the animals belonged to the species A.
hortensis s.s. and 52% to A. distinctus. Of the 31 sites
sampled, 13 (42%) contained both species, 10 (32%)
contained only A. distinctus and eight (26%) contained
only A. hortensis s.s. In the 13 sites where both species
coexisted, seven (54%) were dominated (i.e. 50% of
the animals) by A. distinctus, three (23%) were dominated by A. hortensis s.s. and three (23%) had similar
numbers of both species. All the A. hortensis s.s. had a
fully developed reproductive system, while 10 (5%) A.
distinctus specimens, despite large body size and the
fact that the structure associated with the outlet of the
epiphallus in the atrium allowed species identification,
did not have a fully developed reproductive system.
Arion hortensis s.s. spermatophores were found in nine
animals, but no A. distinctus spermatophores were
found. The frequencies of A. hortensis s.s. and A. distinctus in gardens and in other habitats were significantly different (2 111.7, P 0.001; see Table 2A).
Arion hortensis s.s. was more frequent in gardens, while
A. distinctus was more frequent in the other habitats
sampled.
In A. distinctus, 61.3% had a bipartite oviduct, and
38.7% had a tripartite oviduct. A ligula-like structure
inside the proximal part of the oviduct was never found
in the bipartite form, but was present in most of the
animals of the tripartite form. The frequencies of the
bi- and the tripartite form of A. distinctus were very different at sites where only A. distinctus occurred and at
sites where both species occurred (2 24.4, P 0.001;
Figure 1. Distribution of Arion hortensis s.s. and A. distinctus in the sampled area, based on the internal anatomy of 394 specimens. Records
from the literature based on Oberer & Krumscheid (1998) and Turner et al. (1998).
210
ARION HORTENSIS S.S. AND A. DISTINCTUS IN SWITZERLAND
Table 1. Original sites and UTM coordinates for the animals included in this study, and number of animals from each location. Sampling method: S by sight, T traps. Arion distinctus type A form with
bipartite oviduct, type B form with tripartite oviduct. All UTM coordinates refer to the square 32T of the
worldwide grid.
A. distinctus
Site (canton)
Etzgen (AG)
Gipf-Overfrick (AG)
Niederlenz (AG)
Seon (AG)
Mellikon (AG)
Binningen (BL)
Gelterkinden (BL)
Wintherthur (ZH)
Bülach (ZH)
Guntetswil (ZH)
Bern (BE)
Grossdietwil (LU)
Trimbach (SO)
Frick-1 (AG)
Frick-2 (AG)
Frick-3 (AG)
Frick-4 (AG)
Frick-5 (AG)
Frick-6 (AG)
Frick-7 (AG)
Frick-8 (AG)
Laufen (BL)
Eschenbach (LU)
Aesch (BL)
Pfungen (ZH)
Tägerwilen-1 (TG)
Tägerwilen-2 (TG)
Rüstenschwil (AG)
Hosenruck (TG)
Luttingen
(SW Germany)
Lienheim
(SW Germany)
1 1 km
grid UTM
Habitat and
sampling method
MT3269
MT2460
MT3750
MT3744
MT5168
LT9266
MT1357
MT8263
MT6663
MT8665
LT8001
MT1524
MT1546
MT2663
MT2663
MT2663
MT2662
MT2662
MT2662
MT2663
MT2861
LT8752
MT4819
LT9159
MT7262
NT1078
NT1278
MT5129
NT0959
MT3068
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (S)
Garden (ST)
Garden (ST)
Garden (ST)
Wildflower-strip (ST)
Wildflower-strip (ST)
Wildflower-strip (ST)
Wildflower-strip (ST)
Wildflower-strip (S)
Wildflower-strip (S)
Field margin (S)
Grassland (S)
Grassland (S)
Rhubarb (S)
Vegetables (S)
Field margin (S)
Strawberries (S)
Field margin (S)
MT5268
Field margin (S)
see Table 2B). The bipartite form was more frequent at
sites where only A. distinctus occurred, while the tripartite form was more frequent at sites where both species
coexisted.
With respect to external appearance, the typical form
of the A. hortensis s.s. found in this study had a bluegrey (54% of the specimens) or blue-black (46% of the
specimens) general colour. The lowest row of tubercles
was pure white and contrasted strongly with the dark
colour of the body (Table 3). The right mantle band
was judged to run over the pneumostome in 44% of the
specimens of A. hortensis s.s. and through the pneumostome in 42% of the specimens, while in 14% the position of the band was doubtful. Most A. distinctus had a
yellowish brown general colour (86% of the specimens).
Type A
2
1
4
5
1
7
10
Type B
2
3
1
4
3
4
3
1
6
10
15
9
5
8
3
8
5
1
3
3
9
3
4
10
10
2
5
7
3
5
3
7
3
A. hortensis
s.s.
10
10
8
5
13
4
10
2
5
10
10
28
14
26
10
2
2
4
10
6
5
2
In 41% of the A. distinctus, the lowest row of tubercles
was white-cream and less conspicuous than in A. hortensis s.s. In 59% of the A. distinctus, the right mantle
band ran through the pneumostome, while in 29% it
ran over the pneumostome, and in 12% the position of
the band was doubtful.
Only three copulations were observed. The same pair
of A. distinctus was seen copulating twice; the second
time they were killed immediately, and after dissection
a spermatophore was found within the atrium of one
slug. Both mates had a bipartite oviduct. One pair of
A. hortensis s.s. was also seen copulating. Although
copulation between a mixed pair was never actually
seen, one A. hortensis s.s. and one A. distinctus were seen
on a big patch of mucus in a more or less encircled posi-
211
J. IGLESIAS & B. SPEISER
tion: dissection confirmed the heterospecific identity of
the animals and a typical A. distinctus spermatophore
was found within the atrium of the A. hortensis s.s,
indicating that they had mated. The A. distinctus had a
bipartite oviduct and did not have a spermatophore
within the atrium.
DISCUSSION
In this study, A. hortensis s.s. was almost equally as frequent as A. distinctus. The geographical distribution of
the two species does not show any clear pattern. Sites
containing both species were the most abundant and
they were evenly spread over the study area. In contrast, A. distinctus is much more abundant and more
widely distributed than A. hortensis s.s. in Belgium (De
Wilde, 1983) and in the Netherlands (De Winter, 1984;
Gittenberger, Backhuys & Ripken, 1984). For Switzer-
land also, there are many more records of A. distinctus
than of A. hortensis s.s. (Oberer & Krumscheid, 1998;
Turner et al., 1998). Arion hortensis s.s. has probably
been overlooked in Switzerland, since slugs of the A.
hortensis complex were usually assumed to be A. distinctus and most of the previous data are based on
external features. From our data, however, it cannot be
decided whether A. hortensis s.s. in Switzerland has
been largely overlooked until now, or whether it has
become more frequent. Arion hortensis s.s. is a species
with a predominantly Atlantic distribution (De Winter,
1984) and it might be spreading over Central Europe.
The congeneric pest species Arion lusitanicus, originally
endemic to the Iberian Peninsula, has been spread over
Central, Northern and Eastern Europe apparently by
international trade and mainly through introduction in
home gardens (von Proschwitz, 1997). As A. hortensis s.s.
was also found to be closely associated with gardens, it
might be spreading in a similar way. However, we do not
Table 2. Number of slugs of different species and, for A. distinctus, with different internal
morphology, a) in gardens versus other habitats (wildflower strips, field margins, grassland, strawberry and vegetable fields), and b) at sites where only A. distinctus occurred
versus sites where both species coexisted. A. distinctus type A form with bipartite
oviduct, type B form with tripartite oviduct.
A. hortensis
s.s.
a) Habitat type
Gardens
other habitats
b) Sites with
only A. distinctus
both species
A. distinctus
total
A. distinctus
type A
A. distinctus
type B
155
35
57
147
31
94
26
53
76
115
89
88
37
27
52
Table 3. Numbers of specimens with different morphological and anatomical characteristics, determined from 190 A. hortensis s.s. and 204 A. distinctus (* general colour
determined from a subsample of 100 A. hortensis s.s. and 90 A. distinctus).
External morphology
Position of the right mantle band
over the pneumostome
through the pneumostome
position doubtful
General body colour*
predominantly blue-grey
predominantly blue-black
predominantly yellowish brown
Internal anatomy
Oviduct tripartite with ligula-like structure
Oviduct tripartite without ligula-like structure
Oviduct bipartite with ligula-like structure
Oviduct bipartite without ligula-like structure
212
A. hortensis s.s.
A. distinctus
84
79
27
58
121
25
54
46
0
4
9
77
190
0
0
0
72
7
0
125
ARION HORTENSIS S.S. AND A. DISTINCTUS IN SWITZERLAND
have data about the occurrence of A. hortensis s.s. in
natural habitats and we cannot exclude expansion of
its range for other (natural) reasons.
Our observations agree with Davies (1979) in the fact
that A. distinctus matures and breeds later than A. hortensis s.s. Some of the large A. distinctus had a poorly
developed reproductive system, while all the large A.
hortensis s.s. specimens were completely mature. Also,
nine spermatophores of A. hortensis s.s., but none of A.
distinctus were found in freshly collected and dissected
animals.
In our samples of A. distinctus, we found 39% of individuals with a tripartite oviduct. In the British Isles the
tripartite form accounted for one third of the animals
(Davies, 1977). De Wilde (1983) did not find the tripartite form in Belgium. According to De Winter (1984),
the tripartite form seems to be common in the western
Alps, but rare in the rest of Europe. In Northern Germany, the tripartite form is rarer than the bipartite (H.
Reise, personal communication). Barker (1999) found
both forms in New Zealand. Davies (1977) pointed out
that either the bi- or the tripartite form of A. distinctus
may predominate temporarily in a population. We
found a highly significant difference in the frequency of
both forms of A. distinctus between sites where only this
species occurred and sites where both species coexisted,
but caution is needed in the interpretation of this result.
The finding of an A. distinctus spermatophore within
the atrium of an A. hortensis s.s. specimen indicates
that interspecific matings are at least attempted. However, hybridization between the two species is believed
to be extremely improbable since the two species differ
in morphological, behavioural (Davies, 1977, 1979),
anatomical (De Wilde, 1983; De Winter, 1984; Backeljau & Marquet, 1985) and electrophoretic criteria
(Backeljau, 1985; Dolan & Flemming, 1988; Backeljau
& De Bruyn, 1990). The spermatophores of A. hortensis
s.s. and A. distinctus are completely different (Backeljau
& Van Beeck, 1986). In A. hortensis s.s., the spermatophore is thick, with a hard attachment collar, a straight
serrated ridge and a strongly curved hook at the posterior end. In A. distinctus, the spermatophore is much
more slender, the attachment collar is poorly developed,
has no or only very weak serrations, and the posterior
end is not curved as a hook. The clear differences among
the spermatophores and genital parts involved in their
transfer are believed to constitute an effective physical
barrier to interbreeding (Davies, 1977; Backeljau & Van
Beeck, 1986). The finding reported here of one species’
spermatophore within the atrium of the other species
means that the above-mentioned physical barrier is not
completely effective. Yet, the physical possibility of
spermatophore transfer between different species does
not mean that interspecific fertilization of the eggs
occurs. Moreover, we do not know whether this event
observed in the laboratory also takes place under natural
conditions. In indoor cultures, Davies (1977) observed
that sexually active slugs often perform courtship (following and nibbling) with members of the other two
sibling species.
This study confirms that a safe distinction between
A. hortensis s.s. and A. distinctus is only possible using
internal anatomy (Kerney et al., 1983; De Winter, 1984;
Backeljau & Van Beeck, 1986). Because such criteria
are time-consuming and cannot be used in the field, we
assessed the accuracy of external features, i.e. differences in colouration and in the banding pattern. The
general body colouration cannot be considered as a
criterion for a reliable identification of the two species,
but it allows a reasonable approximation. All the A.
hortensis s.s. in our study area were either blue-grey or
blue-black, with a strikingly white lowest row of tubercles. In A. distinctus, 86% of the specimens were yellowish brown. However, similar colouration is reported
for both species from different sites, and it is not certain
within what geographical range this criterion can be
used. Davies (1979), De Wilde (1983) and De Winter
(1984) described the typical A. hortensis s.s. as blueblack slugs, while the blue-grey colour has been described for both A. hortensis s.s. and A. distinctus
(Davies, 1977). The strikingly white lowest row of
tubercles mentioned by Davies (1979) and De Winter
(1984) was characteristic of A. hortensis s.s. in our study
area. De Winter (1984) described the typical colour of
A. distinctus as yellowish brown, and he also noted that
some A. distinctus had a whitish lowest row of tubercles, less conspicuous than those in A. hortensis s.s.
Arion distinctus was described as yellowish grey by
Davies (1979) and De Wilde (1983), but the variable
general colour of both species was also pointed out by
both authors. The existence of a different tinge in the
head and tentacles of both species, reddish or violet in
A. hortensis s.s. and blue-black or grey in A. distinctus
(Davies, 1979; De Wilde, 1983; De Winter, 1984; Gittenberger et al., 1984), was not assessed in this study.
The position of the right mantle band (running over
the pneumostome in A. hortensis s.s. and through the
pneumostome in A. distinctus) is often mentioned as
characteristic for the identification of the two species
(Davies, 1977, 1979; De Wilde, 1983; Gittenberger et
al., 1984). De Winter (1984) stated that in most of the
specimens of A. distinctus, the band runs through the
pneumostome, but in the neotype of the species selected by him, the band runs over the pneumostome. In
this study, the position of the right mantle band conformed with the literature in only 44% of all A. hortensis
213
J. IGLESIAS & B. SPEISER
s.s. and 59% of all A. distinctus. Judgement of this character needs the band to have well defined edges, which
is not always the case. Accordingly, we conclude that
the position of the band is not a good character for
external identification of the species.
ACKNOWLEDGEMENTS
We want to thank H. Reise, J. Castillejo and two anonymous
referees for their comments on the manuscript, S. Capt
(CSCF Neuchâtel) for help with coordinate transformation,
and all those who supplied us with slug samples. This study
was financed by a grant from the University of Santiago de
Compostela to J. Iglesias and by the Swiss Federal Office for
Education and Science (BBW grant no. 97.0194, linked with
EU FAIR project CT 97–3355).
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