Overexploitation, habitat destruction and a changing climate threaten
populations of the Roman snail (Helix pomatia Linnaeus, 1758), which has led to a high protection
status in Germany. Vertebrate and invertebrate predators, including
parasites and facultative parasitoids, further cause pressure on
populations. Given the conservation concern for H. pomatia and its rarity in the study
region (Cottbus, Germany), we studied how predators and facultative
parasitoids utilize H. pomatia shells with a focus on non-invasive field methods. As
previous studies indicated that shell size may affect prey selection by
predators, morphometric traits were measured in eight subpopulations. We
identified the total number and percentage of H. pomatia shells that showed external
attack marks by predators and internal utilization marks by Diptera pupae
and related those utilization patterns to the morphometric traits of shells.
A large proportion of the shells in local subpopulations showed signs of
external attack and internal utilization, and both utilization forms were
positively correlated. External attacks by predators were more frequent in
larger shells and internal utilization by Diptera was more common in shells
with higher body density. These results suggest a considerable pressure by
predators and potential facultative parasitoids on H. pomatia populations in the study
area. Future research should focus on the relationship between snails from
the family Helicidae and flies from the genus Discomyza. Conservation programmes should
consider abiotic habitat conditions together with potential trophic
interactions to maximize the success of conservation strategies.
Introduction
The Roman snail (Helix pomatia Linnaeus, 1758) is of considerable commercial interest as human
food (also called “edible snail”; Bloszyk et al., 2010; Gheoca, 2013) and in medical
research (Dwek et al., 2001). Exploitation by humans is a potential cause for
population declines (Welch and Pollard, 1975; Andreev, 2006), especially as
the species has a relatively slow reproduction and maturation rate
(Ligaszewski et al., 2014) and long dormancy periods (Lind, 1989).
Nevertheless habitat destruction (Andreev, 2006) and a changing climate
(Nicolai and Ansart, 2017) may threaten H. pomatia populations in the future as well,
particularly in areas with unfavourable soil conditions. Those conservation
concerns resulted in the development of breeding programmes to protect the
species (Hardouin, 1995; Ligaszewski et al., 2014). National and EU-level
regulations address overexploitation by creating different protection
categories (Bouchet et al., 1999; Ligaszewski et al., 2016). National
regulations protect H. pomatia in Germany (Bundesartenschutzverordnung (BArtSchV)
Paragraph 1 Satz 1) and control the collection of snails, but they do not
implement specific conservation programmes. The study area, in the Federal
State of Brandenburg has a continental, dry climate with a limited presence
of calcareous soils which both contribute to the rarity of the species and
through this increase its conservation value. A citizen science project
coordinated by the Nature and Biodiversity Conservation Union focuses on the
identification of remaining habitats of H. pomatia and highlights the public awareness
for the conservation of this species in the study region (NABU, 2019).
In addition to human exploitation, habitat management and climatic
fluctuations, pressure from natural enemies may further affect populations
of H. pomatia. Birds (e.g. Coracias garrulus Linnaeus (European roller) and Phasianus colchicus Linnaeus (pheasant)),
rodents (e.g. Apodemus sylvaticus (Linnaeus) (wood mouse) or Rattus rattus (Linnaeus) (black rat)), reptiles
(e.g. Anguis fragilis Linnaeus, 1758 (slow worm)) and ground beetles (e.g. Cychrus species) feed
on H. pomatia (Coupland and Barker, 2004). Cychrus species even have morphological
adaptations to their mouth parts to allow them to attack and consume snails
(Digweed, 1993), but other, more opportunistic predaceous ground beetle
species also attack terrestrial snails (Larochelle, 1990). Several Diptera
species (e.g. Fannia canicularis (Linnaeus), Sarcophaga (Myorhina) nigrivantris, Chaetopleurophora bohemanni or Spiniphora bergenstammi) may act as facultative parasitoids of
H. pomatia (Barker et al., 2004). For other Diptera species, information is less well
known or conflicting. For example, Discomyza species, like D. incurva, breed in dead snails
(Ferrar, 1987; Zatwarnicki and Mathis, 2007) and have been considered as parasites
of H. pomatia for a long time (von Bergenstamm, 1864). Previous studies from Europe
describe the occurrence of D. incurva in snail shells as rare or did not find this
species in shells (Beaver, 1977; Buck et al., 2006).
Very little is known about population-level effects of predation on
terrestrial snails (Millar and Waite, 1999), but even less is known about
selection of prey or host snails by predators or parasitoids (Vermeij, 1995).
Natural enemies of terrestrial snails often leave marks on the shell, either
through external attack marks damaging the shell or internal utilization
marks by larvae of pupae. Only two previous studies have used these marks to
contribute to a better understanding of predation on terrestrial snails:
Millar and Waite (2004) recorded patterns of shell damage in an English
woodland and Němec and Horsák (2019) recently compared the identity
of predator groups causing marks on the shells of the steppe snail Granaria frumentum
(Draparnaud, 1801). Predation at the population level affects morphometric
traits of shells (e.g. shell size; Goodfriend, 1986), and larger shells may
even suggest a selective advantage against future predation (Liew and Schilthuizen, 2014). Shell size also affects predation, as for example
smaller individuals of Cepaea nemoralis (Linnaeus, 1758) are more frequently attacked by
beetles than larger individuals (Oosterhoff, 1977). Birds, for example song
thrushes, showed preferences for larger shell sizes in the same species, but
prey choice also depended on the different morphs in this snail species
(reviewed in Goodfriend, 1986). Simultaneously considering external attack
and internal utilization marks on snail shells together with morphometric
shell traits will therefore contribute to a better understanding of attack
and utilization patterns in H. pomatia populations.
Given the conservation concern for H. pomatia and its rarity in the study region, this
field study focused on an improved understanding of how predators and
facultative parasitoids utilize H. pomatia, with a focus on non-invasive field methods.
We identified the number and percentage of H. pomatia shells that showed external
attack marks by predators and internal utilization marks by Diptera pupae.
To understand drivers of attack and utilization patterns, we measured
morphometric traits of shells and related them to the observed proportion of
marks in local subpopulations. We hypothesize that larger snail shells are
more vulnerable to external attacks of predators due to a higher visibility
but that the proportion of internal utilization marks by Diptera pupae is
independent of morphometric traits.
Material and methodsStudy area and snail sampling
The study area “Sachsendorfer Wiesen” is part of an approximately 350 ha
large nature conservation area in Cottbus, Germany (Wollmann, 2002). After
previous intensive agricultural use, the area has been managed as an amenity
grassland since 1991. The single management practice is mowing, and the
cutting frequency is once or twice a year. The vegetation in the area is
dominated by Urtica dioica L. (common nettle), Aegopodium podagraria L. (ground elder) and Chelidonium majus L. (greater
celandine).
The municipality of Cottbus gave permission to perform this research, under
the conditions that no individuals of H. pomatia will be harmed and that areas that
have been designated for the protection of the bird species Crex crex (Linnaeus,
1758) (corn crake) will not be entered.
We selected eight subpopulations of H. pomatia with a minimum distance of 30 m and
physical barriers such as by railway tracks or buildings between them. Prior
to the sampling of shells, the whole study area was carefully surveyed for
the presence of H. pomatia individuals and subpopulation habitats were
selected based on their isolation from nearby habitat patches. Between 28 September 2016 and 30 November 2017, the same researcher sampled 642 empty
H. pomatia shells (range of shells per subpopulation 34–166; Table 1) for examination
of external attack marks by predators or internal utilization marks by
Diptera pupae. Visual search for empty shells is a non-destructive sampling
technique, which is a key priority for studies of protected species. This
approach across the subpopulation area was optimized for the collection of a
high number of empty shells across the subpopulation area. However, estimates of morphometric traits may be biased towards larger,
more conspicuous shells, and attack and utilization marks may result from
interactions after the snail already died. To estimate subpopulation
densities, we visually counted all living individuals in spring 2017 and
spring 2018 within an area of 9 m2 at three locations in each
subpopulation. This approach was optimized for a standardized sampling of
subregions in each subpopulation to derive reliable estimates of population
sizes of living snails. Live individuals of the protected species H. pomatia were not
sampled or killed during this study.
The estimated subpopulation size, total number of shells examined
(i.e. number of shells examined for external attack marks), percentage of
shells with external attack marks, subset of shells examined for internal
utilization marks, and percentage of shells with internal utilization marks.
The final column shows the mean number of pupae observed per shell with
internal utilization marks ± standard error of the mean.
SubpopulationSubpopulationNo. shells% externalNo. shells% internalMean pupaesizeexternalinternalper shell127366366.73464.716.5±4.62202516628.37934.323.1±6.73279314414.67748.625.1±5.941635141.23056.721.2±4.8516953415.73339.413.4±3.46155310731.83548.611.3±2.972683548.63450.016.4±3.3822284247.63148.46.4±2.0Utilization marks
Out of the total 642 shells that were sampled for external attack marks, a
random subsample of 353 shells was opened and checked for internal
utilization marks by Diptera pupae. This was done in the laboratory, where
we used needle-nose pliers to open shells from the aperture around the
columella up to the apex. All marks indicating attacks on the outside of the
shell were recorded in the category “external attack” (Fig. 1a). Note that
these marks are not equivalent to predation records, as the cause of
mortality remains unknown and as marks could result from post-mortem
attacks. External damage to shells by larger mammals is very unlikely, as
the area is not visited by wild boars and as visits from other larger
mammals are extremely rare due to the close proximity to human
infrastructure and settlements. Only shells with marks indicating the
presence of Diptera pupae (preserved pupae or black marks on the inside of
the shell indicating attachment points of pupae) were considered for the
category internal utilization mark (Fig. 1b and c). Discomyza incurva (Fallén, 1823), as a
common species found in shells in this study, have larvae that are known to
feed on decaying H. pomatia (von Bergenstamm, 1864; Sequy, 1934). It is unknown
whether this species attacks living snails or primarily deposits eggs on
snail carcasses (Kofler and Mildner, 2004), and internal marks cannot be
differentiated between predation or scavenging events.
Helix pomatia shells with (a) external attack marks (bird attack), (b) internal
utilization marks from Diptera pupae and (c) details of internal utilization
marks with Diptera pupae.
The scale bar shows 1 cm in (a) and (b) and 1 mm in (c).
Morphometric traits and soil pH
The following morphometric traits were recorded from all subpopulations. The
average mass of snails with shell was calculated on-site in each
subpopulation by weighting living snails with a CS digital scale in April 2017 after hibernation. This was done per subpopulation for a minimum of 30
randomly selected snails per subpopulation to result in an average total
mass of snails per subpopulation (hereafter 149 “masstotal”). Between
autumn 2016 and spring 2017 a minimum of 30 empty shells were collected in
each subpopulation and weighed resulting in the average total mass (in g) of
shells per subpopulation (hereafter “massshell”). The average mass of
shells (massshell) was then subtracted from the average mass of
snails in each subpopulation (masstotal) to provide an estimate of
the mass of snail bodies without shells per subpopulation
(hereafter “massbody”; Sepúlveda et al., 2012). In all subpopulations we
measured 30 to 100 shells for shell height and width (in mm) with a sliding
calliper. Shell volume (hereafter “volumeshell”) was calculated for these
shells by filling empty shells with sand and by then measuring the volume of
sand per shell. Body density was mostly measured among aquatic gastropods in
order to determine vulnerability regarding earthquakes or predators (Baums
et al., 2003; Seike et al., 2019; Steward and McHenry, 2010), but this has not been
addressed in terrestrial snails. Due to state laws considering the
protection of H. pomatia, we needed to use a non-destructive method to
calculate the quotient of the average body mass without shell
(massbody) and the average volume of shells (volumeshell) in each
subpopulation.
To measure local soil pH, 76 soil samples were taken from the upper 10 cm
across the subpopulations. Depending on the area size for each subpopulation
two to six soil samples were taken and the average soil pH was calculated
for each area. Soil pH was measured using the Microprocessor-Präzisions-pH/mV-Meter pH 539 (Wissenschaftliche-Technische-Werkstätten GmbH)
and 0.01 M CaCl2. The soil sample was taken from the upper 10 cm as Helix pomatia is
primarily in contact with this soil layer.
Statistical analyses
Regression analyses were performed with distance-based linear models
(DistLMs), an approach which can use non-Euclidean resemblance measures and
derives p values from permutations (Legendre and Anderson, 1999; McArdle
and Anderson, 2001). This approach has the advantages of allowing for internal
standardization if predictor variables are not measured on the same scale
(e.g. different morphometric traits like height in mm and mass in g) and
relaxes the assumption that errors have to be normally distributed (Anderson
et al., 2008). To test for the effect of soil pH, the percentage of internal
utilization or external attack marks and the number of pupae on
subpopulation size, we independently related these four predictors to the
local estimate of snail density with DistLM. To find the best model
predicting the variation in all four considered morphometric traits, we
related soil pH, the percentage of internal utilization or external marks,
and the number of pupae per shell as predictor variables to a resemblance
matrix based on a multivariate dataset including the width (mm), height
(mm), mass with (g) and without shell (g), and body density ratio in a single
multiple multivariate regression model. We used Gower distances to generate
a resemblance matrix of snail subpopulations to internally standardize for
the different measurement scales of morphometric traits. The best model in
this multiple, multivariate regression approach was selected based on data
on from subpopulations (N=8) and the AICc (version of Akaike information criterion with correction for small sample sizes). criteria for small sample sizes
from all models with all possible predictor combinations. Models within
2Δ AICc units of the best model are considered in the results
section. All p values were based on 9999 permutations. Correlation analyses
were performed using Pearson correlations. Principle coordinates ordination
(PCO) illustrates the relationships between morphometric traits and
predictors in an unconstrained ordination. All statistical analyses were
performed with Primer v7.0 and the PERMANOVA add-on.
Results
The average estimated density of snails across the subpopulations was
0.4±0.1 (mean ± SD) individuals per square metre. Out of 642 shells of
H. pomatia analysed for external attack marks, 207 (32 %) showed signs of external
attacks (Table 1). Out of 353 shells analysed for marks of internal
utilization by Diptera pupae, 159 (45 %) showed such signs.
The percentage of shells with external attack and internal utilization marks
correlated significantly across subpopulations (Fig. 2a, R=0.79;
p=0.020). The percentage of internal utilization marks further
significantly correlated to the local soil pH across subpopulations (Fig. 2b, R=-0.74; p=0.036). Other correlations between soil pH, percentage of
internal utilization and external attack marks, and average number of pupae
per shell were not significant (p>0.05).
Relationship between internal utilization marks and (a) external
attack marks and (b) soil pH in shells of Helix pomatia in the studied subpopulations
(N=8). Note that a single shell could show external attack and internal
utilization marks.
The correlation of local density of snails per subpopulation was not
significant to soil pH (R2=0.39; p=0.108) or the
percentage of internal (R2=0.04; p=0.410), external
attack marks (R2=0.04; p=0.637) nor to the average
number of pupae per attacked shell (R2=0.06; p=0.555).
In total, 49 % of all analysed shells contained pupae and the average
number of pupae per shell was 18.0±1.9 (Table 1).
The best model to predict the variation in the analysed morphometric traits
included the percentage of external attack marks as single significant
predictor (AICc =56.5; R2=0.35; p=0.039), with one
alternative model within 2ΔAICc units (internal utilization marks
only: AICc =58.07; R2=0.21; p=0.219). Both soil pH
(R2=0.06; p=0.794) and the average number of pupae per
shell (R2=0.03; p=0.911) did not significantly affect
the morphometric traits of shells. The ordination shows that most of the
overall variation in all morphometric traits was explained by the individual
variation in size (height and mass in Fig. 3) of shells (axis 1=58.2 %)
and body density (axis 2=28.4 %). Larger shells had more external attack
marks, and shells with higher body density had more internal utilization
marks (Fig. 3).
Principle coordinates ordination based on a resemblance matrix
(Gower distances) from morphometric traits (shell height and width
in millimetres, shell mass in grams, mass without shell in grams and body density in mass : volume
ratio) in the studied subpopulations. Vectors for morphometric traits
(without arrow) and predictors (with arrow: soil pH, % internal
utilization and external attack marks) were superimposed based on Pearson
correlations with axis scores of the individual subpopulations.
Among the vertebrate predators in the study area, Turdus philomelos, Turdus merula Linnaeus, 1758 and Pica pica
(Linnaeus, 1758) were most frequently observed. Arvicolinae and Natrix natrix (Linnaeus,
1758) were also present, but restricted to certain areas.
Discussion
A large proportion of the shells in local subpopulations showed signs of
external attack (207 of 642 shells) and internal utilization (159 of 353
shells), and both utilization forms were positively correlated. Larger shells
were more prone to external attack, and a higher body density resulted in
more frequent internal utilization by Diptera. These results suggest a
considerable pressure on H. pomatia by predators and potential facultative parasitoids
in the study area.
Previous studies suggest that terrestrial snails are often not an important
component of vertebrate diets and more related to certain periods (Goodhart,
1958; Davies and Snow, 1965; Gruar et al., 2003). Amongst the potential
vertebrate predators, we observed T. philomelos, Turdus merula Linnaeus, 1758 and Pica pica (Linnaeus, 1758) to
attack individuals of H. pomatia in the study area. Turdus philomelos may be a major predator of
invertebrates in the study area, but snails account for less than 20 % of
the diet in this species, while other bird species incorporate even lower
numbers of snails into their diet (≤5 %; Krištin, 1992). Previous
research showed that external predators prefer snails with bigger shells due
to the investment of energy in handling and breaking snails (Zach, 1978;
Rosin et al., 2011; Brodersen et al., 2002; Allen, 2004). Furthermore, most snails are
nocturnal and hide during the day (South, 1992) and larger shells may be more
conspicuous during daytime. This positive relationship between shell size
and external attack rates on the shell may be most important for visual
predators (e.g. birds), as smaller less visually oriented predators may
rather prefer snail prey with smaller shells (e.g. Oosterhoff, 1977). The
present study shows that subpopulations with larger shells have higher
proportions of external attack marks than subpopulations with smaller shell
size. High predation pressure can affect population dynamics in terrestrial
snail species but does not necessarily lead to a decline in population size
(Allen, 2004). Invertebrate species that attack snails from the outside may
have different preferences. Several beetle species incorporate gastropods
into their diet (Symondson, 2004) but prefer smaller and injured snails due
to attraction by emitted mucus (Mead, 1961; Wheater, 1987; Digweed, 1993).
Regarding internal utilization, a large proportion of shells showed internal
utilization marks from Diptera pupae (mainly genus Discomyza). In this study, we
observed a large number of pupae (up to 128) per shell and 45 % of all
analysed shells showed signs of utilization by Discomyza pupae. Discomyza incurva was previously
considered as rare or recorded in low numbers from snail shells (Drake, 2006;
Hofer and Waitzbauer, 2000), an observation we could not confirm in this
study. Buck et al. (2006) stated that Discomyza flies only have a limited impact on
snail populations. Potential body density showed the strongest correlation
with percentages of internal utilization marks per subpopulation, and a high
body density may result in higher oviposition rates by female flies. A
higher nutritional value in snails with higher body density could explain
the observed relationship. Other studies already confirmed that female flies
of the family Phoridae prefer protein-rich food (Coupland and Barker, 2004)
and that the fecundity of female flies in the family Sciomyzidae depends on
the quality of the food (Beaver, 1973; Knutson and Vala, 2002). However, it
remains unknown to what extent Discomyza incurva attacks living snails or primarily feeds on
snail carcasses. Future research in this area could focus on live samples of
Helix pomatia and Discomyza incurva to study interactions between these species in the laboratory. Field
observations should address the timing of attacks and the state of the
snail/shell at times of attack by the fly.
Larvae from different Diptera species have different pH optima (Grunewald,
1976; Uutala, 1987; Arimoro et al., 2007). Manipulation of
the pH value of food attractants for example considerably altered the number
of attracted female fruit flies (Bateman and Morton, 1981; Epsky et al.,
1993; Heath et al., 1994; Duyck et al., 2004). Regarding the observed positive
relationship between soil pH and the percentage of internal utilization
marks in this study, soil pH values may have indirectly affected the number
of ovipositing female Diptera. Snails consume soil (Elmslie, 1998; Mensink
and Henry, 2011), and the diet alters the mineral content of the body tissue
(Ireland and Marigomez, 1992; Ademolu et al., 2004) with potential
consequences for their vulnerability to female flies.
The present study documents a high potential predation pressure and a
positive relationship between external attack and internal utilization marks
in subpopulations of H. pomatia in unfavourable environmental conditions. Previous
studies documented that protection of H. pomatia subpopulations against vertebrate
predators can contribute to an increase of population sizes (Sherley et al., 1998; Neuweger et al., 2001). In such conservation programmes,
it is important to consider that external predators prefer larger
individuals. Predators may vacate a feeding site, as soon as large
individuals are exploited, and the snail population may recover relatively
quickly after major predator species vacated the area (Mead, 1979). As H. pomatia has
one of the highest legal protection statuses in Germany, priority needs to be
given to the protection of suitable habitats.
Data availability
Data can be requested via the responsible author Claudia Tluste: claudia.fuessel@yahoo.de.
Author contributions
CT carried out the field work as well as the data processing and the writing of the paper. KB was responsible for statistical analyses
in Sect. 2.4 as well as corrections within the paper. UB was responsible for corrections
in between and provided advice. TN provided additional helpful information regarding shell marks.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We thank the municipality of Cottbus for the permission to perform research
in the “Sachsendorfer Wiesen” landscape protection area. Matthias Foellmer, Carolyn Trietsch, one anonymous referee and the subject
editor contributed valuable comments to a previous
version of this manuscript.
Review statement
This paper was edited by Matthias Foellmer and reviewed by Carolyn Trietsch and one anonymous referee.
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