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Interspecific competition among terrestrial slugs

Interspecific competition among terrestrial slugs Journal of The Malacological Society of London Molluscan Studies Journal of Molluscan Studies (2022) 88 : eyac007. https://doi.org/10.1093/mollus/eyac007 Published online 4 April 2022 Interspecific competition among terrestrial slugs 1 2 Johan Watz and Daniel Nyqvist River Ecology and Management Research Group (RivEM), Department of Environmental and Life Sciences, Karlstad University, Karlstad, Sweden; and Department of Environment, Land and Infrastructure Engineering, Politecnico di Torino, Turin, Italy Correspondence: J. Watz; e-mail: johan.watz@kau.se (Received 2 August 2021; editorial decision 22 November 2021) ABSTRACT Interspecific competition among terrestrial gastropods has previously been considered to have little effect on population dynamics and local distribution. Recent studies, however, demonstrate several cases in which interspecific competition plays a major role in structuring terrestrial gastropod communities. To explore the general importance of interspecific competition for the ecology of slugs, we conducted a semi-systematic literature review, synthesizing available peer-reviewed literature relating interspecific interactions to the fol- lowing: (1) mortality and reproduction; (2) activity, movement, feeding and growth; and (3) habitat use and geographical distribution of slugs. To support the literature on slugs, we also reviewed literature on terres- trial snails. The body of available literature is relatively limited, but the effect of interspecific competition on survival, reproduction, movement and activity has clearly been demonstrated in laboratory experiments for different slug species. The occurrence of interspecific competition seems, however, to be species specific, and no negative effects due to the presence of heterospecifics have been reported for many of the species com- binations investigated to date. Most of the studies demonstrating interspecific effects between slug species involved interference from a few aggressive species (mainly Limax maximus as the aggressor). In addition, sev- eral correlative studies have indicated that in terrestrial gastropods, habitat use and geographical distribution might be mediated by interspecific competition. Further, well-designed experiments are needed to explore the general importance of interspecific competition among slugs, potentially with a focus on interactions between invasive and native species, where the lack of a shared evolutionary history and niche separation may increase the intensity of competition. Such experimental studies may produce information that has implications for the conservation of native species, as well as for management of invasive pests, because interspecific competition may result in local extinction of vulnerable species and influence the possibility of non-native species establishing invasive populations in new areas. INTRODUCTION interspecific competition among slugs, an animal group containing many serious and increasingly widespread (occurring worldwide in Interspecific competition reduces fitness among members of differ- some cases) pests of agricultural and horticultural crops ( Douglas ent species that use or defend shared limited resources ( Gustafsson, & Tooker, 2012 ; Cameron, 2016 ). 1987 ), and the characteristics of this biotic interaction can mediate Passive dispersal through human transport of plants and soil has coexistence and influence the evolution of the species involved. facilitated invasions of alien slugs into new areas far from their natu- In some cases, interspecific competition results in niche differen- ral range. Some of these species have become serious pests on crops, tiation, spatial or temporal displacement from a habitat, or local with substantial economic costs in the form of production loss and extinction. The competitive mechanisms underlying these effects pest control programmes (see reviews by South, 1992 ; Barker, 2002 ; are either exploitation, where resource use leads to depletion for Cameron, 2016 ). The introduction of alien slugs creates new com- other individuals, or interference, where individuals directly or binations of sympatric species, and the biotic interactions among indirectly prevent others from using the resource ( Barker, 2002 ; these species may have far-reaching ecological consequences, Dhondt, 2012 ). Understanding the mechanisms and predicting with implications for the design of integrated pest management the outcomes of competition between species may be critical, programmes. both for managing problematic, undesirable pests and for con- Although heavily debated, competition has been shown to shape serving vulnerable and desirable species. The aim of this review arthropod pest communities ( Stewart, 1996 ; Reitz & Trumble, is to synthesize the published scientific literature that addresses 2002 ), and among phytophagous insects, the evidence for its © The Author(s) 2022. Published by Oxford University Press on behalf of The Malacological Society of London. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Review Article J. WATZ AND D. NYQVIST Figure 1. A schematic figure showing the screening of papers on interspecific competition among terrestrial gastropods. Numbers within parentheses indicate the number of papers. importance is now indisputable ( Kaplan & Denno, 2007 ). Inter- petition NOT (marine OR freshwater)]”. This resulted in 786 pub- specific competition among terrestrial gastropods has previously lications (Fig. 1 ). In a first screening of titles and abstracts, 739 pub- been considered to have little effect on population dynamics and lications were excluded (the focus of these was typically on plant or local distribution ( South, 1992 ; Horsák, Zelený & Hájek, 2014 ; parasite ecology, sperm competition, or freshwater and marine gas- Cameron, 2016 ), and it has been reasoned that shelter and food tropods). The remaining 47 papers were read in detail, with 23 pub- resources should not constitute limiting factors ( N emec ˇ et al ., 2021 ). lications that lacked original data or were not relevant to our study Contrastingly, recent studies have demonstrated that interspecific being excluded. When reading the publications that we included competition plays a major role in structuring terrestrial gastropod (and their reference lists) and browsing the recent papers that had communities ( von Oheimb et al ., 2018 ) and is a significant factor cited them, we found 19 additional relevant publications that we when conserving vulnerable species ( O’Hanlon, Fahy & Gormally, had missed using our search string. These publications were also in- 2020 ) and managing pests ( Baker, 2021 ). Moreover, the underly- cluded in our study (i.e. ‘snowballed’). Thus, in total we reviewed 43 ing mechanisms (i.e. behaviours demonstrating exploitation of re- publications (Fig. 1 ; Supplementary Material Table S1); 16 of these sources and direct and indirect interference) that may lead to in- had information on slugs, whereas 27 focused exclusively on snails. terspecific competition among slugs and snails have been known for long (e.g. Cameron & Carter, 1979 ; Rollo, 1983a ; Baur & Baur, RESULTS 1990 ). The existing body of literature exploring the ecology and evo- Of the 16 slug papers included in our review, 8 investigated the out- lution of terrestrial gastropods has focused mainly on snails, owing come of potential competition through the study of slug distribu- partly to rich collections of shells ( Cameron, 2016 ). Here, we focus tion, 7 were based on experiments (often testing a particular com- on the reported outcomes and underlying mechanisms of interspe- petitive mechanism) and 1 described both laboratory experiments cific competition among slugs, but in cases where such information and the mapping of wild slugs. Five of the eight experimental pa- is lacking, we include available data from snails. Our aim is to ex- pers studying slug interactions found evidence of competition. Four plore the general importance of interspecific competition for the of these included non-native Limax maximus , whereas one included ecology of slugs. Specifically, we use a semi-systematic approach the interaction between the arguably native Geomalacus maculosus and ( Snyder, 2019 ) to categorize and synthesize information from pub- Lehmannia marginata . lished papers on the basis of three types of effects: (1) mortality and reproduction; (2) activity, movement, feeding and growth; and (3) habitat use and geographical distribution. Effects on mortality and reproduction Only a few studies have examined how interspecific competition directly affects the mortality rates and reproductive output of dif- ferent slug species. The most studied competitive interactions are MATERIAL AND METHODS those that include L. maximus and its negative effect on other species The Web of Science Core Collection was used for the literature (Fig. 2 ). In a series of enclosure experiments involving the non- search, with access to the following databases: Arts & Humanities natives L. maximus and Arion ater , and the native Ariolimax columbianus , Citation Index (1975–present), Conference Proceedings Citation interspecific competition affected survival, the number of eggs laid, Index—Science (1990–present), Conference Proceedings Citation egg size, the number of egg batches ( Rollo, 1983a ) and access Index—Social Science & Humanities (1990–present), Emerging to egg-laying habitat ( Rollo & Wellington, 1979 ). A common fac- Sources Citation Index (2015–present), Science Citation Index Ex- tor across the interspecific interactions was that the aggressive L. panded (1900–present) and Social Sciences Citation Index (1956– maximus reduced the performance of one or both of the other present). We used the search string “[(slug* OR snail*) AND com- species. Mortality was high for both A. ater and Ariolimax columbianus 2 SLUG COMPETITION Figure 2. A leopard slug Limax maximus interacting with a Spanish slug Arion vulgaris . Direct interference competition mediated by aggressive behaviour from leopard slugs has been reported in several studies. during August, coinciding with high temperatures and increased patterns. When interspecific competition strongly influences these aggressiveness of L. maximus. Late in the season, Ariolimax columbianus patterns, we expect niche separation, displacement or local extinc- also experienced increased mortality in sympatry with A. ater ; the tion. There are studies that indicate feeding niche separation (e.g. cause for this seems to have not been direct competition but the between L. maximus , Lehmannia marginata , Limax flavus and Limacus dying off of the semelparous A. ater after egg laying, with the decay- maculatus ; Cook & Radford, 1988 ) as well as those indicating little or ing carcasses being a source of pathogens ( Rollo, 1983a ). Thus, the no separation ( N emec ˇ et al ., 2021 ). However, experimental studies negative effect of A. ater on Ariolimax columbianus in the enclosure is with manipulated treatments to simulate allopatry vs sympatry are likely not important in nature. In addition, both A. ater and Arioli- needed to disentangle whether observed niche separation in feeding max columbianus produced fewer eggs, whereas A. ater also produced is caused by competition or simply represents different adaptations. smaller eggs and fewer egg batches in sympatry with L. maximus Aggression in slugs varies with species, size and season. Rollo & than in allopatry . Limax maximus , on the other hand, produced dou- Wellington (1979) studied direct interactions among several terres- ble the number of eggs in sympatry with the two other species as trial gastropods and no agonistic behaviours were seen during win- it did in allopatry. Between A. ater and Ariolimax columbianus (both ter, when instead individuals were seen to aggregate. Aggressive in- dominated by L. maximus ), no significant interspecific effects on re- teractions peaked in August, coinciding with the egg-laying season. production were observed. Limax maximus and, to some extent, A. subfuscus were aggressive, at- Similarly, in an enclosure experiment, involving Philomycus car- tacking and even pursuing other slugs (Fig. 2 ), especially during the olinianus and Arion subfuscus , no negative effects on P. carolinianus of reproductive period. interspecific competition (compared to intraspecific competition) Our review of the literature shows that L. maximus also plays were seen on the number of eggs laid. Instead, when food and shel- a central role in the interspecific effects relating to activity and ter were abundant (but not when these resources were limited), P. growth. In enclosure experiments, L. maximus reduced the feeding carolinianus laid about 40% more eggs in sympatry with A. subfuscus time of and induced weight loss in Ariolimax columbianus , and reduced than in allopatry ( Paustian, 2010 ) . Surprisingly, and in contrast to the time spent on courtship and growth by A. ater ( Rollo, 1983b ). these results, A. subfuscus has previously been considered a relatively Both the last two species also spent substantially more time climbing aggressive slug species ( Rollo & Wellington, 1979 ; Paustian, 2010 ). the walls of the enclosure when kept together with L. maximus than As is the case for research on slugs, only a few studies demonstrate when kept alone, a behaviour that may be interpreted as a way to interspecific effects on mortality and reproduction rates in snails. escape aggression. Arion ater and Ariolimax columbianus , on the other Interspecific density dependence has been observed at high densi- hand, did not affect each other’s activity and growth rates ( Rollo, ties of Cepaea snails, and the mucus trails of Theba pisana have been 1983b ). Limax maximus also seems to displace both A. ater and Arion observed to reduce the survival of Cernuella virgata ( Baker, 2021 ), in- vulgaris in arena experiments ( Winter, Ørmen & Bøckman, 2009 ). dicating that interspecific interactions can affect the population dy- Effects on the activity patterns of interspecific competition have namics of terrestrial gastropods. Contrastingly, in a study of several also been identified as playing a role in vitrinid semi-slugs. Adult small-bodied grassland snails, in which the effects of habitat frag- vitrinids in regions where they coexist with limacid slugs are active mentation on population dynamics, local extinction and habitat re- only during late autumn and winter, whereas in regions without li- colonization were investigated, Stoll, Oggier & Baur (2009) did not macids, these semi-slugs are active throughout the year ( Hausdorf, find any evidence of interspecific competition. 2001 ). It has been suggested that shelters for egg laying and resting, which are close to food resources, constitute a limiting factor for Effects on activity, movement, feeding and growth terrestrial slugs and the availability of these resources may thus relate to competition ( Paustian, 2010 ). In the enclosure experi- The adjustment of feeding and movement behaviour in response ments discussed earlier, both A. ater and Ariolimax columbianus pre- to external and internal cues is pivotal for terrestrial gastropods to ferred shelters located close to food sources when in allopatry, successfully complete their life cycles. Abiotic conditions, as well but were displaced by L. maximus during the entire study period as the presence of con- and heterospecifics, may mediate activity 3 J. WATZ AND D. NYQVIST ( Ariolimax columbianus ) or during the mating period of L. maximus ( A. mainly at high altitudes, whereas in places without limacids, vit- ater ) ( Rollo & Wellington, 1979 ; Rollo, 1983b ). Contrastingly, Cook rinids are not restricted to these areas and can be found also at low (1981) showed that L. maximus did not exclude L. flavus , Limacus mac- altitudes. Likely as a consequence of narrower realized niches, vit- ulatus or Lehmannia marginata from an artificial resting shelter. rinid semi-slugs have not diversified where their ranges overlap with Interference competition is not exclusive to direct aggressive con- those of limacids. Moreover, Hausdorf (2001) referred to two exam- test behaviour and indirect interference has also been reported for ples of vitrinids that have colonized new islands in Macaronesia and slugs. For example, O’Hanlon et al . (2020) showed that Lehmannia East Africa lacking limacid slugs and indicated that these vitrinids marginata avoided mucus trails from G. maculosus . A similar effect of showed evidence of competitive release and increased diversifica- Lehmannia marginata mucus on G. maculosus was not found. Although tion. no evidence of direct aggressive interactions between species was On the local scale, negative associations have been found be- observed, this aversion to mucus trails acts as an indirect media- tween several terrestrial slug species. Examples include between G. tor of interference competition. Conversely, mucus trails can attract maculosus and Lehmannia marginata in field plots in Ireland ( O’Hanlon other individuals, and in choice experiments with Deroceras laeve , et al ., 2020 ) and between L. maximus and large arionids in Norway slugs spent more time in areas pretreated with mucus trails from ( Ørmen, Winter & Bøckman, 2010 ). There are also several cases of conspecifics than in areas without mucus ( Jordaens et al ., 2003 ). no (or positive) associations, for example between P. carolinianus , M. In follow-up experiments, no difference was observed regardless of mutabilis and A. subfuscus ( Paustian, 2010 ). whether mucus came from conspecifics or from Deroceras reticulatum Interspecific effects on distribution, on both local and large or Deroceras panormitanum . scales, have been studied more extensively in snails than in slugs. In addition to studies on the effects of interspecific competition Lack of co-occurrence, in combination with overlapping distribu- among slugs on activity, feeding, movement and growth, there are tion, may indicate interspecific competitive displacement, and such several arena-experiment- and field-based studies on this topic patterns have been observed for several snail species combinations involving terrestrial snails. Interspecific density-dependent growth ( Mumladze, 2014 ; Hoxha et al ., 2019 ). For several groups of snails, (as strong as or stronger than the magnitude of intraspecific density niche separation has been seen as indirect evidence of (historic) in- dependence) has been observed in several snail species ( Cameron terspecific competition ( Baur, Baur & Fröberg, 1994 ; Chiba, 1999 ; & Carter, 1979 ; Tattersfield, 1981 ; Baur & Baur, 1990 ; Campbell von Oheimb et al ., 2018 ). For example, Kimura & Chiba (2010) et al ., 2015 ). Interspecific snail interactions have also been seen combined experimental and field studies to show that the aggres- to reduce feeding ( Smallridge & Kirby, 1988 ; Dörler et al. , 2021 ), sive attacks of Euhadra quaesita on Euhadra peliomphala affected the growth ( Smallridge & Kirby, 1988 ; Kimura & Chiba, 2010 ) and growth of the latter species, which was found to be displaced in activity ( Dan & Bailey, 1982 ; Smallridge & Kirby, 1988 ), as well the wild. Survey data showed that E. peliomphala was displaced from as to cause habitat displacement in enclosure experiments ( Tilling, the ground-level habitats it occupied in allopatry to higher, above- 1985 ). As in slugs, the mechanism behind the negative effect of one ground habitats in the vegetation when in sympatry with E. quaesita . snail species on another has been attributed to direct aggressive Approaching the same phenomenon from the opposite perspective, interactions ( Kimura & Chiba, 2010 ) or to the indirect effect Parent & Crespi (2009) showed that for the endemic snail fauna of of mucus trails ( Cameron & Carter, 1979 ; Dan & Bailey, 1982 ; Galápagos, the number of local congeners was negatively related Smallridge & Kirby, 1988 ; Baker, 2021 ). Studies of snails show no to intraspecific phenotypic variation. This result indicates that in- effects on growth ( Perry & Arthur, 1991 ; Bloch & Willig, 2009 ), terspecific competition may play an important role in niche sepa- activity ( Cowie & Jones, 1987 ; Bull et al. , 1992 ) and dispersal ( Baur, ration and that competitive release can lead to rapid adaptive ra- 1993 ) arising from interspecific interactions. Naturally, the same diation in terrestrial gastropods. In contrast, several geographically species combinations may be found to compete or not to compete, and taxonomically diverse studies have found no evidence of any depending on the context and parameters tested (e.g. Tilling, 1985 ; interspecific effects on distribution ( Cameron & Cook, 2001 ; Bloch Cowie & Jones, 1987 ). Lastly, the individual characteristics of in- & Willig, 2010 ; Horsák et al ., 2014 ; Wronski et al. , 2014 ). teracting animals might also affect the outcome of the competitive interactions ( Campbell et al. , 2015 ). DISCUSSION Effects on habitat use and geographical distribution The available literature on interspecific competition among slug Microhabitat separation, as shown, for example, in studies of the species is relatively limited. Many studies indicate competitive inter- vertical distributions of A. ater , Arion fasciatus , Arion hortensis , Arion in- action between two species, but fail to provide strong experimental termedius , A. subfuscus , D. reticulatum and Tandonia budapestensis ( Hunter, evidence for its existence. For interspecific competition to occur, 1966 ; Jennings & Barkham, 1979 ), may be caused by interspecific there are three prerequisites ( Dhondt, 2012 ): (1) the two species competition. However, as a direct comparison between the micro- must share a resource; (2) intraspecific competition for this resource habitat use of slugs in the presence and absence of potential com- has to occur; and (3) the resource must be limiting. When these petitors is lacking, no inference can be drawn as to whether the prerequisites are fulfilled, interspecific competition can be shown separation is caused by different habitat preferences or interspecific in one of three ways: (1) resource use by one species reduces the competitive exclusion. In the USA, introduced A. subfuscus and the availability of the resource for the other species; (2) the presence of native taxa P. carolinianus and Megapallifera mutabilis live sympatrically. individuals of one species reduces the fitness (or a proxy for fitness, Niche overlap between these three species was found to occur only such as growth, survival or reproductive output) of members of the between A. subfuscus and P. carolinianus ( Paustian & Barbosa, 2012 ). other species; or (3) the density and distribution of one species are The co-occurrence of these two species, despite their niche overlap, negatively affected by the presence of the other species. Generally, indicates that interspecific competitive interactions between them interspecific competition is considered to be important when its are weak or absent. effects exceed those of intraspecific competition, thus potentially Habitat exclusion and local extinction caused by interspecific having both ecological and evolutionary implications. Studying competition (or in some cases hybridization; Zemanova, Knop & such interactions may help us to understand or predict patterns Heckel, 2017 ) may in the long run influence large-scale spatial of, for example, habitat exclusion, local extinction and invasion of distribution and macroevolution. Hausdorf (2001) showed that in- alien species. Experiments must, however, be carefully designed terspecific competition between limacid slugs and vitrinid semi- to demonstrate or test the existence and strength of interspecific slugs has indeed affected the distribution and radiation of vitrinids. competition, with the inclusion of suitable treatments and controls. In regions where species of both groups are found, vitrinids exist Ideally, experiments should include single-species treatments and 4 SLUG COMPETITION treatments with individuals of one species being added, as well as and dominant (e.g. Limax maximus ) could negatively affect other slug substituted, at different densities of the other species (i.e. response species within its new range and thereby alter local ecosystems. In surface experiments sensu Inouye, 2001 ). In the publications studied agriculture and garden systems, this could either increase or de- for this review, such an experimental design was lacking. crease crop damage, depending on which species are negatively af- Interspecific competition affecting survival, reproduction, move- fected ( Dörler et al. , 2021 ). Competition between slug species does ment and activity has clearly been demonstrated in laboratory not appear to be affecting population development in general, but experiments of a few slug species. The occurrence of interspe- in the specific cases when competition is strong, different pest man- cific competition seems, however, to be species specific, and many agement strategies may affect the competitive outcome ( Zhao et al. , species combinations that were investigated did not reveal any neg- 2017 ) and, thus, influence their success rates. Thus, farmers and ative effects of the presence of heterospecifics. For most of the re- gardeners may benefit from considering competitive interactions in viewed studies, it is difficult to distinguish between exploitation and their integrated pest management by, for example, minimizing the interference competition as the source of the interspecific competi- adverse effects on beneficial competitors ( Moon, 1980 ). tive effects. All clear examples of interspecific competition in slugs, however, were apparently cases of interference competition medi- ated by aggressive interactions ( Rollo & Wellington, 1979 ; Rollo, SUPPLEMENTARY MATERIAL 1983a , b ) or of aversion to mucus trails ( O’Hanlon et al ., 2020 ). Conversely, exploitation competition likely has limited importance Supplementary material is available at Journal of Molluscan Studies in terrestrial slugs, although feeding rates can differ between sym- online. patric species ( Hoxha et al ., 2019 ; Dörler et al ., 2021 ). The effects of interspecific competition between terrestrial gas- tropods are potentially understudied, and particularly studies of the effects on mortality and reproduction are lacking. These in- ACKNOWLEDGEMENTS teractions possibly play a minor role in population dynamics, and This work was supported by the Royal Swedish Academy of the lack of publications may partly be caused by the “file-drawer Agriculture and Forestry (grant no. GFS2020-0042). We thank effect” arising from negative results ( Rosenthal, 1979 ). Yet, there Jonas Roth for valuable comments on an earlier version of the are undoubtedly examples of pairs of species in which one species manuscript. causes the mortality, has a negative effect on the reproduction, and causes diet and activity changes of the other species, at least under certain environmental conditions. 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Interspecific competition among terrestrial slugs

Watz, Johan; Nyqvist, Daniel
Journal of Molluscan Studies , Volume 88 (2): 1 – Apr 4, 2022
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Journal of The Malacological Society of London Molluscan Studies Journal of Molluscan Studies (2022) 88 : eyac007. https://doi.org/10.1093/mollus/eyac007 Published online 4 April 2022 Interspecific competition among terrestrial slugs 1 2 Johan Watz and Daniel Nyqvist River Ecology and Management Research Group (RivEM), Department of Environmental and Life Sciences, Karlstad University, Karlstad, Sweden; and Department of Environment, Land and Infrastructure Engineering, Politecnico di Torino, Turin, Italy Correspondence: J. Watz; e-mail: johan.watz@kau.se (Received 2 August 2021; editorial decision 22 November 2021) ABSTRACT Interspecific competition among terrestrial gastropods has previously been considered to have little effect on population dynamics and local distribution. Recent studies, however, demonstrate several cases in which interspecific competition plays a major role in structuring terrestrial gastropod communities. To explore the general importance of interspecific competition for the ecology of slugs, we conducted a semi-systematic literature review, synthesizing available peer-reviewed literature relating interspecific interactions to the fol- lowing: (1) mortality and reproduction; (2) activity, movement, feeding and growth; and (3) habitat use and geographical distribution of slugs. To support the literature on slugs, we also reviewed literature on terres- trial snails. The body of available literature is relatively limited, but the effect of interspecific competition on survival, reproduction, movement and activity has clearly been demonstrated in laboratory experiments for different slug species. The occurrence of interspecific competition seems, however, to be species specific, and no negative effects due to the presence of heterospecifics have been reported for many of the species com- binations investigated to date. Most of the studies demonstrating interspecific effects between slug species involved interference from a few aggressive species (mainly Limax maximus as the aggressor). In addition, sev- eral correlative studies have indicated that in terrestrial gastropods, habitat use and geographical distribution might be mediated by interspecific competition. Further, well-designed experiments are needed to explore the general importance of interspecific competition among slugs, potentially with a focus on interactions between invasive and native species, where the lack of a shared evolutionary history and niche separation may increase the intensity of competition. Such experimental studies may produce information that has implications for the conservation of native species, as well as for management of invasive pests, because interspecific competition may result in local extinction of vulnerable species and influence the possibility of non-native species establishing invasive populations in new areas. INTRODUCTION interspecific competition among slugs, an animal group containing many serious and increasingly widespread (occurring worldwide in Interspecific competition reduces fitness among members of differ- some cases) pests of agricultural and horticultural crops ( Douglas ent species that use or defend shared limited resources ( Gustafsson, & Tooker, 2012 ; Cameron, 2016 ). 1987 ), and the characteristics of this biotic interaction can mediate Passive dispersal through human transport of plants and soil has coexistence and influence the evolution of the species involved. facilitated invasions of alien slugs into new areas far from their natu- In some cases, interspecific competition results in niche differen- ral range. Some of these species have become serious pests on crops, tiation, spatial or temporal displacement from a habitat, or local with substantial economic costs in the form of production loss and extinction. The competitive mechanisms underlying these effects pest control programmes (see reviews by South, 1992 ; Barker, 2002 ; are either exploitation, where resource use leads to depletion for Cameron, 2016 ). The introduction of alien slugs creates new com- other individuals, or interference, where individuals directly or binations of sympatric species, and the biotic interactions among indirectly prevent others from using the resource ( Barker, 2002 ; these species may have far-reaching ecological consequences, Dhondt, 2012 ). Understanding the mechanisms and predicting with implications for the design of integrated pest management the outcomes of competition between species may be critical, programmes. both for managing problematic, undesirable pests and for con- Although heavily debated, competition has been shown to shape serving vulnerable and desirable species. The aim of this review arthropod pest communities ( Stewart, 1996 ; Reitz & Trumble, is to synthesize the published scientific literature that addresses 2002 ), and among phytophagous insects, the evidence for its © The Author(s) 2022. Published by Oxford University Press on behalf of The Malacological Society of London. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Review Article J. WATZ AND D. NYQVIST Figure 1. A schematic figure showing the screening of papers on interspecific competition among terrestrial gastropods. Numbers within parentheses indicate the number of papers. importance is now indisputable ( Kaplan & Denno, 2007 ). Inter- petition NOT (marine OR freshwater)]”. This resulted in 786 pub- specific competition among terrestrial gastropods has previously lications (Fig. 1 ). In a first screening of titles and abstracts, 739 pub- been considered to have little effect on population dynamics and lications were excluded (the focus of these was typically on plant or local distribution ( South, 1992 ; Horsák, Zelený & Hájek, 2014 ; parasite ecology, sperm competition, or freshwater and marine gas- Cameron, 2016 ), and it has been reasoned that shelter and food tropods). The remaining 47 papers were read in detail, with 23 pub- resources should not constitute limiting factors ( N emec ˇ et al ., 2021 ). lications that lacked original data or were not relevant to our study Contrastingly, recent studies have demonstrated that interspecific being excluded. When reading the publications that we included competition plays a major role in structuring terrestrial gastropod (and their reference lists) and browsing the recent papers that had communities ( von Oheimb et al ., 2018 ) and is a significant factor cited them, we found 19 additional relevant publications that we when conserving vulnerable species ( O’Hanlon, Fahy & Gormally, had missed using our search string. These publications were also in- 2020 ) and managing pests ( Baker, 2021 ). Moreover, the underly- cluded in our study (i.e. ‘snowballed’). Thus, in total we reviewed 43 ing mechanisms (i.e. behaviours demonstrating exploitation of re- publications (Fig. 1 ; Supplementary Material Table S1); 16 of these sources and direct and indirect interference) that may lead to in- had information on slugs, whereas 27 focused exclusively on snails. terspecific competition among slugs and snails have been known for long (e.g. Cameron & Carter, 1979 ; Rollo, 1983a ; Baur & Baur, RESULTS 1990 ). The existing body of literature exploring the ecology and evo- Of the 16 slug papers included in our review, 8 investigated the out- lution of terrestrial gastropods has focused mainly on snails, owing come of potential competition through the study of slug distribu- partly to rich collections of shells ( Cameron, 2016 ). Here, we focus tion, 7 were based on experiments (often testing a particular com- on the reported outcomes and underlying mechanisms of interspe- petitive mechanism) and 1 described both laboratory experiments cific competition among slugs, but in cases where such information and the mapping of wild slugs. Five of the eight experimental pa- is lacking, we include available data from snails. Our aim is to ex- pers studying slug interactions found evidence of competition. Four plore the general importance of interspecific competition for the of these included non-native Limax maximus , whereas one included ecology of slugs. Specifically, we use a semi-systematic approach the interaction between the arguably native Geomalacus maculosus and ( Snyder, 2019 ) to categorize and synthesize information from pub- Lehmannia marginata . lished papers on the basis of three types of effects: (1) mortality and reproduction; (2) activity, movement, feeding and growth; and (3) habitat use and geographical distribution. Effects on mortality and reproduction Only a few studies have examined how interspecific competition directly affects the mortality rates and reproductive output of dif- ferent slug species. The most studied competitive interactions are MATERIAL AND METHODS those that include L. maximus and its negative effect on other species The Web of Science Core Collection was used for the literature (Fig. 2 ). In a series of enclosure experiments involving the non- search, with access to the following databases: Arts & Humanities natives L. maximus and Arion ater , and the native Ariolimax columbianus , Citation Index (1975–present), Conference Proceedings Citation interspecific competition affected survival, the number of eggs laid, Index—Science (1990–present), Conference Proceedings Citation egg size, the number of egg batches ( Rollo, 1983a ) and access Index—Social Science & Humanities (1990–present), Emerging to egg-laying habitat ( Rollo & Wellington, 1979 ). A common fac- Sources Citation Index (2015–present), Science Citation Index Ex- tor across the interspecific interactions was that the aggressive L. panded (1900–present) and Social Sciences Citation Index (1956– maximus reduced the performance of one or both of the other present). We used the search string “[(slug* OR snail*) AND com- species. Mortality was high for both A. ater and Ariolimax columbianus 2 SLUG COMPETITION Figure 2. A leopard slug Limax maximus interacting with a Spanish slug Arion vulgaris . Direct interference competition mediated by aggressive behaviour from leopard slugs has been reported in several studies. during August, coinciding with high temperatures and increased patterns. When interspecific competition strongly influences these aggressiveness of L. maximus. Late in the season, Ariolimax columbianus patterns, we expect niche separation, displacement or local extinc- also experienced increased mortality in sympatry with A. ater ; the tion. There are studies that indicate feeding niche separation (e.g. cause for this seems to have not been direct competition but the between L. maximus , Lehmannia marginata , Limax flavus and Limacus dying off of the semelparous A. ater after egg laying, with the decay- maculatus ; Cook & Radford, 1988 ) as well as those indicating little or ing carcasses being a source of pathogens ( Rollo, 1983a ). Thus, the no separation ( N emec ˇ et al ., 2021 ). However, experimental studies negative effect of A. ater on Ariolimax columbianus in the enclosure is with manipulated treatments to simulate allopatry vs sympatry are likely not important in nature. In addition, both A. ater and Arioli- needed to disentangle whether observed niche separation in feeding max columbianus produced fewer eggs, whereas A. ater also produced is caused by competition or simply represents different adaptations. smaller eggs and fewer egg batches in sympatry with L. maximus Aggression in slugs varies with species, size and season. Rollo & than in allopatry . Limax maximus , on the other hand, produced dou- Wellington (1979) studied direct interactions among several terres- ble the number of eggs in sympatry with the two other species as trial gastropods and no agonistic behaviours were seen during win- it did in allopatry. Between A. ater and Ariolimax columbianus (both ter, when instead individuals were seen to aggregate. Aggressive in- dominated by L. maximus ), no significant interspecific effects on re- teractions peaked in August, coinciding with the egg-laying season. production were observed. Limax maximus and, to some extent, A. subfuscus were aggressive, at- Similarly, in an enclosure experiment, involving Philomycus car- tacking and even pursuing other slugs (Fig. 2 ), especially during the olinianus and Arion subfuscus , no negative effects on P. carolinianus of reproductive period. interspecific competition (compared to intraspecific competition) Our review of the literature shows that L. maximus also plays were seen on the number of eggs laid. Instead, when food and shel- a central role in the interspecific effects relating to activity and ter were abundant (but not when these resources were limited), P. growth. In enclosure experiments, L. maximus reduced the feeding carolinianus laid about 40% more eggs in sympatry with A. subfuscus time of and induced weight loss in Ariolimax columbianus , and reduced than in allopatry ( Paustian, 2010 ) . Surprisingly, and in contrast to the time spent on courtship and growth by A. ater ( Rollo, 1983b ). these results, A. subfuscus has previously been considered a relatively Both the last two species also spent substantially more time climbing aggressive slug species ( Rollo & Wellington, 1979 ; Paustian, 2010 ). the walls of the enclosure when kept together with L. maximus than As is the case for research on slugs, only a few studies demonstrate when kept alone, a behaviour that may be interpreted as a way to interspecific effects on mortality and reproduction rates in snails. escape aggression. Arion ater and Ariolimax columbianus , on the other Interspecific density dependence has been observed at high densi- hand, did not affect each other’s activity and growth rates ( Rollo, ties of Cepaea snails, and the mucus trails of Theba pisana have been 1983b ). Limax maximus also seems to displace both A. ater and Arion observed to reduce the survival of Cernuella virgata ( Baker, 2021 ), in- vulgaris in arena experiments ( Winter, Ørmen & Bøckman, 2009 ). dicating that interspecific interactions can affect the population dy- Effects on the activity patterns of interspecific competition have namics of terrestrial gastropods. Contrastingly, in a study of several also been identified as playing a role in vitrinid semi-slugs. Adult small-bodied grassland snails, in which the effects of habitat frag- vitrinids in regions where they coexist with limacid slugs are active mentation on population dynamics, local extinction and habitat re- only during late autumn and winter, whereas in regions without li- colonization were investigated, Stoll, Oggier & Baur (2009) did not macids, these semi-slugs are active throughout the year ( Hausdorf, find any evidence of interspecific competition. 2001 ). It has been suggested that shelters for egg laying and resting, which are close to food resources, constitute a limiting factor for Effects on activity, movement, feeding and growth terrestrial slugs and the availability of these resources may thus relate to competition ( Paustian, 2010 ). In the enclosure experi- The adjustment of feeding and movement behaviour in response ments discussed earlier, both A. ater and Ariolimax columbianus pre- to external and internal cues is pivotal for terrestrial gastropods to ferred shelters located close to food sources when in allopatry, successfully complete their life cycles. Abiotic conditions, as well but were displaced by L. maximus during the entire study period as the presence of con- and heterospecifics, may mediate activity 3 J. WATZ AND D. NYQVIST ( Ariolimax columbianus ) or during the mating period of L. maximus ( A. mainly at high altitudes, whereas in places without limacids, vit- ater ) ( Rollo & Wellington, 1979 ; Rollo, 1983b ). Contrastingly, Cook rinids are not restricted to these areas and can be found also at low (1981) showed that L. maximus did not exclude L. flavus , Limacus mac- altitudes. Likely as a consequence of narrower realized niches, vit- ulatus or Lehmannia marginata from an artificial resting shelter. rinid semi-slugs have not diversified where their ranges overlap with Interference competition is not exclusive to direct aggressive con- those of limacids. Moreover, Hausdorf (2001) referred to two exam- test behaviour and indirect interference has also been reported for ples of vitrinids that have colonized new islands in Macaronesia and slugs. For example, O’Hanlon et al . (2020) showed that Lehmannia East Africa lacking limacid slugs and indicated that these vitrinids marginata avoided mucus trails from G. maculosus . A similar effect of showed evidence of competitive release and increased diversifica- Lehmannia marginata mucus on G. maculosus was not found. Although tion. no evidence of direct aggressive interactions between species was On the local scale, negative associations have been found be- observed, this aversion to mucus trails acts as an indirect media- tween several terrestrial slug species. Examples include between G. tor of interference competition. Conversely, mucus trails can attract maculosus and Lehmannia marginata in field plots in Ireland ( O’Hanlon other individuals, and in choice experiments with Deroceras laeve , et al ., 2020 ) and between L. maximus and large arionids in Norway slugs spent more time in areas pretreated with mucus trails from ( Ørmen, Winter & Bøckman, 2010 ). There are also several cases of conspecifics than in areas without mucus ( Jordaens et al ., 2003 ). no (or positive) associations, for example between P. carolinianus , M. In follow-up experiments, no difference was observed regardless of mutabilis and A. subfuscus ( Paustian, 2010 ). whether mucus came from conspecifics or from Deroceras reticulatum Interspecific effects on distribution, on both local and large or Deroceras panormitanum . scales, have been studied more extensively in snails than in slugs. In addition to studies on the effects of interspecific competition Lack of co-occurrence, in combination with overlapping distribu- among slugs on activity, feeding, movement and growth, there are tion, may indicate interspecific competitive displacement, and such several arena-experiment- and field-based studies on this topic patterns have been observed for several snail species combinations involving terrestrial snails. Interspecific density-dependent growth ( Mumladze, 2014 ; Hoxha et al ., 2019 ). For several groups of snails, (as strong as or stronger than the magnitude of intraspecific density niche separation has been seen as indirect evidence of (historic) in- dependence) has been observed in several snail species ( Cameron terspecific competition ( Baur, Baur & Fröberg, 1994 ; Chiba, 1999 ; & Carter, 1979 ; Tattersfield, 1981 ; Baur & Baur, 1990 ; Campbell von Oheimb et al ., 2018 ). For example, Kimura & Chiba (2010) et al ., 2015 ). Interspecific snail interactions have also been seen combined experimental and field studies to show that the aggres- to reduce feeding ( Smallridge & Kirby, 1988 ; Dörler et al. , 2021 ), sive attacks of Euhadra quaesita on Euhadra peliomphala affected the growth ( Smallridge & Kirby, 1988 ; Kimura & Chiba, 2010 ) and growth of the latter species, which was found to be displaced in activity ( Dan & Bailey, 1982 ; Smallridge & Kirby, 1988 ), as well the wild. Survey data showed that E. peliomphala was displaced from as to cause habitat displacement in enclosure experiments ( Tilling, the ground-level habitats it occupied in allopatry to higher, above- 1985 ). As in slugs, the mechanism behind the negative effect of one ground habitats in the vegetation when in sympatry with E. quaesita . snail species on another has been attributed to direct aggressive Approaching the same phenomenon from the opposite perspective, interactions ( Kimura & Chiba, 2010 ) or to the indirect effect Parent & Crespi (2009) showed that for the endemic snail fauna of of mucus trails ( Cameron & Carter, 1979 ; Dan & Bailey, 1982 ; Galápagos, the number of local congeners was negatively related Smallridge & Kirby, 1988 ; Baker, 2021 ). Studies of snails show no to intraspecific phenotypic variation. This result indicates that in- effects on growth ( Perry & Arthur, 1991 ; Bloch & Willig, 2009 ), terspecific competition may play an important role in niche sepa- activity ( Cowie & Jones, 1987 ; Bull et al. , 1992 ) and dispersal ( Baur, ration and that competitive release can lead to rapid adaptive ra- 1993 ) arising from interspecific interactions. Naturally, the same diation in terrestrial gastropods. In contrast, several geographically species combinations may be found to compete or not to compete, and taxonomically diverse studies have found no evidence of any depending on the context and parameters tested (e.g. Tilling, 1985 ; interspecific effects on distribution ( Cameron & Cook, 2001 ; Bloch Cowie & Jones, 1987 ). Lastly, the individual characteristics of in- & Willig, 2010 ; Horsák et al ., 2014 ; Wronski et al. , 2014 ). teracting animals might also affect the outcome of the competitive interactions ( Campbell et al. , 2015 ). DISCUSSION Effects on habitat use and geographical distribution The available literature on interspecific competition among slug Microhabitat separation, as shown, for example, in studies of the species is relatively limited. Many studies indicate competitive inter- vertical distributions of A. ater , Arion fasciatus , Arion hortensis , Arion in- action between two species, but fail to provide strong experimental termedius , A. subfuscus , D. reticulatum and Tandonia budapestensis ( Hunter, evidence for its existence. For interspecific competition to occur, 1966 ; Jennings & Barkham, 1979 ), may be caused by interspecific there are three prerequisites ( Dhondt, 2012 ): (1) the two species competition. However, as a direct comparison between the micro- must share a resource; (2) intraspecific competition for this resource habitat use of slugs in the presence and absence of potential com- has to occur; and (3) the resource must be limiting. When these petitors is lacking, no inference can be drawn as to whether the prerequisites are fulfilled, interspecific competition can be shown separation is caused by different habitat preferences or interspecific in one of three ways: (1) resource use by one species reduces the competitive exclusion. In the USA, introduced A. subfuscus and the availability of the resource for the other species; (2) the presence of native taxa P. carolinianus and Megapallifera mutabilis live sympatrically. individuals of one species reduces the fitness (or a proxy for fitness, Niche overlap between these three species was found to occur only such as growth, survival or reproductive output) of members of the between A. subfuscus and P. carolinianus ( Paustian & Barbosa, 2012 ). other species; or (3) the density and distribution of one species are The co-occurrence of these two species, despite their niche overlap, negatively affected by the presence of the other species. Generally, indicates that interspecific competitive interactions between them interspecific competition is considered to be important when its are weak or absent. effects exceed those of intraspecific competition, thus potentially Habitat exclusion and local extinction caused by interspecific having both ecological and evolutionary implications. Studying competition (or in some cases hybridization; Zemanova, Knop & such interactions may help us to understand or predict patterns Heckel, 2017 ) may in the long run influence large-scale spatial of, for example, habitat exclusion, local extinction and invasion of distribution and macroevolution. Hausdorf (2001) showed that in- alien species. Experiments must, however, be carefully designed terspecific competition between limacid slugs and vitrinid semi- to demonstrate or test the existence and strength of interspecific slugs has indeed affected the distribution and radiation of vitrinids. competition, with the inclusion of suitable treatments and controls. In regions where species of both groups are found, vitrinids exist Ideally, experiments should include single-species treatments and 4 SLUG COMPETITION treatments with individuals of one species being added, as well as and dominant (e.g. Limax maximus ) could negatively affect other slug substituted, at different densities of the other species (i.e. response species within its new range and thereby alter local ecosystems. In surface experiments sensu Inouye, 2001 ). In the publications studied agriculture and garden systems, this could either increase or de- for this review, such an experimental design was lacking. crease crop damage, depending on which species are negatively af- Interspecific competition affecting survival, reproduction, move- fected ( Dörler et al. , 2021 ). Competition between slug species does ment and activity has clearly been demonstrated in laboratory not appear to be affecting population development in general, but experiments of a few slug species. The occurrence of interspe- in the specific cases when competition is strong, different pest man- cific competition seems, however, to be species specific, and many agement strategies may affect the competitive outcome ( Zhao et al. , species combinations that were investigated did not reveal any neg- 2017 ) and, thus, influence their success rates. Thus, farmers and ative effects of the presence of heterospecifics. For most of the re- gardeners may benefit from considering competitive interactions in viewed studies, it is difficult to distinguish between exploitation and their integrated pest management by, for example, minimizing the interference competition as the source of the interspecific competi- adverse effects on beneficial competitors ( Moon, 1980 ). tive effects. All clear examples of interspecific competition in slugs, however, were apparently cases of interference competition medi- ated by aggressive interactions ( Rollo & Wellington, 1979 ; Rollo, SUPPLEMENTARY MATERIAL 1983a , b ) or of aversion to mucus trails ( O’Hanlon et al ., 2020 ). Conversely, exploitation competition likely has limited importance Supplementary material is available at Journal of Molluscan Studies in terrestrial slugs, although feeding rates can differ between sym- online. patric species ( Hoxha et al ., 2019 ; Dörler et al ., 2021 ). The effects of interspecific competition between terrestrial gas- tropods are potentially understudied, and particularly studies of the effects on mortality and reproduction are lacking. These in- ACKNOWLEDGEMENTS teractions possibly play a minor role in population dynamics, and This work was supported by the Royal Swedish Academy of the lack of publications may partly be caused by the “file-drawer Agriculture and Forestry (grant no. GFS2020-0042). We thank effect” arising from negative results ( Rosenthal, 1979 ). Yet, there Jonas Roth for valuable comments on an earlier version of the are undoubtedly examples of pairs of species in which one species manuscript. causes the mortality, has a negative effect on the reproduction, and causes diet and activity changes of the other species, at least under certain environmental conditions. 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Published: Apr 4, 2022

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