Niche partitioning and indication of ontogenetic niche shifts in forest slugs according to stable isotopes

Niche partitioning and indication of ontogenetic niche shifts in forest slugs according to stable... The turnover of slug assemblages suggests niche partitioning along gradients of microclimatic conditions and food availability (Kappes, 2006; Kappes and Schilthuizen, 2014). Within forests, most slugs such as those of the genus Arion feed on the leaf litter, but usually consume only a small portion of the annual input (e.g. Seifert and Shutov, 1981; Theenhaus and Schaefer, 1999). Some slug species can locally turn over up to 7.4% of the annual leaf litter input (Gupta and Oli, 1998). The attractiveness of microhabitats such as woody debris to slugs and snails is hypothesized to be partly caused by the presence of deadwood-associated fungi and microbial biofilms (Fog, 1979; Kappes, 2006). It appears that some slugs may forage on lichens and fungi (Frömming, 1954), and some generalists include varying portions of green plants, fruits, dead animals or faeces in their diets (Boback, 1952; Frömming, 1954; Richter, 1979). As a result, the trophic position of slugs is often difficult to identify. One method to visualize the breadth and overlap of nutritional niches makes use of the stable isotopic signature of the animals. For example, Schmidt et al. (2004) illustrated that stable isotopes can be used to characterize nutritional niches of field slugs and Meyer and Yeung (2011) analysed the isotopic composition of selected native and invasive gastropods on Hawaii. These authors included in their analyses samples of leaf litter and green plants as likely food items. Here, we provide stable isotopic data from different native forest slugs. As our study was performed on slugs from closed-canopy forests devoid of a herb layer, green plants were not included in our approach, but we sampled fungi as potential food sources. Environmental samples and slugs were collected in late autumn 2012 in beech-dominated forests northwest of Niedeggen, Eifel Hills, Germany. Environmental samples were leaf litter (n = 2), leaf litter and deadwood overgrown with visible fungal hyphae (each n = 1) and the fruiting body of a Basidiomycete (n = 1). The forests had a high canopy closure with no green plants on the forest floor. Slug taxa were Limax cinereoniger Wolf, 1803, Malacolimax tenellus (O. F. Müller, 1774) and Lehmannia marginata (O. F. Müller, 1774) (Limacidae) and Arion rufus (Linnaeus, 1758), A. intermedius Normand, 1852, A. silvaticus Lohmander, 1937 and A. fuscus agg. (Arionidae). All these taxa usually differ in size and colour: L. cinereoniger usually reaches more than 15 cm in length and is of black colour. The other large slug, A. rufus, is over 12 cm long and usually brilliant red when adult, whereas its juveniles are whitish and resemble adults of A. intermedius, which is usually about 3 cm long, more yellowish white and unbanded in the forests under study. Arion silvaticus is up to 4 cm extended and greyish with longitudinal bands, whereas A. fuscus agg. reaches up to 7 cm in length and is yellowish-brown with dark longitudinal bands. Malacolimax tenellus is up to 5 cm long and waxy-translucent yellow, and L. marginata is about 7 cm extended and grey-brown with obscure bands. We sampled three specimens from each taxon with the exception of A. rufus, of which we sampled three juveniles and three adults. Individuals were cooled and finally frozen. Slug tissue (foot muscle) and detritus were dried at 60 °C for more than 48 h before sample preparation and stable isotope analysis of δ13C and δ15N at the Stable Isotope Facility of the University of Davis, California. Isotopic signatures were visualized in a biplot. The calculation of isotopic niches is based on a Bayesian approach, especially suitable for small sample sizes. Briefly, a covariance matrix is calculated from the δ13C and δ15N values and its variation estimated by a Markov chain Monte Carlo (MCMC) sampling simulation. Ellipses around isotopic values of each species were calculated with SIBER (Jackson et al., 2011) in R v. 3.0 (R Development Core Team, 2007). Nonoverlapping ellipses indicate dietary differences (Jackson et al., 2011). As indicated by the ellipses, niche differentiation was larger between than within genera (Fig. 1). Lehmannia marginata showed the most extreme isotopic signatures; its highly negative δ15N values are typical of cyanobacteria. Cyanobacteria are symbionts of some lichens, but may also grow on the bark of trees. This result is in line with the well known feeding preferences of L. marginata (e.g. Frömming, 1954). However, L. marginata is not the only slug that is known to consume cyanobacteria. Selective grazing on lichen cephalodia with Nostoc has for example been described for boreal A. fuscus (Asplund and Gauslaa, 2010). Figure 1. View largeDownload slide Biplot of the δ15N and δ13C isotope values of the slugs and environmental samples with leaf litter reference lines and ellipses as drawn by SIBER. Figure 1. View largeDownload slide Biplot of the δ15N and δ13C isotope values of the slugs and environmental samples with leaf litter reference lines and ellipses as drawn by SIBER. The isotopic signatures of the other slug species suggest that they at least partially consume fungal hyphae. The isotopic values support observations by Frömming (1954) that M. tenellus, and to a lesser extent Limax cinereoniger, predominantly consume fungi. The three above-mentioned limacids are typical inhabitants of old-growth forests (Kappes, 2006). In general, isotopic composition of the species of Arion in the studied forests tended to be clustered and to overlap (Fig. 1). Interestingly, ontogenetic niche shifts are indicated in A. rufus. Juvenile A. rufus were somewhat similar to A. intermedius in terms of colour and size, but clearly differed in isotopic signature. It can be speculated that these differences in isotopic composition, and their changes during growth, reflect their occupied niches, i.e. avoidance of competition between parents and offspring on the one hand and offspring and A. intermedius on the other. Alternatively, isotopic differences in body tissue of larger individuals of A. rufus could reflect previous dietary inputs, i.e. seasonal changes in food sources. Interestingly, A. intermedius in a Metrosideros-dominated forest on Hawaii had δ13C −24.1 ± 0.6 and δ15N −4.4 ± 1.6 (Meyer and Yeung, 2011); i.e. slug δ13C was the same (this study: −24.0 ± 0.4) but δ15N was more than two delta-units lower than in our study, though leaf litter δ15N was only about one delta-unit lower in the study of Meyer and Yeung (2011). This difference supports the idea of flexible nutrition as a response to resource availability. Although forest-inhabiting gastropods occasionally feed on a variety of items, such as decaying herbs, fruits or seeds (e.g. Frömming, 1954; Richter, 1979; Türke et al., 2010), most slug species fitted well into the line between leaf litter and fungi. Our study hence suggests that the within-stand distribution pattern of gastropods is partly driven by the presence of (palatable) fungi and that forest slugs, with the exception of L. marginata, participate in a fungus-enhanced detritus food web. Our study therefore demonstrates that high δ15N values do not necessarily indicate predatory feeding, as was assumed for Limax maximus and Oxychilus alliarius (Meyer and Yeung, 2011), but can also originate from fungivory. Given the small sample sizes, our pilot study is generating, rather than testing, hypotheses. Future isotope-based studies should test the assumptions (1) of slow evolutionary niche shifts, with niche differentiation being larger between than within genera and (2) that larger slugs such as A. rufus, which change colour along with size during growth, also change their nutritional niche. To this end, slug sample sizes will need to be increased and a higher variety of environmental samples (such as green plants, leaf litter, beech nuts, faeces of vertebrates, dead invertebrates, fungi and lichens) needs to be included, besides sampling in at least two seasons to monitor dietary shifts. ACKNOWLEDGEMENTS Lutz Dalbeck (Biologische Station Düren) kindly helped with site selection. We thank B. Rüttgers (Untere Landschaftsbehörde Düren) and R. Jansen (Regionalforstamt Rureifel-Jülicher Börde) for permissions. Katrin Friebe and Erich Biermann (University of Cologne) helped to process the isotope samples. We also would like thank two anonymous reviewers for their constructive comments. REFERENCES Asplund, A. & Gauslaa, Y. 2010. The gastropod Arion fuscus prefers cyanobacterial to green algal parts of the tripartite lichen Nephroma arcticum due to low chemical defence. Lichenologist , 42: 113– 117. Google Scholar CrossRef Search ADS   Boback, A.W. 1952. Zur Frage eines forstlichen Schadens durch die Waldnacktschnecke Arion subfuscus. Journal of Pest Science , 25: 189. Fog, K. 1979. Studies on decomposing wooden stumps II. Statistical studies of snail-microflora relations on stump surfaces. Pedobiologia , 19: 183– 199. Frömming, E. 1954. Biologie der mitteleuropäischen Landgastropoden . Duncker and Humblot, Berlin. Gupta, P.K. & Oli, B.P. 1998. Consumption and assimilation of evergreen oak litter by the slug Anadenus altivagus in Kumaon Himalayan Forests, India. Ecoscience , 5: 494– 501. Google Scholar CrossRef Search ADS   Jackson, A.L., Inger, R., Parnell, A.C. & Bearhop, S. 2011. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology , 80: 595– 602. Google Scholar CrossRef Search ADS PubMed  Kappes, H. 2006. Relations between forest management and slug assemblages (Gastropoda) of deciduous regrowth forests. Forest Ecology and Management , 237: 450– 457. Google Scholar CrossRef Search ADS   Kappes, H. & Schilthuizen, M. 2014. Habitat effects on slug assemblages and introduced species. Journal of Molluscan Studies , 80: 47– 54. Google Scholar CrossRef Search ADS   Meyer, W.M. & Yeung, N.W. 2011. Trophic relationships among terrestrial molluscs in a Hawaiian rain forest: analysis of carbon and nitrogen isotopes. Journal of Tropical Ecology , 27: 441– 445. Google Scholar CrossRef Search ADS   R Development Core Team. 2007. R: a language and environment for statistical computing . R Foundation for Statistical Computing, Vienna, Austria. Richter, K.O. 1979. Aspects of nutrient cycling by Ariolimax columbianus (Mollusca: Arionidae) in Pacific Northwest coniferous forests. Pedobiologia , 19: 60– 74. Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E. & Scrimgeour, C.M. 2004. Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. Pedobiologia , 48: 171– 180. Google Scholar CrossRef Search ADS   Seifert, D.V. & Shutov, S.V. 1981. The consumption of leaf litter by land molluscs. Pedobiologia , 21: 159– 165. Theenhaus, A. & Schaefer, M. 1999. Energetics of the red slug Arion rufus (Gastropoda) and of the gastropod community in a beech forest on limestone. Malacologia , 41: 197– 208. Türke, M., Heinze, E., Andreas, K., Svendsen, S.M., Gossner, M.M. & Weisser, W.W. 2010. Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia , 163: 681– 693. Google Scholar CrossRef Search ADS PubMed  © The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Molluscan Studies Oxford University Press

Niche partitioning and indication of ontogenetic niche shifts in forest slugs according to stable isotopes

Loading next page...
 
/lp/ou_press/niche-partitioning-and-indication-of-ontogenetic-niche-shifts-in-jHqiRsYzcQ
Publisher
Oxford University Press
Copyright
© The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com
ISSN
0260-1230
eISSN
1464-3766
D.O.I.
10.1093/mollus/eyx042
Publisher site
See Article on Publisher Site

Abstract

The turnover of slug assemblages suggests niche partitioning along gradients of microclimatic conditions and food availability (Kappes, 2006; Kappes and Schilthuizen, 2014). Within forests, most slugs such as those of the genus Arion feed on the leaf litter, but usually consume only a small portion of the annual input (e.g. Seifert and Shutov, 1981; Theenhaus and Schaefer, 1999). Some slug species can locally turn over up to 7.4% of the annual leaf litter input (Gupta and Oli, 1998). The attractiveness of microhabitats such as woody debris to slugs and snails is hypothesized to be partly caused by the presence of deadwood-associated fungi and microbial biofilms (Fog, 1979; Kappes, 2006). It appears that some slugs may forage on lichens and fungi (Frömming, 1954), and some generalists include varying portions of green plants, fruits, dead animals or faeces in their diets (Boback, 1952; Frömming, 1954; Richter, 1979). As a result, the trophic position of slugs is often difficult to identify. One method to visualize the breadth and overlap of nutritional niches makes use of the stable isotopic signature of the animals. For example, Schmidt et al. (2004) illustrated that stable isotopes can be used to characterize nutritional niches of field slugs and Meyer and Yeung (2011) analysed the isotopic composition of selected native and invasive gastropods on Hawaii. These authors included in their analyses samples of leaf litter and green plants as likely food items. Here, we provide stable isotopic data from different native forest slugs. As our study was performed on slugs from closed-canopy forests devoid of a herb layer, green plants were not included in our approach, but we sampled fungi as potential food sources. Environmental samples and slugs were collected in late autumn 2012 in beech-dominated forests northwest of Niedeggen, Eifel Hills, Germany. Environmental samples were leaf litter (n = 2), leaf litter and deadwood overgrown with visible fungal hyphae (each n = 1) and the fruiting body of a Basidiomycete (n = 1). The forests had a high canopy closure with no green plants on the forest floor. Slug taxa were Limax cinereoniger Wolf, 1803, Malacolimax tenellus (O. F. Müller, 1774) and Lehmannia marginata (O. F. Müller, 1774) (Limacidae) and Arion rufus (Linnaeus, 1758), A. intermedius Normand, 1852, A. silvaticus Lohmander, 1937 and A. fuscus agg. (Arionidae). All these taxa usually differ in size and colour: L. cinereoniger usually reaches more than 15 cm in length and is of black colour. The other large slug, A. rufus, is over 12 cm long and usually brilliant red when adult, whereas its juveniles are whitish and resemble adults of A. intermedius, which is usually about 3 cm long, more yellowish white and unbanded in the forests under study. Arion silvaticus is up to 4 cm extended and greyish with longitudinal bands, whereas A. fuscus agg. reaches up to 7 cm in length and is yellowish-brown with dark longitudinal bands. Malacolimax tenellus is up to 5 cm long and waxy-translucent yellow, and L. marginata is about 7 cm extended and grey-brown with obscure bands. We sampled three specimens from each taxon with the exception of A. rufus, of which we sampled three juveniles and three adults. Individuals were cooled and finally frozen. Slug tissue (foot muscle) and detritus were dried at 60 °C for more than 48 h before sample preparation and stable isotope analysis of δ13C and δ15N at the Stable Isotope Facility of the University of Davis, California. Isotopic signatures were visualized in a biplot. The calculation of isotopic niches is based on a Bayesian approach, especially suitable for small sample sizes. Briefly, a covariance matrix is calculated from the δ13C and δ15N values and its variation estimated by a Markov chain Monte Carlo (MCMC) sampling simulation. Ellipses around isotopic values of each species were calculated with SIBER (Jackson et al., 2011) in R v. 3.0 (R Development Core Team, 2007). Nonoverlapping ellipses indicate dietary differences (Jackson et al., 2011). As indicated by the ellipses, niche differentiation was larger between than within genera (Fig. 1). Lehmannia marginata showed the most extreme isotopic signatures; its highly negative δ15N values are typical of cyanobacteria. Cyanobacteria are symbionts of some lichens, but may also grow on the bark of trees. This result is in line with the well known feeding preferences of L. marginata (e.g. Frömming, 1954). However, L. marginata is not the only slug that is known to consume cyanobacteria. Selective grazing on lichen cephalodia with Nostoc has for example been described for boreal A. fuscus (Asplund and Gauslaa, 2010). Figure 1. View largeDownload slide Biplot of the δ15N and δ13C isotope values of the slugs and environmental samples with leaf litter reference lines and ellipses as drawn by SIBER. Figure 1. View largeDownload slide Biplot of the δ15N and δ13C isotope values of the slugs and environmental samples with leaf litter reference lines and ellipses as drawn by SIBER. The isotopic signatures of the other slug species suggest that they at least partially consume fungal hyphae. The isotopic values support observations by Frömming (1954) that M. tenellus, and to a lesser extent Limax cinereoniger, predominantly consume fungi. The three above-mentioned limacids are typical inhabitants of old-growth forests (Kappes, 2006). In general, isotopic composition of the species of Arion in the studied forests tended to be clustered and to overlap (Fig. 1). Interestingly, ontogenetic niche shifts are indicated in A. rufus. Juvenile A. rufus were somewhat similar to A. intermedius in terms of colour and size, but clearly differed in isotopic signature. It can be speculated that these differences in isotopic composition, and their changes during growth, reflect their occupied niches, i.e. avoidance of competition between parents and offspring on the one hand and offspring and A. intermedius on the other. Alternatively, isotopic differences in body tissue of larger individuals of A. rufus could reflect previous dietary inputs, i.e. seasonal changes in food sources. Interestingly, A. intermedius in a Metrosideros-dominated forest on Hawaii had δ13C −24.1 ± 0.6 and δ15N −4.4 ± 1.6 (Meyer and Yeung, 2011); i.e. slug δ13C was the same (this study: −24.0 ± 0.4) but δ15N was more than two delta-units lower than in our study, though leaf litter δ15N was only about one delta-unit lower in the study of Meyer and Yeung (2011). This difference supports the idea of flexible nutrition as a response to resource availability. Although forest-inhabiting gastropods occasionally feed on a variety of items, such as decaying herbs, fruits or seeds (e.g. Frömming, 1954; Richter, 1979; Türke et al., 2010), most slug species fitted well into the line between leaf litter and fungi. Our study hence suggests that the within-stand distribution pattern of gastropods is partly driven by the presence of (palatable) fungi and that forest slugs, with the exception of L. marginata, participate in a fungus-enhanced detritus food web. Our study therefore demonstrates that high δ15N values do not necessarily indicate predatory feeding, as was assumed for Limax maximus and Oxychilus alliarius (Meyer and Yeung, 2011), but can also originate from fungivory. Given the small sample sizes, our pilot study is generating, rather than testing, hypotheses. Future isotope-based studies should test the assumptions (1) of slow evolutionary niche shifts, with niche differentiation being larger between than within genera and (2) that larger slugs such as A. rufus, which change colour along with size during growth, also change their nutritional niche. To this end, slug sample sizes will need to be increased and a higher variety of environmental samples (such as green plants, leaf litter, beech nuts, faeces of vertebrates, dead invertebrates, fungi and lichens) needs to be included, besides sampling in at least two seasons to monitor dietary shifts. ACKNOWLEDGEMENTS Lutz Dalbeck (Biologische Station Düren) kindly helped with site selection. We thank B. Rüttgers (Untere Landschaftsbehörde Düren) and R. Jansen (Regionalforstamt Rureifel-Jülicher Börde) for permissions. Katrin Friebe and Erich Biermann (University of Cologne) helped to process the isotope samples. We also would like thank two anonymous reviewers for their constructive comments. REFERENCES Asplund, A. & Gauslaa, Y. 2010. The gastropod Arion fuscus prefers cyanobacterial to green algal parts of the tripartite lichen Nephroma arcticum due to low chemical defence. Lichenologist , 42: 113– 117. Google Scholar CrossRef Search ADS   Boback, A.W. 1952. Zur Frage eines forstlichen Schadens durch die Waldnacktschnecke Arion subfuscus. Journal of Pest Science , 25: 189. Fog, K. 1979. Studies on decomposing wooden stumps II. Statistical studies of snail-microflora relations on stump surfaces. Pedobiologia , 19: 183– 199. Frömming, E. 1954. Biologie der mitteleuropäischen Landgastropoden . Duncker and Humblot, Berlin. Gupta, P.K. & Oli, B.P. 1998. Consumption and assimilation of evergreen oak litter by the slug Anadenus altivagus in Kumaon Himalayan Forests, India. Ecoscience , 5: 494– 501. Google Scholar CrossRef Search ADS   Jackson, A.L., Inger, R., Parnell, A.C. & Bearhop, S. 2011. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology , 80: 595– 602. Google Scholar CrossRef Search ADS PubMed  Kappes, H. 2006. Relations between forest management and slug assemblages (Gastropoda) of deciduous regrowth forests. Forest Ecology and Management , 237: 450– 457. Google Scholar CrossRef Search ADS   Kappes, H. & Schilthuizen, M. 2014. Habitat effects on slug assemblages and introduced species. Journal of Molluscan Studies , 80: 47– 54. Google Scholar CrossRef Search ADS   Meyer, W.M. & Yeung, N.W. 2011. Trophic relationships among terrestrial molluscs in a Hawaiian rain forest: analysis of carbon and nitrogen isotopes. Journal of Tropical Ecology , 27: 441– 445. Google Scholar CrossRef Search ADS   R Development Core Team. 2007. R: a language and environment for statistical computing . R Foundation for Statistical Computing, Vienna, Austria. Richter, K.O. 1979. Aspects of nutrient cycling by Ariolimax columbianus (Mollusca: Arionidae) in Pacific Northwest coniferous forests. Pedobiologia , 19: 60– 74. Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E. & Scrimgeour, C.M. 2004. Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. Pedobiologia , 48: 171– 180. Google Scholar CrossRef Search ADS   Seifert, D.V. & Shutov, S.V. 1981. The consumption of leaf litter by land molluscs. Pedobiologia , 21: 159– 165. Theenhaus, A. & Schaefer, M. 1999. Energetics of the red slug Arion rufus (Gastropoda) and of the gastropod community in a beech forest on limestone. Malacologia , 41: 197– 208. Türke, M., Heinze, E., Andreas, K., Svendsen, S.M., Gossner, M.M. & Weisser, W.W. 2010. Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia , 163: 681– 693. Google Scholar CrossRef Search ADS PubMed  © The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com

Journal

Journal of Molluscan StudiesOxford University Press

Published: Feb 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 12 million articles from more than
10,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Unlimited reading

Read as many articles as you need. Full articles with original layout, charts and figures. Read online, from anywhere.

Stay up to date

Keep up with your field with Personalized Recommendations and Follow Journals to get automatic updates.

Organize your research

It’s easy to organize your research with our built-in tools.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

Monthly Plan

  • Read unlimited articles
  • Personalized recommendations
  • No expiration
  • Print 20 pages per month
  • 20% off on PDF purchases
  • Organize your research
  • Get updates on your journals and topic searches

$49/month

Start Free Trial

14-day Free Trial

Best Deal — 39% off

Annual Plan

  • All the features of the Professional Plan, but for 39% off!
  • Billed annually
  • No expiration
  • For the normal price of 10 articles elsewhere, you get one full year of unlimited access to articles.

$588

$360/year

billed annually
Start Free Trial

14-day Free Trial