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Is fern endozoochory widespread among fern-eating herbivores?


Endozoochory is an important dispersal mechanism for seed plants and has recently been demonstrated to occur also in spore plants, such as ferns, which are commonly consumed by herbivores. However, it is not known whether fern species from particular habitats are differentially preferred by herbivores and whether their spores differ in their ability to survive the gut passage of herbivores. Such differences would suggest adaptation to endozoochorous dispersal, as it is known for seed plants. Moreover, it is unclear whether herbivore species differ in their efficiency to disperse fern spores. In a factorial experiment, we fed fertile leaflets of 13 fern species from different forest and open habitats to three polyphagous herbivore species and recorded the germination of spores from feces after 46 and 81 days. Fern spores germinated in 66 % of all samples after 46 days. At this stage, germination success differed among fern and herbivore species, but was independent of the ferns’ habitat. Interestingly, after 81 days fern spores germinated in 85 % of all samples and earlier significant differences in germination success among fern and herbivore species were not sustained. The overall high germination success and the absence of differences among fern species from different habitats together with the consistency across three tested herbivores strongly imply endozoochorous dispersal to be a taxonomically widespread phenomenon among fern-eating herbivores, which all might act as potential dispersal vectors.

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  • Arosa ML, Ramos JA, Quintanilla D, Brown LG (2010) First report of fern (Culcita macrocarpa) spore consumption by a small mammal (Apodemus sylvaticus). Mamm Biol 75:115–121

    Google Scholar 

  • Balick MJ, Furth DG, Cooper-Driver G (1978) Biochemical and evolutionary aspects of arthropod predation on ferns. Oecologia 35:55–89

    Article  Google Scholar 

  • Baur B, Baur H, Roesti C, Roesti D (2006) Die Heuschrecken der Schweiz. Haupt Verlag, Bern, p 352

    Google Scholar 

  • Boch S, Prati D, Werth S, Rüetschi J, Fischer M (2011) Lichen endozoochory by snails. PLoS One 6(4):e18770

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  • Boch S, Berlinger M, Fischer M, Knop E, Nentwig W, Türke M, Prati D (2013) Fern and bryophyte endozoochory by slugs. Oecologia 172:817–822

    PubMed  Article  Google Scholar 

  • Boch S, Fischer M, Knop E, Allan E (2015) Endozoochory by slugs can increase bryophyte establishment and species richness. Oikos 124:331–336

    Article  Google Scholar 

  • Bråthen KA, González VT, Iversen M, Killengreen S, Ravolainen VT, Ims RA, Yoccoz NG (2007) Endozoochory varies with ecological scale and context. Ecography 30:308–320

    Article  Google Scholar 

  • Brouwers NC, Newton AC, Bailey S (2011) The dispersal ability of wood cricket (Nemobius sylvestris) (Orthoptera: Gryllidae) in a wooded landscape. Eur J Entomol 108:117–125

    Article  Google Scholar 

  • Carlisle DB, Ellis PE (1968) Bracken and locust ecdysones: their effects on molting in the desert locust. Science 159:1472–1474

    PubMed  CAS  Article  Google Scholar 

  • Cooper-Driver GA (1990) Defense strategies in bracken, Pteridium aquilinum (L.) Kuhn. Ann Mo Bot Gard 77:281–286

    Article  Google Scholar 

  • Cousens R, Dytham C, Law R (2008) Dispersal in plants: a population perspective. Oxford University Press, Oxford, p 221

    Book  Google Scholar 

  • Crawley MJ (1983) Herbivory: the dynamics of animal-plant inetractions. Blackwell Scientific Publications, Oxford, p 437

    Google Scholar 

  • Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Glime JM (2013) Invertebrates. Chapter 4. In: Glime JM (ed) Bryophyte Ecology. Volume 2. Bryological Interaction. [online]. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Accessed 19 Nov 2015

  • Guiden P, Gorchov DL, Nielsen C, Schauber E (2015) Seed dispersal of an invasive shrub, Amur honeysuckle (Lonicera maackii), by white-tailed deer in a fragmented agricultural-forest matrix. Plant Ecol 216:939–950

    Article  Google Scholar 

  • Herrera CM (2001) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Science, Oxford, pp 185–208

    Google Scholar 

  • Hickey JR, Flynn RW, Buskirk SW, Gerow KG, Wilson MF (1999) An evaluation of a mammalian predator, Martes americana, as a disperser of seeds. Oikos 87:499–508

    Article  Google Scholar 

  • Kempel A, Nater P, Fischer M, van Kleunen M (2013) Plant-microbe-herbivore interactions in invasive and non-invasive alien plant species. Funct Ecol 27:498–508

    Article  Google Scholar 

  • Kreft H, Jetz W, Mutke J, Barthlott W (2010) Contrasting environmental and regional effects on global pteridophyte and seed plant diversity. Ecography 33:408–419

    Article  Google Scholar 

  • Landolt E, Bäumler B, Erhardt A et al (2010) Flora Indicativa. Ökologische Zeigerwerte und biologische Kennzeichen zur Flora der Schweiz und der Alpen. 2nd edn. Haupt Verlag, Bern, p 378

  • Lauber K, Wagner G, Gygax A (2012) Flora Helvetica, 5th edn. Haupt Verlag, Bern, p 1656

    Google Scholar 

  • Lind EM, Borer E, Seabloom E et al (2013) Life-history constraints in grassland plant species: a growth–defence trade-off is the norm. Ecol Lett 16:513–521

    PubMed  Article  Google Scholar 

  • Mauricio R, Bowers D (1990) Do caterpillars disperse their damage?: larval foraging behavior of two herbivores, Euphydryas phaeton (Nymphalidae) and Pieris rapae (Pieridae). Ecol Entomol 15:153–161

    Article  Google Scholar 

  • Mesipuu M, Shefferson RP, Kull T (2009) Weather and herbivores influence fertility in the endangered fern Botrychium multifidum (S.G. Gmel.) Rupr. Plant Ecol 203:23–31

    Article  Google Scholar 

  • Page CN (2002) Ecological strategies in fern evolution: a neopteridological overview. Rev Palaeobot Palyno 119:1–33

    Article  Google Scholar 

  • Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416

    Article  Google Scholar 

  • Pangua E, Lindsay S, Dyer A (1994) Spore germination and gamtophyte development in three species of Asplenium. Ann Bot 73:587–593

    Article  Google Scholar 

  • Pfenninger M, Weigand A, Bálint M, Klussmann-Kolb A (2014) Misperceived invasion: the Lusitanian slug (Arion lusitanicus auct. non-Mabille or Arion vulgaris Moquin-Tandon 1855) is native to Central Europe. Evol Appl 7:702–713

    PubMed  PubMed Central  Article  Google Scholar 

  • Qintanilla LG, Pajarón S, Pangua E, Amigo J (2008) Effect of temperature on germination in northernmost populations of Culcita macrocarpa and Woodwardia radicans. Plant Biol 2:612–617

    Article  Google Scholar 

  • Rojas JC, Wyatt TD, Birch MC (2000) Flight and oviposition behavior toward different host plant species by the cabbage moth, Mamestra brassicae (L.) (Lepidoptera. Noctuidae). J Insect Behav 13:247–254

    Article  Google Scholar 

  • Sawamura M, Kawakita A, Kato M (2009) Fern-spore-feeder interaction in temperate forests in Japan: sporing phenology and spore-feeding insect community. Am J Bot 96:594–604

    PubMed  Article  Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353

    PubMed  Article  Google Scholar 

  • Smith BL (1997) The toxicity of bracken fern (genus Pteridium) to animals and its relevance to man. In: D’Mello JPF (ed) Handbook of plant and fungal toxicants. CRC Press, Boca Raton, pp 63–76

    Google Scholar 

  • Speiser B (2001) Food and feeding behaviour. In: Barker GM (ed) The biology of terrestrial mollusks. CABI, Wallingford, pp 259–288

    Chapter  Google Scholar 

  • Traveset A, Rodríguez-Pérez J, Pías B (2008) Seed trait changes in dispersers’ guts and consequences for germination and seedling growth. Ecology 89:95–106

    PubMed  Article  Google Scholar 

  • Türke M, Heinze E, Andreas K et al (2010) Seed consumption and dispersal in ant-dispersed plants by slugs. Oecologia 163:681–693

    PubMed  Article  Google Scholar 

  • Türke M, Andreas K, Gossner MM et al (2012) Are gastropods, rather than ants, important dispersers of seeds of myrmecochorous forest herbs? Am Nat 179:124–131

    PubMed  Article  Google Scholar 

  • Tutin TG, Burges NA, Chater AO et al (1993) Flora Europaea, Psilotaceae to platanaceae. Vol 1. Cambridge University Press, Cambridge, p 581

  • van Tooren BF, During HJ (1988) Viable plant diaspores in the guts of earthworms. Acta Bot Neerl 37:181–185

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

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We thank Korinna Esfeld, Yvonne Künzi, and Janique Bertschi for assistance, Leon Westerd for providing Mamestra brassicae egg batches and the editor William E. Rogers as well as two anonymous reviewers for their constructive comments and their efforts with this manuscript.

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Correspondence to Steffen Boch.

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Communicated by William E. Rogers.

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Boch, S., Berlinger, M., Prati, D. et al. Is fern endozoochory widespread among fern-eating herbivores?. Plant Ecol 217, 13–20 (2016).

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  • Dispersal
  • Invertebrate
  • Mutualism
  • Plant-animal interaction
  • Pteridophyta
  • Spore germination