Complicating a complex ecosystem function: the controversial role of gastropods in a myremcochorous seed dispersal mutualism

Several thousand plant species worldwide are adapted to seed dispersal by ants (myrmecochory) and they are a dominant part of many plant communities, as is the case in European beech forests. Ants, however, are often rare in beech forests. The consequence of this paradox might be that the majority of seeds fall prey to seed predators and myrmecochores migrate mostly by vegetative spread. I compared ant, gastropod and myrmecochore abundance data from beech forests and I conducted seed removal experiments. Gastropods contributed most to the seed removal. Therefore I offered seeds to four gastropod species in the laboratory and I collected red slugs (Arion rufus) in beech forests and searched for seeds in their feces. I tested their dispersal potential by assessing germination rates of slug-defecated seeds and distances red slugs move in the field. The cover and species richness of myrmecochores in beech forests was negatively correlated with the abundance of ants but positively with the abundance of gastropods, supporting my assumption of a discrepancy in the presence of plants and their ant-dispersers. Gastropods were most important for seed removal in my removal experiments, while rodents and insects including ants played only a minor role. Laboratory feeding experiments showed that gastropods consumed seeds of all plant species offered. Swallowed seeds were defecated undamaged and germinated as well as control seeds. I also discovered seeds in the feces of wild-caught red slugs. Thus, gastropods may act as seed dispersers. Red slugs moved up to 14.6 m in 15 hours, the median gut passage time of seeds, and thus, might transport seeds even further than ants. The results of my experiments indicate that myrmecochores might lack ants as their seed dispersers in beech forests, but they also suggest that ants could be substituted by gastropods

Fern and bryophyte endozoochory by slugs

Endozoochory plays a prominent role for the dispersal of seed plants, and dispersal vectors are well known. However, for taxa such as ferns and bryophytes, endozoochory has only been suggested anecdotally but never tested in controlled experiments. We fed fertile leaflets of three ferns and capsules of four bryophyte species to three slug species. We found that, overall, spores germinated from slug feces in 57.3% of all 89 fern and in 51.3% of all 117 bryophyte samples, showing that the spores survived gut passage of slugs. Moreover, the number of samples within which spores successfully germinated did not differ among plant species but varied strongly among slug species. This opens new ecological perspectives suggesting that fern and bryophyte endozoochory by gastropods is a so-far-overlooked mode of dispersal, which might increase local population sizes of these taxa by spore deposition on suitable substrate

Weeds and endangered herbs have unforeseen dispersal helpers in the agri-environment: gastropods and earthworms

Agri-environmental schemes involving organic farming or set-aside management aim at promoting biodiversity and restoring ecosystem functioning in agrarian landscapes. Application of pesticides in these crop fields is strongly regulated facilitating the spread of weeds but also allowing for the establishment of endangered herbs and a variety of animals. Recent studies found gastropods and earthworms to be legitimate dispersers of seeds of wild plants. We assumed that both groups also play a significant role in the spread and establishment of wild plants within crop fields. Therefore, we are conducting a series of experiments in three different study systems on (1) the role of earthworms and gastropods as dispersers of rare herbs and weeds in an organic rye field in Germany, (2) the seed feeding behavior of gastropods of plants sown in fallow ground in Switzerland, and (3) weed dispersal in irrigated rice fields by golden apple snails in the Philippine

Do Invasive Earthworms Affect the Functional Traits of Native Plants?

As ecosystem engineers, invasive earthworms are one of the main drivers of plant community changes in North American forests previously devoid of earthworms. One explanation for these community changes is the effects of earthworms on the reproduction, recruitment, and development of plant species. However, few studies have investigated functional trait responses of native plants to earthworm invasion to explain the mechanisms underlying community changes. In a mesocosm (Ecotron) experiment, we set up a plant community composed of two herb and two grass species commonly found in northern North American forests under two earthworm treatments (presence vs. absence). We measured earthworm effects on above- and belowground plant biomass and functional traits after 3 months of experiment. Our results showed that earthworm presence did not significantly affect plant community biomass and cover. Furthermore, only four out of the fifteen above- and belowground traits measured were affected by earthworm presence. While some traits, such as the production of ramets, the carbon and nitrogen content of leaves, responded similarly between and within functional groups in the presence or absence of earthworms, we observed opposite responses for other traits, such as height, specific leaf area, and root length within some functional groups in the presence of earthworms. Plant trait responses were thus species-specific, although the two grass species showed a more pronounced response to earthworm presence with changes in their leaf traits than herb species. Overall, earthworms affected some functional traits related to resource uptake abilities of plants and thus could change plant competition outcomes over time, which could be an explanation of plant community changes observed in invaded ecosystems

Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees

Recent research shows that earthworms can alter defense traits of plants against herbivores and pathogens by affecting soil biochemistry. Yet, the effects of invasive earthworms on defense traits of native plants from previously earthworm-free ecosystems as well as the consequences for multitrophic interactions are virtually unknown. Here we use a combination of an observational study and a complementary experimental study to investigate the effects of invasive earthworms on leaf defense traits, herbivore damage and pathogen infection in two poplar tree species (Populus balsamifera and Populus tremuloides) native to North American boreal forests. Our observational study showed that earthworm invasion was associated with enhanced leaf herbivory (by leaf-chewing insects) in saplings of both tree species. However, we only detected significant shifts in the concentration of chemical defense compounds in response to earthworm invasion for P. balsamifera. Specifically, leaf phenolic concentrations, including salicinoids and catechin, were lower in P. balsamifera from earthworm-invaded sites. Our experimental study confirmed an earthworm-induced reduction in leaf defense levels in P. balsamifera for one of the defense compounds, tremulacin. The experimental study additionally showed that invasive earthworms reduced leaf dry matter content, potentially increasing leaf palatability, and enhanced susceptibility of trees to infection by a fungal pathogen, but not to aphid infestation, in the same tree species. Synthesis. Our results show that invasive earthworms can decrease the concentrations of some chemical defense compounds in P. balsamifera, which could make them susceptible to leaf-chewing insects. Such potential impacts of invasive earthworms are likely to have implications for tree survival and competition, native tree biodiversity and ecosystem functioning

Termite sensitivity to temperature affects global wood decay rates.

Deadwood is a large global carbon store with its store size partially determined by biotic decay. Microbial wood decay rates are known to respond to changing temperature and precipitation. Termites are also important decomposers in the tropics but are less well studied. An understanding of their climate sensitivities is needed to estimate climate change effects on wood carbon pools. Using data from 133 sites spanning six continents, we found that termite wood discovery and consumption were highly sensitive to temperature (with decay increasing >6.8 times per 10°C increase in temperature)-even more so than microbes. Termite decay effects were greatest in tropical seasonal forests, tropical savannas, and subtropical deserts. With tropicalization (i.e., warming shifts to tropical climates), termite wood decay will likely increase as termites access more of Earth's surface

Gastropod Seed Dispersal: An Invasive Slug Destroys Far More Seeds in Its Gut than Native Gastropods

Seed dispersal is one of the most important mechanisms shaping biodiversity, and animals are one of the key dispersal vectors. Animal seed dispersal can directly or indirectly be altered by invasive organisms through the establishment of new or the disruption of existing seed dispersal interactions. So far it is known for a few gastropod species that they ingest and defecate viable plant seeds and consequently act as seed dispersers, referred to as gastropodochory. In a multi-species experiment, consisting of five different plant species and four different gastropod species, we tested with a fully crossed design whether gastropodochory is a general mechanism across native gastropod species, and whether it is altered by the invasive alien slug species Arion lusitanicus. Specifically, we hypothesized that a) native gastropod species consume the seeds from all tested plant species in equal numbers (have no preference), b) the voracious invasive alien slug A. lusitanicus – similarly to its herbivore behaviour – consumes a higher amount of seeds than native gastropods, and that c) seed viability is equal among different gastropod species after gut passage. As expected all tested gastropod species consumed all tested plant species. Against our expectation there was a difference in the amount of consumed seeds, with the largest and native mollusk Helix pomatia consuming most seeds, followed by the invasive slug and the other gastropods. Seed damage and germination rates did not differ after gut passage through different native species, but seed damage was significantly higher after gut passage through the invasive slug A. lusitanicus, and their germination rates were significantly reduced

Species, Diaspore Volume and Body Mass Matter in Gastropod Seed Feeding Behavior

<div><p>Background</p><p>Seed dispersal of ant-dispersed plants (myrmecochores) is a well studied ecosystem function. Recently, slugs have been found to act as seed dispersers of myrmecochores. The aim of our study was to (1) further generalize the finding that gastropods feed on seeds of myrmecochores and hence may act as seed dispersers, (2) to test whether gastropod body mass and the volume of diaspores have an influence on the seed dispersal potential.</p><p>Methodology and Principal Findings</p><p>We assessed the seed dispersal potential of four slug and snail species with a set of seven myrmecochorous plant species from seven different plant families common to Central European beech forests. Diaspores differed in shape and size. Gastropods differed in their readiness to feed on diaspores and in the proportion of seeds that were swallowed as a whole, and this readiness generally decreased with increasing diaspore size. Smaller Arionid slugs (58 mm body length; mean) mostly fed on the elaiosome but also swallowed small diaspores and therefore not only act as elaiosome consumers, a nutrient rich appendage on myrmecochorous diaspores, but may also disperse seeds. Large Arionid slugs (>100 mm body length) swallowed diaspores of all sizes. Diaspores swallowed by gastropods were defecated without damage. Within-species variability in body size also affect seed dispersal potential, as larger individuals of the red slug (<i>Arion rufus</i>) swallowed more diaspores of wood anemone (<i>Anemone nemorosa</i>) than smaller ones.</p><p>Conclusions and Significance</p><p>Our results help to generalize the finding that gastropods consume and potentially disperse seeds of myrmecochores. The dispersal potential of gastropods is strongly influenced by diaspore size in relation to gastropod size.</p></div

Epiphytic bacteria on lettuce affect the feeding behavior of an invasive pest slug

Plant–animal interactions are not isolated pairwise relationships but are always accompanied by diverse assemblages of microbes. Additional to direct effects of microorganisms on their hosts, recent investigations demonstrated that bacteria associated with plants can modify the behavior of organisms of higher trophic levels. However, in the context of herbivory, functions of non-phytopathogenic bacteria colonizing leaf surfaces remain understudied. This study showed that naturally occurring epiphytic bacteria affect the feeding behavior of a generalist herbivore. Epiphytic bacteria isolated from leaves of Lactuca sativa var. capitata were screened for their potential to influence feeding choices of the slug Arion vulgaris. Cultivated bacteria were inoculated in artificial food substrates or on sterile leaves of gnotobiotic lettuce plants and were offered to slugs in different behavioral bioassays. A large proportion of bacterial strains tested induced behavioral alterations in the feeding choices of slugs. Behavioral responses of slugs were further modified by antibiotic treatment of slugs prior to choice tests indicating that both bacteria associated with plants and animals affect plant–animal interactions. Our results emphasize the important role of bacteria in plant–animal interactions and suggest a prominent role of bacteria in herbivory in natural, horticultural, and agricultural systems

Relationship of diaspore volume and the dispersal potential.

<p>Relationship between diaspore volume and the dispersal potential of diaspores by gastropods described as the number of diaspores swallowed (Ns) of the number of diaspores offered (No) to all gastropod individuals. Results are given as mean ± standard error (SE).</p