Seed handling behaviours of native and invasive seed-dispersing ants differentially influence seedling emergence in an introduced plant
TL;DR: Handling by ants may be a benefit of myrmecochory and favourable nest conditions may enhance emergence, and functional differences in ant species may result in different outcomes for plant partners.
Abstract: Myrmecochory, or ant-mediated seed dispersal, is an important ecological interaction in which ants benefit by gaining nutrition from lipid-rich elaiosomes attached to seeds and plants benefit from having their seeds dispersed away from parent plants. Most research on the benefits of myrmecochory focuses on primary dispersal, in which ants move seeds to nests, or secondary dispersal, in which ants deposit intact seeds in middens after consuming elaiosomes. Less is known about how ants handle seeds inside nests and if handling influences plant fitness.
The seed handling behaviours of a native ‘keystone disperser’, Aphaenogaster rudis s.l., and an invasive seed-disperser, Myrmica rubra L., on an introduced herb, Chelidonium majus L., were compared. We conducted a greenhouse experiment to test if handling by ants, manual removal of elaiosomes, or no handling (controls) influenced seedling emergence. Colony-level differences in handling behaviours and plant responses were also examined.
Aphaenogaster rudis retained seeds inside nests longer than M. rubra, but there was no difference in the amount of elaiosome removed by the two species. There was no difference in the proportion of seedlings that emerged among treatments, but seedlings emerged earlier when handled by A. rudis. Additionally, more seedlings emerged and seedlings emerged earlier the longer seeds were retained inside ant nests.
This study suggests that handling by ants may be a benefit of myrmecochory. This is probably not due to elaiosome removal; rather favourable nest conditions may enhance emergence. Also, functional differences in ant species may result in different outcomes for plant partners.
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TL;DR: A review of the state of the art of alien plant research with emphasis on conceptual advances and knowledge gains on general patterns and drivers, biotic interactions, and evolution is given in this paper.
Abstract: We review the state of the art of alien plant research with emphasis on conceptual advances and knowledge gains on general patterns and drivers, biotic interactions, and evolution. Major advances i...
131 citations
Cites background from "Seed handling behaviours of native ..."
...…the 502 invasive ant Myrmica rubra, as well as the native ant Aphaenogaster rudis, contribute to seed 503 dispersal and thus spread of the invasive plant Chelodonium majus, the presence of a seed-dispersing invasive ant promoted dominance of invasive alien plants over natives (Prior et al. 2014)....
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TL;DR: It is shown that strongly interacting introduced mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species (‘invasional meltdown’) if invasive partners strongly interact.
Abstract: Generalized mutualisms are often predicted to be resilient to changes in partner identity. Variation in mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species (‘invasional meltdown’) if invasive partners strongly interact. Here we show how invasion by a seed-dispersing ant (Myrmica rubra) promotes recruitment of a co-introduced invasive over native ant-dispersed (myrmecochorous) plants. We created experimental communities of invasive (M. rubra) or native ants (Aphaenogaster rudis) and invasive and native plants and measured seed dispersal and plant recruitment. In our mesocosms, and in laboratory and field trials, M. rubra acted as a superior seed disperser relative to the native ant. By contrast, previous studies have found that invasive ants are often poor seed dispersers compared with native ants. Despite belonging to the same behavioural guild, seed-dispersing ants were not functionally redundant. Instead, native and invasive ants had strongly divergent effects on plant communities: the invasive plant dominated in the presence of the invasive ant and the native plants dominated in the presence of the native ant. Community changes were not due to preferences for coevolved partners: variation in functional traits of linked partners drove differences. Here, we show that strongly interacting introduced mutualists can be major drivers of ecological change.
58 citations
TL;DR: It is found that elaiosome robbing by slugs reduced seed dispersal by ants, especially in mesocosms with A. rudis, which picks up seeds more slowly than M. rubra, suggesting that invasive slugs can have profound negative effects on Seed dispersal mutualisms.
Abstract: Plant-animal mutualisms, such as seed dispersal, are often vulnerable to disruption by invasive species. Here, we show for the first time how a non-ant invasive species negatively affects seed dispersal by ants. We examined the effects of several animal species that co-occur in a temperate deciduous forest-including native and invasive seed-dispersing ants (Aphaenogaster rudis and Myrmica rubra, respectively), an invasive slug (Arion subfuscus), and native rodents-on a native myrmecochorous plant, Asarum canadense. We experimentally manipulated ant, slug, and rodent access to seed depots and measured seed removal. We also video-recorded depots to determine which other taxa interact with seeds. We found that A. rudis was the main disperser of seeds and that A. subfuscus consumed elaiosomes without dispersing seeds. Rodent visitation was rare, and rodent exclusion had no significant effect on seed or elaiosome removal. We then used data obtained from laboratory and field mesocosm experiments to determine how elaiosome robbing by A. subfuscus affects seed dispersal by A. rudis and M. rubra. We found that elaiosome robbing by slugs reduced seed dispersal by ants, especially in mesocosms with A. rudis, which picks up seeds more slowly than M. rubra. Taken together, our results show that elaiosome robbing by an invasive slug reduces seed dispersal by ants, suggesting that invasive slugs can have profound negative effects on seed dispersal mutualisms.
19 citations
Cites background or result from "Seed handling behaviours of native ..."
...We follow previous studies (Lubertazzi 2012; Prior et al. 2014, 2015) in referring to our study species as A. rudis, but recognize that it is likely Aphaenogaster picea or an undescribed species in this complex....
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...M. rubra disperses seeds of many myrmecochorous plants in both its native (Gorb and Gorb 1999; Fokuhl et al. 2007) and introduced ranges (Prior et al. 2014, 2015)....
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TL;DR: Fruit dehiscence of myrmecochorous plants and peak ant seed dispersal activity occur asynchronously and elaiosome robbing by slugs increased late in the season and thus may disproportionately affect plants with late-dehiscing fruits.
Abstract: Premise of the study Phenological mismatch has received attention in plant-pollinator interactions, but less so in seed dispersal mutualisms. We investigated whether the seasonal availability of myrmecochorous seeds is well matched to the seasonal activity patterns of seed-dispersing ants. Methods We compared seasonal timing of seed removal by a keystone seed-dispersing ant, Aphaenogaster rudis, and fruit dehiscence of several species of plants whose seeds it disperses in a deciduous forest in southern Ontario, Canada. We examined the timing of elaiosome "robbing" by the nonnative slug Arion subfuscus and tested whether seed removal by ants declines in response to supplementation with additional elaiosome-bearing seeds (ant "satiation"). Key results Seed removal from experimental depots peaked early in the season for all plant species and correlated with temperature. In contrast, elaiosome robbing by slugs increased late in the season and thus may disproportionately affect plants with late-dehiscing fruits. Ant colonies removed seeds at similar rates regardless of seed supplementation, indicating that satiation likely does not impact seasonal patterns of seed dispersal in this system. Fruits of the five myrmecochorous plant species in our study dehisced at discrete intervals throughout the season, with minimal overlap among species. Peak dehiscence did not overlap with peak seed removal for any plant species. Conclusions Fruit dehiscence of myrmecochorous plants and peak ant seed dispersal activity occur asynchronously. Whether future climate warming will shift ant and plant phenologies in ways that have consequences for seed dispersal remains an open question.
11 citations
TL;DR: Seed manipulation by ants can play a key role in seed germination through two main behaviours: elaiosome detachment and seed scarification, which have only been quantified independently.
Abstract: 1. Seed manipulation by ants can play a key role in seed germination through two main behaviours: elaiosome detachment and seed scarification. Despite the fact that these behaviours are commonplace, their effects have only been quantified independently, and their consequences on seed germination remain controversial.
10 citations
References
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TL;DR: Technique non parametrique pour la signification statistique de tables de tests utilisees dans les etudes sur l'evolution notamment.
Abstract: Technique non parametrique pour la signification statistique de tables de tests utilisees dans les etudes sur l'evolution notamment
14,666 citations
"Seed handling behaviours of native ..." refers methods in this paper
...Differences among treatments were assessed by comparing P -values using sequential Bonferroni (Rice, 1989; Crawley, 2007)....
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Book•
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01 Jan 2007
TL;DR: The R Book is the first comprehensive reference manual for the R language, including practical guidance and full coverage of the graphics facilities, and introduces the advantages of the R environment, detailing its applications in a wide range of disciplines.
Abstract: The high-level language of R is recognized as one of the most powerful and flexible statistical software environments, and is rapidly becoming the standard setting for quantitative analysis, statistics and graphics. R provides free access to unrivalled coverage and cutting-edge applications, enabling the user to apply numerous statistical methods ranging from simple regression to time series or multivariate analysis. Building on the success of the authors bestselling Statistics: An Introduction using R, The R Book is packed with worked examples, providing an all inclusive guide to R, ideal for novice and more accomplished users alike. The book assumes no background in statistics or computing and introduces the advantages of the R environment, detailing its applications in a wide range of disciplines. Provides the first comprehensive reference manual for the R language, including practical guidance and full coverage of the graphics facilities. Introduces all the statistical models covered by R, beginning with simple classical tests such as chi-square and t-test. Proceeds to examine more advance methods, from regression and analysis of variance, through to generalized linear models, generalized mixed models, time series, spatial statistics, multivariate statistics and much more. The R Book is aimed at undergraduates, postgraduates and professionals in science, engineering and medicine. It is also ideal for students and professionals in statistics, economics, geography and the social sciences.
6,975 citations
"Seed handling behaviours of native ..." refers methods in this paper
...Differences among treatments were assessed by comparing P -values using sequential Bonferroni (Rice, 1989; Crawley, 2007)....
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...In both analyses, we incorporated time-specific hazard distributions (weibull) given that removal rates were not constant over time (Crawley, 2007)....
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...Model comparisons and model significance were tested with χ2 tests (Crawley, 2007)....
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...Significance was tested with a χ2 test (Crawley, 2007)....
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DOI•
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29 Sep 2022
TL;DR: The R Book is the first comprehensive reference manual for the R language, including practical guidance and full coverage of the graphics facilities, and introduces the advantages of the R environment, detailing its applications in a wide range of disciplines.
Abstract: The high-level language of R is recognized as one of the most powerful and flexible statistical software environments, and is rapidly becoming the standard setting for quantitative analysis, statistics and graphics. R provides free access to unrivalled coverage and cutting-edge applications, enabling the user to apply numerous statistical methods ranging from simple regression to time series or multivariate analysis. Building on the success of the authors bestselling Statistics: An Introduction using R, The R Book is packed with worked examples, providing an all inclusive guide to R, ideal for novice and more accomplished users alike. The book assumes no background in statistics or computing and introduces the advantages of the R environment, detailing its applications in a wide range of disciplines. Provides the first comprehensive reference manual for the R language, including practical guidance and full coverage of the graphics facilities. Introduces all the statistical models covered by R, beginning with simple classical tests such as chi-square and t-test. Proceeds to examine more advance methods, from regression and analysis of variance, through to generalized linear models, generalized mixed models, time series, spatial statistics, multivariate statistics and much more. The R Book is aimed at undergraduates, postgraduates and professionals in science, engineering and medicine. It is also ideal for students and professionals in statistics, economics, geography and the social sciences.
6,732 citations
TL;DR: The view that tightly coevolved, plant‐vertebrate seed dispersal systems are extremely rare is supported and perspectives on mutualisms in screening protocols will improve the ability to predict whether a given plant species could invade a particular habitat.
Abstract: Many introduced plant species rely on mutualisms in their new habitats to overcome barriers to establishment and to become naturalized and, in some cases, invasive. Mutualisms involving animal-mediated pollination and seed dispersal, and symbioses between plant roots and microbiota often facilitate invasions. The spread of many alien plants, particularly woody ones, depends on pollinator mutualisms. Most alien plants are well served by generalist pollinators (insects and birds), and pollinator limitation does not appear to be a major barrier for the spread of introduced plants (special conditions relating to Ficus and orchids are described). Seeds of many of the most notorious plant invaders are dispersed by animals, mainly birds and mammals. Our review supports the view that tightly coevolved, plant-vertebrate seed dispersal systems are extremely rare. Vertebrate-dispersed plants are generally not limited reproductively by the lack of dispersers. Most mycorrhizal plants form associations with arbuscular mycorrhizal fungi which, because of their low specificity, do not seem to play a major role in facilitating or hindering plant invasions (except possibly on remote islands such as the Galapagos which are poor in arbuscular mycorrhizal fungi). The lack of symbionts has, however, been a major barrier for many ectomycorrhizal plants, notably for Pinus spp. in parts of the southern hemisphere. The roles of nitrogen-fixing associations between legumes and rhizobia and between actinorhizal plants and Frankia spp. in promoting or hindering invasions have been virtually ignored in the invasions literature. Symbionts required to induce nitrogen fixation in many plants are extremely widespread, but intentional introductions of symbionts have altered the invasibility of many, if not most, systems. Some of the world's worst invasive alien species only invaded after the introduction of symbionts. Mutualisms in the new environment sometimes re-unite the same species that form partnerships in the native range of the plant. Very often, however, different species are involved, emphasizing the diffuse nature of many (most) mutualisms. Mutualisms in new habitats usually duplicate functions or strategies that exist in the natural range of the plant. Occasionally, mutualisms forge totally novel combinations, with profound implications for the behaviour of the introduced plant in the new environment (examples are seed dispersal mutualisms involving wind-dispersed pines and cockatoos in Australia; and mycorrhizal associations involving plant roots and fungi). Many ecosystems are becoming more susceptible to invasion by introduced plants because: (a) they contain an increasing array of potential mutualistic partners (e.g. generalist frugivores and pollinators, mycorrhizal fungi with wide host ranges, rhizobia strains with infectivity across genera); and (b) conditions conductive for the establishment of various alien/alien synergisms are becoming more abundant. Incorporating perspectives on mutualisms in screening protocols will improve (but not perfect) our ability to predict whether a given plant species could invade a particular habitat.
1,382 citations
"Seed handling behaviours of native ..." refers background in this paper
...This suggests that both native and invasive ants could contribute to the spread of C. majus; an expected response for introduced plants involved in diffuse mutualisms (Richardson et al., 2000)....
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...majus; an expected response for introduced plants involved in diffuse mutualisms (Richardson et al., 2000)....
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