Mutualism Disruption Research Articles

Occurrence of arbuscular mycorrhizal herbsis selectively decreased in communities invaded by alien tree <i>Acer negundo</i>

We tested whether one of the consequences of alien plant invasion predicted by the mutualism disruption hypothesis was true in regard to ash-leaved maple (Acer negundo L.). The study aimed to determine whether the occurrence of mycorrhizal and non-mycorrhizal herbs varied similarly or differently in communities with different degrees of A. negundo dominance. We analysed the results of 78 relevés carried out in the Belarusian Polesie, the Middle Volga region and the Middle Urals. In each region, communities with dominance of A. negundo and without it were described. The mycorrhizal status of plant species was determined using the FungalRoot Database. It was found, with an increase in probability of arbuscular mycorrhiza formation, the frequency of those species’ registration was decreased in A. negundo thickets. On the contrary, with an increase in probability of non-mycorrhizal status, the frequency of those species’ registration was increased in A. negundo thickets. Therefore, in communities dominated by A. negundo, the occurrence of arbuscular mycorrhizal herbs was selectively decreased.

The Invasion Ecology of Mutualism

Successful invasive species commonly depend on the establishment of mutualistic interactions with native and nonnative biota. In turn, invasive species can affect native mutualisms and community stability. Here, we examine different forms of mutualist acquisition by invasive species and the causes and consequences of mutualism abandonment for invasion processes. Additionally, we delve into the quantitative and qualitative effects of invaders on native biota via mutualism disruption that can occur through direct and diverse indirect pathways. These effects of invasive species on native biota via mutualistic interactions can often be a consequence of the invaders’ abundance, which should be considered a prime predictor when evaluating the impact of invasive species on native mutualisms and community stability. We propose that the ecological as well as the evolutionary consequences of mutualism disruption and switches caused by invasive species can play crucial roles in determining future biodiversity.

Occurrence of Arbuscular Mycorrhizal Herbs Decreases Selectively in Communities Dominated by Invasive Tree Acer negundo.

We tested whether one of the consequences predicted for alien plant invasion by the mutualism disruption hypothesis was true in the case of the ash-leaved maple Acer negundo L. The study aimed to determine whether the occurrences of mycorrhizal and nonmycorrhizal herbs varied similarly or differently in communities with varying degrees of A. negundo dominance. The analysis included the results of 78 vegetation descriptions carried out in Belarusian Polesia, the Middle Volga region, and the Middle Urals. Communities with or without A. negundo dominance were described in each region. The mycorrhizal status of plant species was determined using the FungalRoot Database. Species that are more likely to form arbuscular mycorrhiza were found to occur less frequently in A. negundo thickets. On the contrary, a higher probability of the nonmycorrhizal status was associated with a lower frequency of detection in A. negundo thickets. Therefore, the occurrence of arbuscular mycorrhizal herbs was found to selectively decrease in communities dominated by A.negundo.

Invasion‐mediated mutualism disruption is evident across heterogeneous environmental conditions and varying invasion intensities

The impact of a biological invasion on native communities is expected to be uneven across invaded landscapes due to differences in local abiotic conditions, invader abundance, and traits and composition of the native community. One way to improve predictive ability about the impact of an invasive species given variable conditions is to exploit known mechanisms driving invasive species' success. Invasive plants frequently exhibit allelopathic traits, which can be directly toxic to plants or indirectly impact them via disruption of root symbionts, including mycorrhizal fungi. The indirect mechanism – mutualism disruption – is predicted to impact plants that rely on mycorrhizas but not affect non‐mycorrhizal plant species. To assess whether invader‐driven mutualism disruption explains observed changes in native plant communities, we analyzed long‐term (1998–2018) plant cover data from forest plots across the state of Illinois. We evaluated native plant communities experiencing a range of abundance of invasive allelopathic garlic mustard Alliaria petiolata and varying environmental conditions. Consistent with the mutualism disruption hypothesis, we showed that as garlic mustard abundance increased over time in 0.25 m2 sampling quadrats, the abundance of mycorrhizal plant species decreased, but non‐mycorrhizal plant species did not. Over space and time, garlic mustard abundance predicted plant abundances and diversity at the quadrat level, but this relationship was not present at a larger scale when quadrats were aggregated within sites. Garlic mustard's impact on the plant community was highly localized, yet it was as important as abiotic variables for predicting local plant diversity. We showed that garlic mustard abundance was a key predictor of patterns of plant diversity across invasion intensity and environmental heterogeneity in a way that is consistent with mutualism disruption. Our work indicates that the mutualism disruption hypothesis can provide generalizable predictions of the impacts of allelopathic invasive plants that are evident at a broad spatial scale.

Invasive alien plant control: The priority to save one of the most rapidly declining island-endemic plant species worldwide

Invasive alien plant control: The priority to save one of the most rapidly declining island-endemic plant species worldwide

Loss of endangered frugivores from seed dispersal networks generates severe mutualism disruption.

Many tropical seed-dispersing frugivores are facing extinction, but the consequences of the loss of endangered frugivores for seed dispersal is not well understood. We investigated the role of frugivore endangerment status via robustness-to-coextinction simulations (in this context, more accurately described as robustness-to-partner-loss simulations) using data from the Brazilian Atlantic Forest biodiversity hotspot. By simulating the extinction of endangered frugivores, we found a rapid and disproportionate loss of tree species with dispersal partners in the network, and this surprisingly surpassed any other frugivore extinction scenario, including the loss of the most generalist frugivores first. A key driver of this pattern is that many specialist plants rely on at-risk frugivores as seed-dispersal partners. Moreover, interaction compensation in the absence of endangered frugivores may be unlikely because frugivores with growing populations forage on fewer plant species than frugivores with declining populations. Therefore, protecting endangered frugivores could be critical for maintaining tropical forest seed dispersal, and their loss may have higher-than-expected functional consequences for tropical forests, their regeneration processes, and the maintenance of tropical plant diversity.

Demographic consequences of mutualism disruption: Browsing and big-headed ant invasion drive acacia population declines.

Across the globe, biological invasions have disrupted mutualisms, producing reverberating consequences for ecosystems. Although invasive species frequently trigger mutualism disruptions, few studies have quantified the demographic mechanisms by which mutualism breakdown may generate population effects. In a Kenyan savanna, the invasive big-headed ant (Pheidole megacephala) has disrupted a foundational mutualism between the monodominant whistling-thorn tree (Acacia drepanolobium) and native ants (Crematogaster spp.) that deter browsing by large mammalian herbivores. We conducted experiments to quantify the demographic consequences of this mutualism disruption in the presence and absence of large mammalian herbivores. Invasion by P. megacephala exacerbated population declines of A. drepanolobium, primarily through decreased survival and reproduction of adult trees. However, these fitness reductions were small compared to those resulting from the presence of large mammalian herbivores, which negatively impacted growth and survival. Contrary to expectation, the expulsion of metabolically costly Crematogaster mutualists by P. megacephala did not result in higher population growth rates for trees protected from large mammalian herbivores. Our results suggest that invasive P. megacephala may impose a direct metabolic cost to trees exceeding that of native mutualists while providing no protection from browsing by large mammalian herbivores. Across landscapes, we expect that invasion by P. megacephala will reduce A. drepanolobium populations, but that the magnitude and demographic pathways of this effect will hinge on the presence and abundance of browsers.

Fleshy‐fruited invasive shrubs indirectly increase native tree seed dispersal

Biological invasions are one of the main threats to biodiversity and ecosystem functioning in the Anthropocene. Fleshy‐fruited invasive plants establish mutualistic interactions with native seed dispersers and may affect the mutualisms between native partners, negatively by disrupting plant dispersal through competition for seed dispersers or positively by facilitating seed dispersal via the attraction of fruit‐eating animals. Moreover, the invaders' density in the neighborhood of native plants may modulate the direction and/or magnitude of such effects on natives. In mountains of central Argentina, the cessation of fruiting of the dominant native tree Lithraea molleoides overlaps with the beginning of the fruiting of invasive shrubs (Pyracantha spp.). This partial overlap allows for testing opposite predictions regarding the effect of invasive fruits on native seed dispersal. We compared frugivory by seed disperser birds on L. molleoides during non‐overlapping and overlapping periods, at six sites that differed in Pyracantha shrub density (high, low and no‐invasion). We counted frugivory during 2 h on 15 individuals of L. molleoides at each site and period, totaling 360 h of observation. Frugivory on the native tree was similar among sites during the non‐overlapping period and remained constant in both periods at non‐invaded sites. At invaded sites, frugivory increased from non‐overlapping to overlapping period and was greater at highly invaded sites. The resource provided by Pyracantha did not disrupt seed dispersal of the dominant native tree. Rather, it facilitated frugivory by seed dispersers and this effect may be exacerbated with higher fruit availability of invasives. Our results provide a counterview to the prevailingly negative impacts of invasive species on the seed dispersal of native species since the fruiting of invasive plants facilitated the seed dispersal of native species in a continental region contrasts with the mutualism disruption commonly observed in insular environments.

Negative effects of an allelopathic invader on AM fungal plant species drive community-level responses.

The mechanisms causing invasive species impact are rarely empirically tested, limiting our ability to understand and predict subsequent changes in invaded plant communities. Invader disruption of native mutualistic interactions is a mechanism expected to have negative effects on native plant species. Specifically, disruption of native plant‐fungal mutualisms may provide non‐mycorrhizal plant invaders an advantage over mycorrhizal native plants. Invasive Alliaria petiolata (garlic mustard) produces secondary chemicals toxic to soil microorganisms including mycorrhizal fungi, and is known to induce physiological stress and reduce population growth rates of native forest understory plant species. Here, we report on a 11‐yr manipulative field experiment in replicated forest plots testing if the effects of removal of garlic mustard on the plant community support the mutualism disruption hypothesis within the entire understory herbaceous community. We compare community responses for two functional groups: the mycorrhizal vs. the non‐mycorrhizal plant communities. Our results show that garlic mustard weeding alters the community composition, decreases community evenness, and increases the abundance of understory herbs that associate with mycorrhizal fungi. Conversely, garlic mustard has no significant effects on the non‐mycorrhizal plant community. Consistent with the mutualism disruption hypothesis, our results demonstrate that allelochemical producing invaders modify the plant community by disproportionately impacting mycorrhizal plant species. We also demonstrate the importance of incorporating causal mechanisms of biological invasion to elucidate patterns and predict community‐level responses.

Non-intrusive systematic study reveals mutualistic interactions between threatened island endemic species and points to more impactful conservation

Non-intrusive systematic study reveals mutualistic interactions between threatened island endemic species and points to more impactful conservation

Mycorrhizae, invasions, and the temporal dynamics of mutualism disruption

Summary An increasingly recognized impact of plant invaders is the disruption of positive interactions between native plants and their belowground mutualistic mycorrhizal fungi. We reviewed 112 studies from 61 publications that report invader impacts on mycorrhizal fungi. We describe emerging patterns on the frequency of negative, neutral and positive invader effects on mycorrhizal fungal abundance, richness and community composition, and we evaluate how these outcomes vary with invasion age. We also describe the evidence for three mechanisms of disruption: (1) plant‐plant competition that alters host quantity or quality (2) changes in soil properties such as nutrient availability and (3) allelopathy. Invaders can disrupt native mutualisms if they are non‐mycorrhizal, associate with a different type of mycorrhiza, or associate with different taxa of the same type of mycorrhiza as the native plants. Invaders that enrich soil nutrients can cause declines in mycorrhizal abundance, shifts in fungal community composition, and cause native plants to reduce their dependence on mycorrhizas. Invaders that produce allelopathic compounds cause mycorrhizal abundance to decrease and alter community composition because of variation in the sensitivity of different fungi to toxins. While the evidence for disruption of the mycorrhizal mutualism with invasion is strong, temporal patterns have not yet emerged from the literature. Invasion age was not clearly associated with extent of disruption, and the timing of recovery following invader removal was highly variable. Differences in the biology of native and invasive plants, their interactions with mycorrhizal fungi and the surrounding landscape contributed to this variation. Synthesis. Our systematic review suggests that invaders frequently decrease mycorrhizal abundance and alter fungal community composition while only occasionally affecting fungal species richness. The development of invader impacts, as well as the restoration of native communities after invader removal, are influenced by a suite of plant, fungal and environmental traits that change over time. However, few studies have examined the temporal dynamics of mycorrhizal disruption, and results are variable. Future research should focus on the temporal scale of mutualism disruption while considering plant phylogenetics and demography, fungal functional traits such as spore longevity and dispersal, and soil chemistry.

Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network.

Following defaunation, the loss of interactions with mutualists such as pollinators or seed dispersers may be compensated through increased interactions with remaining mutualists, ameliorating the negative cascading impacts on biodiversity. Alternatively, remaining mutualists may respond to altered competition by reducing the breadth or intensity of their interactions, exacerbating negative impacts on biodiversity. Despite the importance of these responses for our understanding of the dynamics of mutualistic networks and their response to global change, the mechanism and magnitude of interaction compensation within real mutualistic networks remains largely unknown. We examined differences in mutualistic interactions between frugivores and fruiting plants in two island ecosystems possessing an intact or disrupted seed dispersal network. We determined how changes in the abundance and behavior of remaining seed dispersers either increased mutualistic interactions (contributing to "interaction compensation") or decreased interactions (causing an "interaction deficit") in the disrupted network. We found a "rich-get-richer" response in the disrupted network, where remaining frugivores favored the plant species with highest interaction frequency, a dynamic that worsened the interaction deficit among plant species with low interaction frequency. Only one of five plant species experienced compensation and the other four had significant interaction deficits, with interaction frequencies 56-95% lower in the disrupted network. These results do not provide support for the strong compensating mechanisms assumed in theoretical network models, suggesting that existing network models underestimate the prevalence of cascading mutualism disruption after defaunation. This work supports a mutualist biodiversity-ecosystem functioning relationship, highlighting the importance of mutualist diversity for sustaining diverse and resilient ecosystems.

Mutualistic strategies minimize coextinction in plant-disperser networks.

The global decline of mutualists such as pollinators and seed dispersers may cause negative direct and indirect impacts on biodiversity. Mutualistic network models used to understand the stability of mutualistic systems indicate that species with low partner diversity are most vulnerable to coextinction following mutualism disruption. However, existing models have not considered how species vary in their dependence on mutualistic interactions for reproduction or survival, overlooking the potential influence of this variation on species' coextinction vulnerability and on network stability. Using global databases and field experiments focused on the seed dispersal mutualism, we found that plants and animals that depend heavily on mutualistic interactions have higher partner diversity. Under simulated network disruption, this empirical relationship strongly reduced coextinction because the species most likely to lose mutualists depend least on their mutualists. The pattern also reduced the importance of network structure for stability; nested network structure had little effect on coextinction after simulations incorporated the empirically derived relationship between partner diversity and mutualistic dependence. Our results highlight a previously unknown source of stability in mutualistic networks and suggest that differences among species in their mutualistic strategy, rather than network structure, primarily accounts for stability in mutualistic communities.

Effects of an invasive predator cascade to plants via mutualism disruption

Invasive vertebrate predators are directly responsible for the extinction or decline of many vertebrate species, but their indirect impacts often go unmeasured, potentially leading to an underestimation of their full impact. When invasives extirpate functionally important mutualists, dependent species are likely to be affected as well. Here, we show that the invasive brown treesnake, directly responsible for the extirpation of forest birds from the island of Guam, is also indirectly responsible for a severe decline in plant recruitment as a result of disrupting the fruit-frugivore mutualism. To assess the impact of frugivore loss on plants, we compare seed dispersal and recruitment of two fleshy-fruited tree species on Guam and three nearby islands with intact disperser communities. We conservatively estimate that the loss of frugivorous birds caused by the brown treesnake may have caused a 61–92% decline in seedling recruitment. This case study highlights the potential for predator invasions to cause indirect, pervasive and easily overlooked interaction cascades.

Invader disruption of belowground plant mutualisms reduces carbon acquisition and alters allocation patterns in a native forest herb.

Invasive plants impose novel selection pressures on naïve mutualistic interactions between native plants and their partners. As most plants critically rely on root fungal symbionts (RFSs) for soil resources, invaders that disrupt plant-RFS mutualisms can significantly depress native plant fitness.Here, we investigate the consequences of RFS mutualism disruption on native plant fitness in a glasshouse experiment with a forest invader that produces known anti-fungal allelochemicals. Over 5months, we regularly applied either green leaves of the allelopathic invader Alliaria petiolata, a nonsystemic fungicide to simulate A. petiolata's effects, or green leaves of nonallelopathic Hesperis matronalis (control) to pots containing the native Maianthemum racemosum and its RFSs. We repeatedly measured M. racemosum physiology and harvested plants periodically to assess carbon allocation. Alliaria petiolata and fungicide treatment effects were indistinguishable: we observed inhibition of the RFS soil hyphal network and significant reductions in M. racemosum physiology (photosynthesis, transpiration and conductance) and allocation (carbon storage, root biomass and asexual reproduction) in both treatments relative to the control. Our findings suggest a general mechanistic hypothesis for local extinction of native species in ecosystems challenged by allelopathicinvaders: RFS mutualism disruption drives carbon stress, subsequent declines in native plant vigor, and, if chronic, declines in RFS-dependent species abundance.

Declining relict plants: Climate effect or seed dispersal disruption? A landscape-scale approach

Declining relict plants: Climate effect or seed dispersal disruption? A landscape-scale approach

A novel impact of a novel weapon: allelochemicals in Alliaria petiolata disrupt the legume-rhizobia mutualism

Some introduced species become invasive by releasing novel allelochemicals into the soil, directly harming nearby plants and soil microbes. Alliaria petiolata (garlic mustard) is an invasive plant, well known to excrete a suite of phytotoxic and anti-microbial allelochemicals, including allyl isothiocyanate (AITC) and benzyl isothiocyanate (BITC). While the effects of these chemicals on plant-mycorrhizae mutualisms are well documented, the effects on other plant-soil microbe interactions, such as the legume-rhizobia mutualism, have not yet been tested. Here, we performed laboratory and greenhouse experiments with both synthetic chemicals and leaf extracts to investigate the effects of allelochemicals in A. petiolata on a native leguminous plant, Amphicarpaea bracteata, and its rhizobia mutualists. We found that BITC reduced rhizobia growth rate in the lab, but had no effect on nodulation in the greenhouse when rhizobia were grown in the presence of plants. AITC did not directly harm either plants or rhizobia, though plants and rhizobia grown in the presence of AITC showed reduced nodulation, indicating that it disrupted the formation of the mutualism itself. We found no effects of A. petiolata allelochemical leaf extracts on plant performance or nodulation. Our data suggest that AITC causes mutualism disruption in this system by preventing the formation of nodules, which reduces plant growth and could threaten the long-term performance of rhizobia. Our study shows that the allelochemicals in A. petiolata disrupt the legume-rhizobia resource mutualism, adding another impact of these novel weapons in addition to their well-documented role in disrupting plant-mycorrhizae symbioses.

Mutualism Disruption Threatens Global Plant Biodiversity: A Systematic Review

BackgroundAs global environmental change accelerates, biodiversity losses can disrupt interspecific interactions. Extinctions of mutualist partners can create “widow” species, which may face reduced ecological fitness. Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions. However, the scope of this problem – the magnitude of biodiversity that may lose mutualist partners and the consequences of these losses – remains unknown.Methodology/Principal FindingsWe conducted a systematic review and synthesis of data from a broad range of sources to estimate the threat posed by vertebrate extinctions to the global biodiversity of vertebrate-dispersed and -pollinated plants. Though enormous research gaps persist, our analysis identified Africa, Asia, the Caribbean, and global oceanic islands as geographic regions at particular risk of disruption of these mutualisms; within these regions, percentages of plant species likely affected range from 2.1–4.5%. Widowed plants are likely to experience reproductive declines of 40–58%, potentially threatening their persistence in the context of other global change stresses.ConclusionsOur systematic approach demonstrates that thousands of species may be impacted by disruption in one class of mutualisms, but extinctions will likely disrupt other mutualisms, as well. Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions. Conservation measures with explicit focus on mutualistic functions could be necessary to bolster populations of widowed species and maintain ecosystem functions.

Effects of Native and Non-Native Vertebrate Mutualists on Plants

Extinctions can leave species without mutualist partners and thus potentially reduce their fitness. In cases where non-native species function as mutualists, mutualism disruption associated with species' extinction may be mitigated. To assess the effectiveness of mutualist species with different origins, we conducted a meta-analysis in which we compared the effectiveness of pollination and seed-dispersal functions of native and non-native vertebrates. We used data from 40 studies in which a total of 34 non-native vertebrate mutualists in 20 geographic locations were examined. For each plant species, opportunistic non-native vertebrate pollinators were generally less effective mutualists than native pollinators. When native mutualists had been extirpated, however, plant seed set and seedling performance appeared elevated in the presence of non-native mutualists, although non-native mutualists had a negative overall effect on seed germination. These results suggest native mutualists may not be easily replaced. In some systems researchers propose taxon substitution or the deliberate introduction of non-native vertebrate mutualists to reestablish mutualist functions such as pollination and seed dispersal and to rescue native species from extinction. Our results also suggest that in places where all native mutualists are extinct, careful taxon substitution may benefit native plants at some life stages.

Testing the mutualism disruption hypothesis: physiological mechanisms for invasion of intact perennial plant communities

Soil resources derived from mutualistic arbuscular mycorrhizal fungi (AMF) play a critical role in the physiological function of many native plant species. Allelopathic plant invasion studies have revealed declines in AMF inoculation potential of invaded soils, and lost opportunities for plants to form new AMF associations. Yet, if allelochemicals also kill AMF external hyphae already associated with plant roots, this mutualism disruption should result in physiological stress for native plants. We previously demonstrated that forest soils infested with garlic mustard (Alliaria petiolata), an allelopathic invader, exhibit reduced fungal hyphal abundance. Here, we demonstrate for the first time that treatment with garlic mustard tissue reduces soil respiration rates and diminishes physiological function of false Solomon's seal (Maianthemum racemosum), an AMF-dependant forest understory native. Treated plants exhibited reduced stomatal conductance and photosynthesis relative to controls, consistent with the proposed loss of AMF function. Such physiological declines, if sustained over several growing seasons, could decrease native understory perennials' growth rates and increase their susceptibility to environmental stresses. These data provide an explicit mechanism that can help explain the loss of established native perennials from invaded mature forests. We propose that the physiological costs of mutualism disruption may be a widespread but previously untested mechanism enhancing the invasion of undisturbed ecosystems by allelopathic species.