Do mutualists matter? The role of pollinators, seed dispersers and belowground symbionts in the invasion success of Acacia

Plant species introduced to new locations may lose their natural enemies but can also leave behind important mutualists. Here, I take a novel comparative approach to identify the potential role of mutualistic interactions in determining invasion outcomes. I examine the strength of pollination, seed dispersal and belowground symbioses with nitrogen-fixing bacteria (rhizobia) across three species that vary in invasion success in both their introduced and native range. I used species of Australian Acacia introduced to New Zealand. I hypothesised that if interactions with mutualists are important for plant invasion then species would vary in the strength of interactions with one or more of the groups of mutualists I examined, and that the pattern of variation would correlate with the degree to which they have established and spread in New Zealand. At each stage I also consider the potentially mediating influence of natural enemies. For A. dealbata, a highly invasive species, and A. baileyana, a species that is widely naturalised in New Zealand, I found no differences in any of the variables I examined in relation to pollination and predispersal seed predation. However, for A. pravissima, currently considered a casual species in New Zealand, pre-dispersal seed predation was lower in New Zealand and overall seed production was much higher relative to conspecifics in Australia, and relative to the other two species. In relation to seed dispersal I found that the three species, which are all adapted for dispersal by ants (myrmecochory), were able to form dispersal mutualisms in New Zealand, potentially to the same degree as in Australia. Seed predation following seed fall was also lower for species in New Zealand than in Australia. There was no variation between the three species in seed removal associated with either dispersal or predation. By examining species’ growth and nodulation with rhizobia in both Australia and New Zealand I found that their ability to spread away from introduction sites could be limited by the availability of rhizobia in New Zealand, relative to Australia. However, there were again no differences between species. This is the first study to have directly measured mutualistic interactions across species that vary in invasive success in both their native and introduced range. I demonstrated that species introduced to new locations are able to establish mutualistic interactions with pollinators and dispersers to the same degree as in their native range. I also found the first direct evidence that the availability of rhizobia could limit species’ abilities to colonise new sites in the introduced range. However, mutualistic associations could not explain the variable invasive success of each species. Overall, these findings suggest that mutualistic interactions may be important for alien plant establishment, but alone cannot explain invasion outcomes. Instead, it is likely that invasive success is determined by a combination of biotic, abiotic and human factors, with the ability to establish mutualistic interactions just one component necessary for successful establishment and spread. These findings underline the importance of such broad geographical and comparative studies in attempts to elucidate drivers of invasion

Availability of soil mutualists may not limit non‐native Acacia invasion but could increase their impact on native soil communities

The availability of compatible mutualistic soil microbes could influence the invasion success of non-native plant species. Specifically, there may be spatial variation in the distribution of compatible microbes, and species-specific variation in plant host ability to associate with available microbes. Although either or both factors could promote or limit invasion, the scale over which most studies are conducted makes it difficult to examine these two possibilities simultaneously. However, this is critical to identifying a role of soil microbes in invasion. A series of recent research projects focused on interactions between Australian Acacia and nitrogen-fixing bacteria (rhizobia) at multiple spatial scales, from the local to the inter-continental, has allowed us to evaluate this question. Collectively, this research reveals that nodulation, performance and rhizobial community composition are all broadly similar across spatial scales and differentially invasive species. Synthesis and applications. We argue that current research provides convincing evidence that interactions with rhizobia do not determine invasion success in Acacia, but instead highlights key knowledge gaps that remain unfilled. Importantly, the ease with which non-native Acacia species form mutualistic associations with rhizobia, regardless of invasive status, highlights the critical need to understand the impacts of all non-native Acacia on native soil communities

Towards a holistic understanding of non-native tree impacts on ecosystem services : A review of Acacia, Eucalyptus and Pinus in Africa

Fast-growing, stress-tolerating tree species belonging to the genera Acacia, Eucalyptus and Pinus have historically been introduced to many tropical and sub-tropical regions to support various economic and environment-regulating functions. While these non-native tree (NNT) species are often highly useful, many are simultaneously invasive, generating negative environmental impacts. Current knowledge regarding the impacts of these NNTs on the ecosystem services (ES) that affect human well-being is largely informed by South African research, which inhibits a broader understanding of the contributions of these trees to those services. Acacia, Eucalyptus and Pinus have been widely introduced globally, yet very little is known about their contribution to ES in many locations. Here, we aimed to summarise the evidence for Acacia, Eucalyptus and Pinus as generating benefits and harm to ES, focusing on sub-Saharan Africa outside of South Africa. We conducted a literature search using the ISI Web of Science, which yielded 125 relevant publications. Although the three genera were reported to affect key ES in sub-Saharan Africa, the data were limited in geographic scope, with a strong bias towards East Africa as well as biases towards certain species and ecosystem service. The benefits of these NNTs relative to their costs are context dependent and may not reflect their actual impacts on ES in sub-Saharan Africa. Our review highlights the need for more systematic research from a broader perspective to manage potential conflicts and guide better management prioritisation

Phylogenetic signals and predictability in plant-soil feedbacks

There is strong evidence for a phylogenetic signal in the degree to which species share co-evolved biotic partners and in the outcomes of biotic interactions. This implies there should be a phylogenetic signal in the outcome of feedbacks between plants and soil microbiota they cultivate. However, attempts to identify a phylogenetic signal in plant-soil feedbacks have produced mixed results. We clarify how phylogenetic signals could arise in plant-soil feedbacks and use a recent compilation of data from feedback experiments to identify: 1) whether there is a phylogenetic signal in the outcome of plant-soil feedbacks; and 2) whether any signal arises through directional or divergent changes in feedback outcomes with evolutionary time. We find strong evidence for a divergent phylogenetic signal in feedback outcomes. Distantly related plant species show more divergent responses to each other's soil microbiota than closely related plant species. The pattern of divergence implies occasional co-evolutionary shifts in how plants interact with soil microbiota, with strongly contrasting feedback responses among some plant lineages. Our results highlight that it is difficult to predict feedback outcomes from phylogeny alone, other than to say that more closely related species tend to have more similar responses

Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings

Dispersal is thought to be a key process underlying the high spatial diversity of tropical forests. Just how important dispersal is in structuring plant communities is nevertheless an open question because it is very difficult to isolate dispersal from other processes, and thereby measure its effect. Using a unique situation, the loss of vertebrate seed dispersers on the island of Guam and their presence on the neighboring islands of Saipan and Rota, we quantify the contribution of vertebrate seed dispersal to spatial patterns of diversity of tree seedlings in treefall gaps. The presence of vertebrate seed dispersers approximately doubled seedling species richness within canopy gaps and halved species turnover among gaps. Our study demonstrates that dispersal plays a key role in maintaining local and regional patterns of diversity, and highlights the potential for ongoing declines in vertebrate seed dispersers to profoundly alter tropical forest composition

Root traits vary as much as leaf traits and have consistent phenotypic plasticity among 14 populations of a globally widespread herb

Our understanding of plant functional trait variation among populations and how this relates to local adaptation to environmental conditions is largely shaped by above-ground traits. However, we might expect below-ground traits linked to resource acquisition and conservation to vary among populations that experience different environmental conditions. Alternatively, below-ground traits might be highly plastic in response to growing conditions, such as availability of soil resources and association with symbiont arbuscular mycorrhizal fungi (AMF). We assessed (i) the strength of among-population variation in above- and below-ground traits, (ii) the effects of growing conditions on among-population variation and (iii) whether variation among populations is linked to source environment conditions, in a globally distributed perennial Plantago lanceolata. Using seeds from 14 populations across three continents, we grew plants in a common garden experiment and measured leaf and root traits linked to resource acquisition and water conservation. We included two sets of experimental treatments (high or low water availability; with and without AMF inoculation), which enabled us to assess trait responses to growing conditions. Across treatments, the percentage of root trait variation explained by populations and continents was 9%–26%, compared to 7%–20% for leaf trait variation. From principal component analysis (PCA), the first PC axis for both root and leaf traits largely reflected plant size, while the second PC broadly captured mass allocation. Root mass allocation (PC 2) was related to mean annual temperature and mean moisture index, indicating that populations from cooler, wetter environments had longer, thinner roots. However, we found little support for a relationship between source environment and leaf trait PCs, root system size (PC1) or individual traits. Water availability and AMF inoculation effects on size were consistent among populations, with larger plants under AMF inoculation, and less mass allocation to leaves under lower water availability. Plantago lanceolata shows substantial population-level variation in a suite of root traits, but that variation is only partially linked to the source environmental variables studied. Despite considerable differences in source abiotic environments, geographically separated populations have retained a strong and similar capacity for phenotypic plasticity both above and below-ground. Read the free Plain Language Summary for this article on the Journal blog.</p

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant

Publication history: Accepted - 19 May 2021; Published - 5 August 2021.Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait–environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.Eesti Teadusagentuur, Grant/Award Number: PRG609 and PUT1409; Academy of Finland; Natural Sciences and Engineering Research Council of Canada; Science Foundation Ireland, Grant/Award Number: 15/ERCD/2803; Spanish Ministry of Science, Innovation and Universities, Grant/Award Number: IJCI-2017- 32039; European Regional Development Fun

Experiment 1 R script

R script used to analyse the data from Experiment 1 and produce Figures 3 - 5

Experiment 1 recruitment data

Number of recruits recorded in each plot for Experiment 1. These data were used for Figures 3 - 5