Inverse priority effects: A role for historical contingency during species losses.

Communities worldwide are losing multiple species at an unprecedented rate, but how communities reassemble after these losses is often an open question. It is well established that the order and timing of species arrival during community assembly shapes forthcoming community composition and function. Yet, whether the order and timing of species losses can lead to divergent community trajectories remains largely unexplored. Here, we propose a novel framework that sets testable hypotheses on the effects of the order and timing of species losses-inverse priority effects-and suggests its integration into the study of community assembly. We propose that the order and timing of species losses within a community can generate alternative reassembly trajectories, and suggest mechanisms that may underlie these inverse priority effects. To formalize these concepts quantitatively, we used a three-species Lotka-Volterra competition model, enabling to investigate conditions in which the order of species losses can lead to divergent reassembly trajectories. The inverse priority effects framework proposed here promotes the systematic study of the dynamics of species losses from ecological communities, ultimately aimed to better understand community reassembly and guide management decisions in light of rapid global change.

Underexplored and growing economic costs of invasive alien trees.

The high ecological impacts of many invasive alien trees have been well documented. However, to date, we lacked synthesis of their economic impacts, hampering management actions. Here, we summarize the cost records of invasive trees to (I) identify invasive trees with cost information and their geographic locations, (II) investigate the types of costs recorded and sectors impacted by invasive trees and (III) analyze the relationships between categories of uses of invasive trees and the invasion costs attributed to these uses. We found reliable cost records only for 72 invasive trees, accumulating a reported total cost of $19.2 billion between 1960 and 2020. Agriculture was the sector with the highest cost records due to invasive trees. Most costs were incurred as resource damages and losses ($3.5 billion). Close attention to the ornamental sector is important for reducing the economic impact of invasive trees, since most invasive trees with cost records were introduced for that use. Despite massive reported costs of invasive trees, there remain large knowledge gaps on most invasive trees, sectors, and geographic scales, indicating that the real cost is severely underestimated. This highlights the need for further concerted and widely-distributed research efforts regarding the economic impact of invasive trees.

Identifying Priorities, Targets, and Actions for the Long-term Social and Ecological Management of Invasive Non-Native Species.

Formulating effective management plans for addressing the impacts of invasive non-native species (INNS) requires the definition of clear priorities and tangible targets, and the recognition of the plurality of societal values assigned to these species. These tasks require a multi-disciplinary approach and the involvement of stakeholders. Here, we describe procedures to integrate multiple sources of information to formulate management priorities, targets, and high-level actions for the management of INNS. We follow five good-practice criteria: justified, evidence-informed, actionable, quantifiable, and flexible. We used expert knowledge methods to compile 17 lists of ecological, social, and economic impacts of lodgepole pines (Pinus contorta) and American mink (Neovison vison) in Chile and Argentina, the privet (Ligustrum lucidum) in Argentina, the yellow-jacket wasp (Vespula germanica) in Chile, and grasses (Urochloa brizantha and Urochloa decumbens) in Brazil. INNS plants caused a greater number of impacts than INNS animals, although more socio-economic impacts were listed for INNS animals than for plants. These impacts were ranked according to their magnitude and level of confidence on the information used for the ranking to prioritise impacts and assign them one of four high-level actions-do nothing, monitor, research, and immediate active management. We showed that it is possible to formulate management priorities, targets, and high-level actions for a variety of INNS and with variable levels of available information. This is vital in a world where the problems caused by INNS continue to increase, and there is a parallel growth in the implementation of management plans to deal with them.

Invasive trees rely more on mycorrhizas, countering the ideal-weed hypothesis.

The ideal-weed hypothesis predicts that invasive plants should be less dependent on mutualisms. However, evidence in favor of or against this hypothesis comes mainly from observational studies. Here, we experimentally tested this hypothesis using a two-factor greenhouse experiment, comparing the seedling growth response of different Pinus species (varying in invasiveness) to ectomycorrhizal fungal inoculation. Most species showed no response until they were 6 mo old, at which point inoculation increased growth between 10 and 260% among the different species. This growth response was higher for species with lower seed mass, higher dispersal ability, higher Z score (a proxy for invasiveness) and higher number of naturalized regions, all of which correspond to higher invasiveness. Our results show that timing is a crucial factor when comparing mycorrhizal dependency of different species. Dependence on mutualistic microorganisms could be part of a strategy in which invasive species produce smaller seeds, in greater number, which can disperse further, but where seedlings are more reliant on mycorrhizas to improve access to water, nutrients, and protection from pathogens. Our results suggest that reliance on mutualisms may enhance, rather than limit, nonnative species in their ability to spread, establish, and colonize.

Sheep feeding preference as a tool to control pine invasion in Patagonia: influence of foliar toughness, terpenoids and resin content.

Herbivores modulate the structure and composition of plant communities, including plant invasions. This is conditioned by plant palatability which can be reduced by its chemical or physical traits. The effects that ungulates browsing has on pine invasions are variable and the empirical evidence on the causes of this variability is scarce. We experimentally explored how sheep browsing preference varies between seedlings of pine species with different invasiveness; Pinus contorta (high invasiveness), P. ponderosa (medium invasiveness), P. radiata (medium invasiveness) and P. jeffreyi (low invasiveness). Secondly, we quantified anti-herbivory chemical compounds and physical traits of these species and related them with sheep preference observed. The browsing incidence of P. contorta was 68%, P. ponderosa 58%, P. radiata 29%, and P. jeffreyi 84%. Among anti-herbivory traits analyzed, α-pinene concentration had a negative effect on the probability of a terminal bud being browsed and on browsing intensity. Meanwhile, foliar toughness was negatively related to browsing intensity and water concentration was positively related to browsing intensity. Also, the most invasive species, P. contorta, was highly damaged. Thus, sheep herbivory could be slowing pine invasion rate; suggesting that could be considered a tool to control early invasions, especially for this particular species.

Highly invasive tree species are more dependent on mutualisms.

Why some species become invasive while others do not remains an elusive question. It has been proposed that invasive species should depend less on mutualisms, because their spread would then be less constrained by the availability of mutualistic partners. We tested this idea with the genus Pinus, whose degree of invasiveness is known at the species level (being highly and negatively correlated with seed size), and which forms obligate mutualistic associations with ectomycorrhizal fungi (EMF). Mycorrhizal dependence is defined as the degree to which a plant needs the mycorrhizal fungi to show the maximum growth. In this regard, we use plant growth response to mycorrhizal fungi as a proxy for mycorrhizal dependence. We assessed the responsiveness of Pinus species to EMF using 1,206 contrasts published on 34 species, and matched these data with data on Pinus species invasiveness. Surprisingly, we found that species that are more invasive depend more on mutualisms (EMF). Seedling growth of species with smaller seeds benefited more from mutualisms, indicating a higher dependence. A higher reliance on EMF could be part of a strategy in which small-seeded species produce more seeds that can disperse further, and these species are likely to establish only if facilitated by mycorrhizal fungi. On the contrary, big-seeded species showed a lower dependence on EMF, which may be explained by their tolerance to stressful conditions during establishment. However, the limited dispersal of larger seeds may limit the spread of these species. We present strong evidence against a venerable belief in ecology that species that rely more on mutualisms are less prone to invade, and suggest that in certain circumstances greater reliance on mutualists can increase spread capacity.

Seed predation does not explain pine invasion success.

Why some non-native plant species invade, and others fail remains an elusive question. Plant invasion success has been associated with specific species traits. Yet, we have limited knowledge of the mechanisms relating these traits to invasion potential. General patterns of biotic resistance by seed predation may provide a mechanism that helps separate invasive from non-invasive plants. Seed predation is an important barrier against plant establishment for many plant species. It may, therefore, create a selective filter against non-native plant establishment based on plant traits related to seed predation rate. In two cafeteria-style seed predation experiments in a steppe ecosystem in Patagonia (Argentina) we provided seeds of 16 non-native Pinaceae covering a 300-fold variation in seed mass, a 200-fold variation in seed volume and 75-fold variation in seed toughness. Seed removal decreased with seed mass and seed volume. Seed toughness was not a significant predictor while seed volume was the best predictor of predators' preference. However, for species of this family small seed size is the most important predictor of species invasiveness. Our results show that seed predation does not explain Pinaceae invasive success. In our system, species that have smaller seeds (i.e., more invasive) are preferentially consumed by seed predators. Seed mass was not the best predictor of granivory rates, despite being the seed trait on which most studies have been focused. Our ability to predict future invasion and understand invasion success could benefit from other studies that focus on the mechanisms behind invasive traits.

Suilloid fungi as global drivers of pine invasions.

Belowground biota can deeply influence plant invasion. The presence of appropriate soil mutualists can act as a driver to enable plants to colonize new ranges. We reviewed the species of ectomycorrhizal fungi (EMF) that facilitate pine establishment in both native and non-native ranges, and that are associated with their invasion into nonforest settings. We found that one particular group of EMF, suilloid fungi, uniquely drive pine invasion in the absence of other EMF. Although the association with other EMF is variable, suilloid EMF are always associated with invasive pines, particularly at early invasion, when invasive trees are most vulnerable. We identified five main ecological traits of suilloid fungi that may explain their key role at pine invasions: their long-distance dispersal capacity, the establishment of positive biotic interactions with mammals, their capacity to generate a resistant spore bank, their rapid colonization of roots and their long-distance exploration type. These results suggest that the identity of mycorrhizal fungi and their ecological interactions, rather than simply the presence of compatible fungi, are key to the understanding of plant invasion processes and their success or failure. Particularly for pines, their specific association with suilloid fungi determines their invasion success in previously uninvaded ecosystems.

How are monospecific stands of invasive trees formed? Spatio-temporal evidence from Douglas fir invasions.

Invasive plant species can produce many impacts on native communities. Impacts can be especially important when the non-natives reach high densities, producing monospecific stands where little grows besides the non-native species. We propose three basic pathways by which monospecific stands of invasive tree species are formed: (i) gradually from the propagule source, (ii) via synchronous establishment and (iii) following several pulses of synchronous establishment. Different patterns can produce different impacts through time and may require different management techniques. This study aims to further our understanding of how monotypic stands of invasive species arise. We documented how monospecific stands are formed during invasion processes by studying patterns of spatio-temporal establishment of several monospecific stands of Douglas fir in Patagonia. We obtained data on tree density, year of establishment, size, distance to the seed source and other related measurements for this tree species along transects from the original seed source (80-year-old plantations) to the edge of the monospecific stand. We found that these monospecific stands arose in a more complex way than expected. While individuals established on average simultaneously over all distances from the seed source, there was substantial variation in time of establishment at all distances. Also, tree density was higher near the source than far from it. Different factors can account for the observed pattern of tree establishment, including seed dispersal, mycorrhizal facilitation and herbivory. Our results elucidate the complexities of spatio-temporal pattern of formation in monospecific stands. This understanding can improve management strategies and techniques for this invasion and other plant invasions in different regions.

Potential problems of removing one invasive species at a time: a meta-analysis of the interactions between invasive vertebrates and unexpected effects of removal programs.

Although the co-occurrence of nonnative vertebrates is a ubiquitous global phenomenon, the study of interactions between invaders is poorly represented in the literature. Limited understanding of the interactions between co-occurring vertebrates can be problematic for predicting how the removal of only one invasive-a common management scenario-will affect native communities. We suggest a trophic food web framework for predicting the effects of single-species management on native biodiversity. We used a literature search and meta-analysis to assess current understanding of how the removal of one invasive vertebrate affects native biodiversity relative to when two invasives are present. The majority of studies focused on the removal of carnivores, mainly within aquatic systems, which highlights a critical knowledge gap in our understanding of co-occurring invasive vertebrates. We found that removal of one invasive vertebrate caused a significant negative effect on native species compared to when two invasive vertebrates were present. These unexpected results could arise because of the positioning and hierarchy of the co-occurring invasives in the food web (e.g., carnivore-carnivore or carnivore-herbivore). We consider that there are important knowledge gaps to determinate the effects of multiple co-existing invaders on native ecosystems, and this information could be precious for management.

Replacement of native by non-native animal communities assisted by human introduction and management on Isla Victoria, Nahuel Huapi National Park.

One of the possible consequences of biological invasions is the decrease of native species abundances or their replacement by non-native species. In Andean Patagonia, southern Argentina and Chile, many non-native animals have been introduced and are currently spreading. On Isla Victoria, Nahuel Huapi National Park, many non-native vertebrates were introduced ca. 1937. Records indicate that several native vertebrates were present before these species were introduced. We hypothesize that seven decades after the introduction of non-native species and without appropriate management to maintain native diversity, non-native vertebrates have displaced native species (given the known invasiveness and impacts of some of the introduced species). We conducted direct censuses in linear transects 500 m long (n = 10) in parallel with camera-trapping (1,253 camera-days) surveys in two regions of the island with different levels of disturbance: high (n = 4) and low (n = 6) to study the community of terrestrial mammals and birds and the relative abundances of native and non-native species. Results show that currently non-native species are dominant across all environments; 60.4% of census records and 99.7% of camera trapping records are of non-native animals. We detected no native large mammals; the assemblage of large vertebrates consisted of five non-native mammals and one non-native bird. Native species detected were one small mammal and one small bird. Species with the highest trapping rate were red and fallow deer, wild boar, silver pheasant (all four species are non-native) and chucao (a native bird). These results suggest that native species are being displaced by non-natives and are currently in very low numbers.

Impact of Non-Native Birds on Native Ecosystems: A Global Analysis.

Introduction and naturalization of non-native species is one of the most important threats to global biodiversity. Birds have been widely introduced worldwide, but their impacts on populations, communities, and ecosystems have not received as much attention as those of other groups. This work is a global synthesis of the impact of nonnative birds on native ecosystems to determine (1) what groups, impacts, and locations have been best studied; (2) which taxonomic groups and which impacts have greatest effects on ecosystems, (3) how important are bird impacts at the community and ecosystem levels, and (4) what are the known benefits of nonnative birds to natural ecosystems. We conducted an extensive literature search that yielded 148 articles covering 39 species belonging to 18 families -18% of all known naturalized species. Studies were classified according to where they were conducted: Africa, Asia, Australasia, Europe, North America, South America, Islands of the Indian, of the Pacific, and of the Atlantic Ocean. Seven types of impact on native ecosystems were evaluated: competition, disease transmission, chemical, physical, or structural impact on ecosystem, grazing/ herbivory/ browsing, hybridization, predation, and interaction with other non-native species. Hybridization and disease transmission were the most important impacts, affecting the population and community levels. Ecosystem-level impacts, such as structural and chemical impacts were detected. Seven species were found to have positive impacts aside from negative ones. We provide suggestions for future studies focused on mechanisms of impact, regions, and understudied taxonomic groups.

Ectomycorrhizal fungal communities coinvading with Pinaceae host plants in Argentina: Gringos bajo el bosque.

Coinvasive ectomycorrhizal (ECM) fungi allow Pinaceae species to invade regions otherwise lacking compatible symbionts, but ECM fungal communities permitting Pinaceae invasions are poorly understood. In the context of Pinaceae invasions on Isla Victoria, Nahuel Huapi National Park, Argentina, we asked: what ECM fungi are coinvading with Pinaceae hosts on Isla Victoria; are some ECM fungal species or genera more prone to invade than others; and are all ECM fungal species that associate with Northern Hemisphere hosts also nonnative, or are some native fungi compatible with nonnative plants? We sampled ECMs from 226 Pinaceae host plant individuals, both planted individuals and recruits, growing inside and invading from plantations. We used molecular techniques to examine ECM fungal communities associating with these trees. A distinctive subset of the ECM fungal community predominated far from plantations, indicating differences between highly invasive and less invasive ECM fungi. Some fungal invaders reported here have been detected in other locations around the world, suggesting strong invasion potential. Fungi that were frequently detected far from plantations are often found in early-successional sites in the native range, while fungi identified as late-successional species in the native range are rarely found far from plantations, suggesting a means for predicting potential fungal coinvaders.

Lack of belowground mutualisms hinders Pinaceae invasions.

Why particular invasions succeed and others fail is not well understood. The role of soil biota has been proposed as important. However, the role of mutualists has received much less attention than that of pathogens. Here we report that lack of adequate ectomycorrhizal fungi hinders invasion by exotic Pinaceae on Isla Victoria, Argentina, by reducing both the probability of establishment and growth of invading individuals. More than one hundred exotic tree species were introduced to this island ca. 80 years ago, but invasive trees are found in high densities only in areas adjacent to plantations. With a series of greenhouse and field experiments we found lower mycorrhizal colonization levels and few fungal species far from original plantings, and key fungal mutualists are confined to areas near plantations, probably owing to dispersal limitations. Low inoculum levels far from the plantations are retarding the invasion. Our experiments indicate that positive interactions belowground can play a key but underappreciated role in invasion dynamics.

Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms.

Although it is increasingly clear that exotic invasive species affect seed-dispersal mutualisms, a synthetic examination of the effect of exotic invasive species on seed-dispersal mutualisms is lacking. Here, we review the impacts of the invasive Argentine ant (Linepithema humile) on seed dispersal. We found that sites with L. humile had 92 per cent fewer native ant seed dispersers than did sites where L. humile was absent. In addition, L. humile did not replace native seed dispersers, as rates of seed removal and seedling establishment were all lower in the presence of L. humile than in its absence. We conclude that potential shifts in plant diversity and concomitant changes in ecosystem function may be a consequence of Argentine ant invasions, as well as invasions by other ant species. Because very few studies have examined the effects of non-ant invasive species on seed-dispersal mutualisms, the prevalence of disruption of seed-dispersal mutualisms by invasive species is unclear.