Mutualism between co-introduced species facilitates invasion and alters plant community structure

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.     

Infiltration of a facultative ant–plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits

1. Ant–plant mutualisms have been the focus of considerable empirical research, but few studies have investigated how introduced ants affect these interactions. Using 2 years of survey data, this study examines how the introduced Argentine ant [Linepithema humile (Mayr)] differs from native ants with respect to its ability to protect the extrafloral nectary‐bearing coast barrel cactus (Ferocactus viridescens) in Southern California. 2. Eighteen native ant species visited cacti in uninvaded areas, but cacti in invaded areas were primarily visited by the Argentine ant. The main herbivore of the coast barrel cactus present at the study sites is a leaf‐footed bug (Narnia wilsoni). 3. Herbivore presence (the fraction of surveys in which leaf‐footed bugs were present on individual cacti) was negatively related to ant presence (the fraction of surveys in which ants were present on individual cacti). Compared with cacti in uninvaded areas, those in invaded areas were less likely to have herbivores and when they did had them less often. 4. Seed mass was negatively related to herbivore presence, and this relationship did not differ for cacti in invaded areas versus those in uninvaded areas. 5. Although the Argentine ant might provide superior protection from herbivores, invasion‐induced reductions in ant mutualist diversity could potentially compromise plant reproduction. The cumulative number of ant species on individual cacti over time was lower in invaded areas and was associated with a shortened seasonal duration of ant protection and reduced seed mass. These results support the hypothesis that multiple partners may enhance mutualism benefits.     

The indirect consequences of a mutualism: comparing positive and negative components of the net interaction between honeydew-tending ants and host plants

1. In ecological webs, net indirect interactions between species are composed of interactions that vary in sign and magnitude. Most studies have focused on negative component interactions (e.g. predation, herbivory) without considering the relative importance of positive interactions (e.g. mutualism, facilitation) for determining net indirect effects. 2. In plant/arthropod communities, ants have multiple top-down effects via mutualisms with honeydew-producing herbivores and harassment of and predation on other herbivores; these ant effects provide opportunities for testing the relative importance of positive and negative interspecific interactions. We manipulated the presence of ants, honeydew-producing membracids and leaf-chewing beetles on perennial host plants in field experiments in Colorado to quantify the relative strength of these different types of interactions and their impact on the ant's net indirect effect on plants. 3. In 2007, we demonstrated that ants simultaneously had a positive effect on membracids and a negative effect on beetles, resulting in less beetle damage on plants hosting the mutualism. 4. In 2008, we used structural equation modelling to describe interaction strengths through the entire insect herbivore community on plants with and without ants. The ant's mutualism with membracids was the sole strong interaction contributing to the net indirect effect of ants on plants. Predation, herbivory and facilitation were weak, and the net effect of ants reduced plant reproduction. This net indirect effect was also partially because of behavioural changes of herbivores in the presence of ants. An additional membracid manipulation showed that the membracid's effect on ant activity was largely responsible for the ant's net effect on plants; ant workers were nearly ten times as abundant on plants with mutualists, and effects on other herbivores were similar to those in the ant manipulation experiment. 5. These results demonstrate that mutualisms can be strong relative to negative direct interspecific interactions and that positive interactions deserve attention as important components of ecological webs.     

Ants suppressing plant pathogens: a review

Ant–plant mutualisms are usually regarded as driven by ants defending plants against herbivores in return for plant‐produced food rewards and housing. However, ants may provide additional services. In a review of published studies on ant–pathogen–plant interactions, we investigated whether ants’ extensive hygiene measures, including the use of ant‐produced antibiotics, extend to their host plants and reduce plant pathogen loads. From 30 reported species combinations, we found that the presence of ants lead to reduced pathogen levels in 18 combinations and to increased levels in 6. On average, ants significantly reduced pathogen incidence with 59%. This effect size did not differ significantly from effect sizes reported from meta‐analyses on herbivore protection. Thus, pathogen and herbivore protection could be of equal importance in ant–plant mutualisms. Considering the abundance of these interactions, ecological impacts are potentially high. Furthermore, awareness of this service may stimulate the development of new measures to control plant diseases in agriculture. It should be noted, though, that studies were biased toward tropical ant–plant symbioses and that the literature in the field is limited at present. Future research on plant pathogens is needed to enhance our understanding of ant–plant mutualisms and their evolution.     

Contrasting effects of an invasive ant on a native and an invasive plant

When invasive species establish in new environments, they may disrupt existing or create new interactions with resident species. Understanding of the functioning of invaded ecosystems will benefit from careful investigation of resulting species-level interactions. We manipulated ant visitation to compare how invasive ant mutualisms affect two common plants, one native and one invasive, on a sub-tropical Indian Ocean island. Technomyrmex albipes, an introduced species, was the most common and abundant ant visitor to the plants. T. albipes were attracted to extrafloral nectaries on the invasive tree (Leucaena leucocephala) and deterred the plant’s primary herbivore, the Leucaena psyllid (Heteropsylla cubana). Ant exclusion from L. leucocephala resulted in decreased plant growth and seed production by 22% and 35%, respectively. In contrast, on the native shrub (Scaevola taccada), T. albipes frequently tended sap-sucking hemipterans, and ant exclusion resulted in 30% and 23% increases in growth and fruit production, respectively. Stable isotope analysis confirmed the more predacious and herbivorous diets of T. albipes on the invasive and native plants, respectively. Thus the ants’ interactions protect the invasive plant from its main herbivore while also exacerbating the effects of herbivores on the native plant. Ultimately, the negative effects on the native plant and positive effects on the invasive plant may work in concert to facilitate invasion by the invasive plant. Our findings underscore the importance of investigating facilitative interactions in a community context and the multiple and diverse interactions shaping novel ecosystems.     

Gallerucida bifasciata (Coleoptera: Chrysomelidae), a potential biological control agent for Japanese knotweed (Fallopia japonica)

Host specificity of foreign natural enemies are becoming more and more critical in classical biological control programs, as concerns about potential risk from introduced biocontrol agents have been increasing recently. Understanding the insect's fundamental and ecological host ranges is the first step in determining the potential for introduction of an insect to control invasive plants. Japanese knotweed, Fallopia japonica (Houttuyn) Ronse Decraene (Polygonaceae) is an invasive weed in the United States and Europe. A leaf beetle, Gallerucida bifasciata (Coleoptera: Chrysomelidae) is an important natural enemy attacking this plant in Asia. However, its host range records were ambiguous. This study examined the beetle's host specificity through a set of choice and no-choice tests in the laboratory and field in its native China. Gallerucida bifasciata larvae were able to complete development on seven of 87 plant species in larval development tests, while adults fed and oviposited on 10 plants in no-choice tests. Multiple choice tests showed adults strongly preferred Fallopia japonica, Persicaria perfoliata (L.) H. Gross and Polygonum multiflorum Thunb over all other plants. Open field tests and field surveys further revealed that these three species were in its ecological host range. The results of this study suggest that G. bifasciata is a potential promising agent for control of Japanese knotweed in the United States and Europe, although additional host specificity tests and risk assessment should be completed.     

Are invasive ants better plant‐defense mutualists? A comparison of foliage patrolling and herbivory in sites with invasive yellow crazy ants and native weaver ants

Benefits arising from facultative mutualisms between ants and plants vary with the identity of the ant partner. Invasive and native ants are both attracted to plants that offer extrafloral nectar, but few studies have compared their abilities to displace herbivores and benefit plants. Yellow crazy ants Anoplolepis gracilipes have invaded eucalypt woodlands of Arnhem Land, northern Australia, where they displace the native dominant weaver ant Oecophylla smaragdina. We compared the plant defense services provided by A. gracilipes and O. smaragdina ants on trees with (Acacia lamprocarpa) and without (Eucalyptus tetrodonta) extrafloral nectar rewards through surrogate herbivore (termite) addition experiments and surveys of herbivore damage. Anoplolepis gracilipes were more likely than O. smaragdina to discover termites on A. lamprocarpa, but the likelihood of termite discovery on E. tetrodonta did not vary with ant species. Anoplolepis gracilipes were also more thorough in their attacks of termites, recruited 3.4–4 times more workers to termites, and were 3.4 times quicker at discovering termites on A. lamprocarpa than were O. smaragdina. Discovery of termites by other predators did not vary significantly between trees in A. gracilipes and O. smaragdina sites. Herbivory scores did not reflect the foliage patrolling pattern by the ants. Old A. lamprocarpa leaves and both new and old leaves and branches on E. tetrodonta in A. gracilipes sites had higher chewing herbivory scores than their counterparts in O. smaragdina sites. Our results reveal that the more aggressive and efficient foliar patrolling by A. gracilipes does not translate to increased plant protection. Ant invasions can disrupt native ant–plant mutualisms despite invasive ants possessing many traits associated with effective plant guarding.     

Community‐wide impact of an exotic aphid on introduced tall goldenrod

1. The aphid Uroleucon nigrotuberculatum Olive, which is specialised to the tall goldenrod, Solidago altissima L., in its native range, has become a dominant species on the introduced tall goldenrod in Japan. How this exotic aphid influenced arthropod communities on the introduced tall goldenrod in aphid‐present (spring) and aphid‐absent (autumn) seasons was examined, using an aphid removal experiment. 2. In spring, aphid presence increased ant abundance because aphid honeydew attracted foraging ant workers. A significant negative correlation was found between the numbers of ants and herbivorous insects other than aphids on the aphid‐exposed plants, but no significant correlation was detected on the aphid‐free plants. Thus, the aphid presence was likely to decrease the abundance of co‐occurring herbivorous insects through removal behaviour of the aphid‐tending ants. There were no significant differences in plant traits between the aphid‐exposed and aphid‐free plants. 3. In autumn, the numbers of lateral shoots and leaves, and the leaf nitrogen content were increased in response to the aphid infestation in spring. Because of the improvement of plant traits by aphid feeding, the abundance of leaf chewers increased on aphid‐exposed plants. In contrast, the abundance of sap feeders decreased on the aphid‐exposed plants. In particular, the dominant scale insect among sap feeders, Parasaissetia nigra Nietner, decreased, followed by a decrease in the abundance of ants attending P. nigra. Thus, aphid feeding may have attenuated the negative impacts of the tending ants on leaf chewers. 4. Aphid presence did not change herbivore species richness but changed the relative density of dominant herbivores, resulting in community‐wide effects on co‐occurring herbivores through ant‐mediated indirect effects, and on temporally separated herbivores through plant‐ and ant‐mediated indirect effects. The aphid also altered predator community composition by increasing and decreasing the relative abundance of aphid‐tending ants in the spring and autumn, respectively.     

Nectar quality affects ant aggressiveness and biotic defense provided to plants

Ant–plant mutualisms are useful models for investigating how plant traits mediate interspecific interactions. As plant‐derived resources are essential components of ant diets, plants that offer more nutritious food to ants should be better defended in return, as a result of more aggressive behavior toward natural enemies. We tested this hypothesis in a field experiment by adding artificial nectaries to individuals of the species Vochysia elliptica (Vochysiaceae). Ants were offered one of four liquid foods of different nutritional quality: amino acids, sugar, sugar + amino acids, and water (control). We used live termites (Nasutitermes coxipoensis) as herbivore competitors and observed ant behavior toward them. In 88 hr of observations, we recorded 1,009 interactions with artificial nectaries involving 1,923 individual ants of 26 species. We recorded 381 encounters between ants and termites, of which 38% led to attack. Sixty‐one percent of these attacks led to termite exclusion from the plants. Recruitment and patrolling were highest when ants fed upon nectaries providing sugar + amino acids, the most nutritious food. This increase in recruitment and patrolling led to higher encounter rates between ants and termites, more frequent attacks, and faster and more complete termite removal. Our results are consistent with the hypothesis that plant biotic defense is mediated by resource quality. We highlight the importance of qualitative differences in nectar composition for the outcome of ant–plant interactions. Abstract in Portuguese is available with online material.     

Seed handling behaviours of native and invasive seed‐dispersing ants differentially influence seedling emergence in an introduced plant

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Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper

The Enemy Release Hypothesis posits that invasion of novel habitats can be facilitated by the absence of coevolved herbivores. However, a new environment and interactions with unfamiliar herbivores may impose selection on invading plants for traits that reduce their attractiveness to herbivores or for enhanced defenses compared to native host plants, leading to a pattern similar to enemy release but driven by evolutionary change rather than ecological differences. The Shifting Defense Hypothesis posits that plants in novel habitats will shift from specialized defense mechanisms to defense mechanisms effective against generalist herbivores in the new range. We tested these ideas by comparing herbivore preference and performance of native (Eurasia)‐ and invasive (New World)‐range Medicago polymorpha, using a generalist herbivore, the soybean looper, that co‐occurs with M. polymorpha in its New World invaded range. We found that soybean loopers varied in preference and performance depending on host genotype and that overall the herbivore preferred to consume plant genotypes from naïve populations from Eurasia. This potentially suggests that range expansion of M. polymorpha into the New World has led to rapid evolution of a variety of traits that have helped multiple populations become established, including those that may allow invasive populations to resist herbivory. Thus, enemy release in a novel range can occur through rapid evolution by the plant during invasion, as predicted by the Shifting Defense Hypothesis, rather than via historical divergence.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

Ant–scale mutualism increases scale infestation,decreases folivory,and disrupts biological control in restored tropical forests

Ant–hemipteran mutualisms can have positive and negative effects on host plants depending on the level of hemipteran infestation and plant protection conferred by ants against folivory. Differential effects of such mutualisms on plant survival are well documented in undisturbed and ant-invaded systems, but few have explored how anthropogenic disturbance affects interactions between hemipterans and native ant species and what the consequences may be for recovering ecosystems. Within a fragmented landscape in Costa Rica, restored tropical forests harbor a mutualism between the native ant Wasmannia auropunctata and the scale insect Alecanochiton marquesi on the abundant, early-successional tree Conostegia xalapensis. I added A. marquesi scales to C. xalapensis seedlings and either allowed or excluded W. auropunctata to investigate if this mutualism leads to increased scale infestation, decreased scale mortality, and decreased folivory. I also examined whether these effects are mediated by the percentage of remnant forest cover in the landscape. I found that seedlings with ants excluded had fewer scale insects and higher herbivory than plants with ants present. I also found evidence that scale mortality due to fungal attack and parasitism was higher on ant-excluded versus ant-allowed seedlings but only at sites with high surrounding landscape forest cover. Together, these results suggest that mutualisms between scale insects and native ants can promote scale infestation, reduce folivory on native plant species, and potentially disrupt biological control of scale insects in recovering tropical forests. Further, my experiment underscores the importance of remnant tropical forests as sources of biological control in anthropogenically disturbed landscapes. Abstract in Spanish is available with online material.     

Thorn‐dwelling ants provide antiherbivore defence for camelthorn trees,Vachellia erioloba,in Namibia

Ants are widely employed by plants as an antiherbivore defence. A single host plant can associate with multiple, symbiotic ant species, although usually only a single ant species at a time. Different plant‐ant species may vary in the degree to which they defend their host plant. In Kenya, ant–acacia interactions are well studied, but less is known about systems elsewhere in Africa. A southern African species, Vachellia erioloba, is occupied by thorn‐dwelling ants from three different genera. Unusually, multiple colonies of all these ants simultaneously and stably inhabit trees. We investigated if the ants on V. erioloba (i) deter insect herbivores; (ii) differ in their effectiveness depending on the identity of the herbivore; and (iii) protect the tree against an important herbivore, the larvae of the lepidopteran Gonometa postica. We show that experimental exclusion of ants leads to greater levels of herbivory on trees. The ants inhabiting V. erioloba are an effective deterrent against hemipteran and coleopteran, but not lepidopteran herbivores. Defensive services do not vary among ant species, but only Crematogaster ants exhibit aggression towards G. postica. This highlights the potential of the V. erioloba–ant mutualism for studying ant–plant interactions that involve multiple, simultaneously resident thorn‐dwelling ant species.     

Testing the enemy release hypothesis: a review and meta-analysis

One of the most cited hypotheses explaining the inordinate success of a small proportion of introduced plants that become pests is the ‘natural enemies hypothesis’. This states that invasive introduced plants spread rapidly because they are liberated from their co-evolved natural enemies. This hypothesis had not been properly tested until recently. Previous reviews on this topic have been narrative and vote counting in nature. In this review, we carried out quantitative synthesis and meta-analysis using existing literature on plants and their herbivores to test the different components of the enemy release hypothesis. We found supporting evidence in that (1) insect herbivore fauna richness is significantly greater in the native than introduced ranges, and the reduction is skewed disproportionally towards specialists and insects feeding on reproductive parts; and (2) herbivore damage levels are greater on native plants than on introduced invasive congeners. However, herbivore damage levels are only marginally greater for plants in native than in introduced ranges, probably due to the small numbers of this type of study. Studies quantifying herbivore impacts on plant population dynamics are too scarce to make conclusions for either comparison of plants in native vs introduced ranges or of co-occurring native and introduced congeners. For future research, we advocate that more than two-way comparisons between plants in native and introduced ranges, or native and introduced congeners are needed. In addition, the use of herbivore exclusions to quantify the impacts of herbivory on complete sets of population vital rates of native vs introduced species are highly desirable. Furthermore, three-way comparisons among congeners of native plants, introduced invasive, and introduced non-invasive plants can also shed light on the importance of enemy release. Finally, simultaneously testing the enemy release hypothesis and other competing hypotheses will provide significant insights into the mechanisms governing the undesirable success of invasive species.     

Floral visitation by the Argentine ant reduces pollinator visitation and seed set in the coast barrel cactus, Ferocactus viridescens

Mounting evidence indicates that trade-offs between plant defense and reproduction arise not only from resource allocation but also from interactions among mutualists. Indirect costs of plant defense by ants, for example, can outweigh benefits if ants deter pollinators. Plants can dissuade ants from occupying flowers, but such arrangements may break down when novel ant partners infiltrate mutualisms. Here, we examine how floral visitation by ants affects pollination services when the invasive Argentine ant (Linepithema humile) replaces a native ant species in a food-for-protection mutualism with the coast barrel cactus (Ferocactus viridescens), which, like certain other barrel cacti, produces extrafloral nectar. We compared the effects of floral visitation by the Argentine ant with those of the most prevalent native ant species (Crematogaster californica). Compared to C. californica, the Argentine ant was present in higher numbers in flowers. Cactus bees (Diadasia spp.), the key pollinators in this system, spent less time in flowers when cacti were occupied by the Argentine ant compared to when cacti were occupied by C. californica. Presumably as a consequence of decreased duration of floral visits by Diadasia, cacti occupied by L. humile set fewer seeds per fruit and produced fewer seeds overall compared to cacti occupied by C. californica. These data illustrate the importance of mutualist identity in cases where plants balance multiple mutualisms. Moreover, as habitats become increasingly infiltrated by introduced species, the loss of native mutualists and their replacement by non-native species may alter the shape of trade-offs between plant defense and reproduction.     

An orb‐weaver spider exploits an ant–acacia mutualism for enemy‐free space

Exploiters of protection mutualisms are assumed to represent an important threat for the stability of those mutualisms, but empirical evidence for the commonness or relevance of exploiters is limited. Here, I describe results from a manipulative study showing that an orb‐weaver spider, Eustala oblonga, inhabits an ant‐acacia for protection from predators. This spider is unique in the orb‐weaver family in that it associates closely with both a specific host plant and ants. I tested the protective effect of acacia ants on E. oblonga by comparing spider abundance over time on acacias with ants and on acacias from which entire ant colonies were experimentally removed. Both juvenile and adult spider abundance significantly decreased over time on acacias without ants. Concomitantly, the combined abundance of potential spider predators increased over time on acacias without ants. These results suggest that ant protection of the ant‐acacia Acacia melanocerus also protects the spiders, thus supporting the hypothesis that E. oblonga exploits the ant–acacia mutualism for enemy‐free space. Although E. oblonga takes advantage of the protection services of ants, it likely exacts little to no cost and should not threaten the stability of the ant–acacia mutualism. Indeed, the potential threat of exploiter species to protection mutualisms in general may be limited to species that exploit the material rewards traded in such mutualisms rather than the protection services.     

Changing light conditions in pine rockland habitats affect the intensity and outcome of ant–plant interactions

Extrafloral nectar (EFN) mediates food‐for‐protection mutualisms between plants and ants. Such mutualisms exist within a complex web of biotic interactions, and in a framework provided by the abiotic environment. Both biotic and abiotic factors, therefore, affect the outcome of ant–plant interactions. We conducted an experiment to determine the effects of ant activity, and light intensity, on herbivory rates, growth, and reproductive fitness in Senna mexicana var. chapmanii, a perennial legume native to pine rockland habitats of south Florida. Forty plants were divided among four treatments in a factorial experimental design with two independent variables: ant activity and light intensity. Plants were divided equally between sunny and shady habitats, and ants were excluded from half of the plants in each habitat type. The presence of ants significantly reduced herbivory rates in S. chapmanii. In shaded habitats, the presence of ants had no effect on plant reproductive fitness, however, in sunny habitats plants with ants produced significantly more seeds over the duration of the 1‐yr study. Ants represent an important biotic defense against herbivores in S. chapmanii; however, their effects on plant fitness are dependent on light conditions. Pine rockland habitats in south Florida have been widely destroyed or mismanaged. In fragments that remain, suppression of fire has led to increased canopy closure and shading of the understory. These changes will likely negatively impact plants that rely on ants for defense. We highlight the importance of conservation efforts to preserve the pine rocklands and the fire regimes on which they rely.     

Aggressiveness of ants attracted to the extrafloral nectary‐bearing plant,Mallotus japonicus,and temporal fluctuations in their abundance

Many plants that bear extrafloral nectaries (EFNs) attract various ant species that can exclude herbivores. The aggressiveness of the attracted ants and their temporal activity patterns are important factors that can affect the efficiency of herbivore exclusion from the plant. However, the characteristics of this mutualistic relationship between EFN‐bearing plants and ants have not been sufficiently elucidated. We investigated the aggressiveness of six ant species against the common armyworm, Spodoptera litura Fabr., and temporal fluctuations in the abundance of four aggressive ant species on an EFN‐bearing plant, Mallotus japonicus (L.f.) Müll. Arg. Workers of Crematogaster teranishii Santschi, Pheidole noda Smith, Pristomyrmex punctatus Smith and Formica japonica Motschoulsky were observed to be highly aggressive. In contrast, workers of Camponotus vitiosus Smith showed low aggressiveness. Paratrechina flavipes Smith workers did not attack the herbivore. The activity patterns of the four aggressive ant species greatly differed. Crematogaster teranishii and Ph. noda workers were constantly active throughout the day and night. In contrast, F. japonica was diurnal. Pristomyrmex punctatus was principally nocturnal. Formica japonica workers foraged solitarily, whereas workers of the other three species foraged in a group or recruited nestmates. Our results suggest that the efficacy of the indirect defense in M. japonicus depends principally on the attracted ant species.     

Introduced ants reduce interaction diversity in a multi‐species,ant–aphid mutualism

Mutualisms contribute in fundamental ways to the origin, maintenance and organization of biological diversity. Introduced species commonly participate in mutualisms, but how this phenomenon affects patterns of interactions among native mutualists remains incompletely understood. Here we examine how networks of interactions among aphid‐tending ants, ant‐tended aphids, and aphid‐attacking parasitoid wasps differ between 12 spatially paired riparian study sites with and without the introduced Argentine ant Linepithema humile in southern California. To resolve challenges in species identification, we used DNA barcoding to identify aphids and screen for parasitoid wasps (developing inside their aphid hosts) from 170 aphid aggregations sampled on arroyo willow Salix lasiolepis. Compared to uninvaded sites, invaded sites supported significantly fewer species of aphid‐tending ants and ant‐tended aphids. At invaded sites, for example, we found only two species of ant‐tended aphids, which were exclusively tended by L. humile, whereas at uninvaded sites we found 20 unique ant–aphid interactions involving eight species of ant‐tended aphids and nine species of aphid‐tending ants. Ant–aphid linkage density was thus significantly lower at invaded sites compared to uninvaded sites. We detected aphid parasitoids in 14% (28/198) of all aphid aggregations. Although the level of parasitism did not differ between invaded and uninvaded sites, more species of wasps were detected within uninvaded sites compared to invaded sites. These results provide a striking example of how the assimilation of introduced species into multi‐species mutualisms can reduce interaction diversity with potential consequences for species persistence.