Carolina L. Morales

Invasive Mutualists Erode Native Pollination Webs

Plant–animal mutualisms are characterized by weak or asymmetric mutual dependences between interacting species, a feature that could increase community stability. If invasive species integrate into mutualistic webs, they may alter web structure, with consequences for species persistence. However, the effect of alien mutualists on the architecture of plant–pollinator webs remains largely unexplored. We analyzed the extent of mutual dependency between interacting species, as a measure of mutualism strength, and the connectivity of 10 paired plant–pollinator webs, eight from forests of the southern Andes and two from oceanic islands, with different incidences of alien species. Highly invaded webs exhibited weaker mutualism than less-invaded webs. This potential increase in network stability was the result of a disproportionate increase in the importance and participation of alien species in the most asymmetric interactions. The integration of alien mutualists did not alter overall network connectivity, but links were transferred from generalist native species to super-generalist alien species during invasion. Therefore, connectivity among native species declined in highly invaded webs. These modifications in the structure of pollination webs, due to dominance of alien mutualists, can leave many native species subject to novel ecological and evolutionary dynamics.

A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants

Alien plant species can alter pollinator visitation and, in turn, the sexual reproduction of natives. Using a conventional and a phylogenetically controlled meta-analytical approach on a data set of 40 studies, we evaluated the effect of alien neighbour plant species (aliens) on visitation to and reproduction of native co-flowering focal species (focals), and compared such effect to that of native neighbours (natives). An overall significantly negative effect of aliens on visitation to and reproduction of focals was confirmed. Interestingly, aliens differed from natives in their effect on visitation, but not on reproductive success. The negative effect of aliens on visitation and reproductive success increased at high relative alien plant abundance, but this increase was proportionally lower than the increase in relative plant abundance. Likewise, effect of aliens on visitation and reproductive success was most detrimental when alien and focal species had similar flower symmetry or colour. The phylogenetic relatedness between alien neighbours and focals influenced the reproductive success effect size. Results of the phylogenetic meta-analysis were only partly consistent with those of the conventional meta-analysis, depending on the response variable and on whether we controlled for the phylogeny of neighbour or focal species, which calls for special attention to control for species relatedness in this type of review. This study demonstrates the predominant detrimental impact of alien plants on pollination and reproduction of natives, and highlights the importance of phenotypic similarity to the outcome of the interaction.

Ecological impacts of invasive alien species on bees

We review direct and indirect impacts of invasive alien species (focussing on plants and insects) on native bees worldwide. Although there is a rapidly growing body of research into the effects of invasive alien plants on native plant pollination via disruption of native mutualisms, there has been little research on the impacts of invasive alien plants directly on bees. Such impacts are likely to vary according to the taxon of plant, the functional specificity of the native bees, and ecosystem context. Conversely, there have been more attempts to document impacts of invasive alien social bees on native bees. Most of these studies only indirectly evaluate competition for resources, have focused on a few native species and findings are sometimes contradictory. However, some studies showed strong negative impacts, suggesting that effects might be species-specific. Additionally, pathogen spillover and reproductive disruption due to interspecific mating has been demonstrated among some closely related taxa. Where we lack unequivocal evidence for impacts however, this should not be interpreted as lack of effect. We recommend that future studies are robustly designed and consider impacts on genetic, species (particularly solitary bees) and ecosystem biodiversity.ZusammenfassungInvasive fremde Arten sind wichtige Antreiber globaler Umweltveränderungen, indem sie direkt oder indirekt auf die einheimische Biodiversität und die Ökosystemprozesse Einfluss nehmen. Die durch einheimische Bienen erbrachten Bestäubungsleistungen werden allgemein durch einen weiten Bereich menschlicher Aktivitäten als gefährdet angesehen, im Blickpunkt dieser zusammenfassenden Untersuchung stehen potentielle Gefährdungen durch invasive Arten. Ziel des Artikels ist, den möglichen Einfluss invasiver fremder Arten auf die einheimischen Bienen abzuschätzen, um Gefährdungen bestimmen und Forschungsprioritäten in diesem Gebiet festlegen zu können. Wir berücksichtigten die Auswirkungen invasiver fremder Pflanzen, Bienen und Parasiten auf das Verhalten, die Populationen und Gesellschaften einheimischer Bienen und die Leistungen, die sie für das Ökosystem erbringen.Invasive fremde Pflanzen können direkt oder indirekt auf die einheimischen Bienen Einfluss nehmen (Abb. 1). Direkter Einfluss beinhaltet die Bereitstellung von Blütenressourcen, wobei deren Wert entsprechend ihrer morphologischen Zugänglichkeit, Nährwert und der zeitlichen und räumlichen Verfügbarkeit der Belohnungen variiert. Ein indirekter Einfluss liegt vor, wenn invasive fremde Pflanzen die einheimische Pflanzengemeinschaft beeinflussen (entweder durch Wettbewerb um abiotische Ressourcen oder um biotische Ressourcen einschließlich der Bestäubung) (Tab. I). Insgesamt können Beeinflussungen des individuellen Verhaltens und Überlebens relativ leicht bestimmt werden, während dagegen Einflüsse auf Populationen oder Gesellschaften wesentlich schwerer vorauszusehen sind und bislang nur wenig untersucht wurden.Der überwiegende Teil der Forschungen über die Auswirkung fremder invasiver Insekten auf die einheimischen Bienen hat sich auf die Auswirkungen von eingeführten sozialen Arten von Honigbienen oder Hummeln bezogen, die um Ressourcen oder Nistplätze in Konkurrenz stehen, die Verbreitung von Pathogenen und Krankheiten verursachen oder die Populationsstruktur durch Hybridisation oder Introgression beeinflussen. Trotz erheblicher Aufmerksamkeit der Forschung gibt es wenig schlüssige Nachweise für eine Kompetition zwischen fremden und einheimischen Bienen um Futterres-sourcen, hauptsächlich weil Untersuchungen zur Kompetition schwierig durchzuführen und zu interpretieren sind. Allerdings haben einige Untersuchungen eine Verminderung der Fitness einheimischer Bienen bei Anwesenheit invasiver fremder Bienen nachgewiesen. Es gibt allerdings so gut wie keine Untersuchungen zur Kompetition um andere Ressourcen als Futterressourcen, dies schließt Nistplätze trotz ihres offensichtlichen kompetitiven Potentials ein. Kürzlich wurde offensichtlich, dass insbesondere in Nordamerika eine der größten von eingeführten Bestäubern ausgehenden Gefährdungen ist, dass sie möglicherweise neuartige Pathogene und Krankheiten auf die einheimischen Bienen übertragen (Tab. II). Die Fähigkeit eingeführter Arten mit einheimischen Arten zu hybridisieren ist gut bekannt, und mit der Entwicklung molekularere Marker zur Erkennung einer Introgression dürfte das Ausmaß des Problems klarer werden.Wir schlagen verschiedene Forschungsschwerpunkte vor, nämlich dass (1) Untersuchungen des Ausmaßes der Auswirkungen sollten sowohl in zeitliches als auch räumlicher Hinsicht erweitert werden, in einem robusten Versuchsdesign strukturiert sein und repliziert werden, (2) besondere Aufmerksamkeit sollte den Auswirkungen auf solitäre und spezialisierte Bienenarten zukommen, (3) eine schnelle Erfassung potentieller Auswirkungen neuer Eindringlinge sollte zu einer raschen Entscheidungsfindung, Überwachung und Entschärfung des Problems führen, (4) die Pathologie, Virulenz und Kreuzinfektiösität von Pathogenen und Parasiten muss besser verstanden werden, und (5) die Auswirkungen weiterer Umweltänderungen auf Grund des Klimawandels müssen wegen der potentiellen räumlichen und zeitlichen Verlagerungen bei invasiven und einheimischen Pflanzen und Bestäubern sowie ihrer Interaktionen in Betracht gezogen werden. Wir empfehlen, dass Erhaltungsmaßnahmen einheimischer Bestäuber eine hohe Priorität zukommen sollte und dass diese Angelegenheit auf der Ebene des gesamten Ökosystems betrachtet werden sollte und nicht anhand eines nur artbasierten Ansatzes.

Does Invasion of Exotic Plants Promote Invasion of Exotic Flower Visitors? A Case Study from the Temperate Forests of the Southern Andes

Habitat disturbance, particularly of human origin, promotes the invasion of exotic plants, which in turn might foster the invasion of alien-interacting animals. Here we assess whether the invasion of exotic plants – mostly mediated by habitat disturbance – facilitates the invasion of exotic flower visitors in temperate forests of the southern Andes, Argentina. We recorded visit frequencies and the identity of visitors to the flowers of 15 native and 15 exotic plant species occurring in different highly disturbed and less disturbed habitats. We identified three alien flower visitors, the hymenopterans Apis mellifera, Bombus ruderatus, and Vespula germanica. We found significantly more visitation by exotic insects in disturbed habitats. This pattern was explained, at least in part, by the association between alien flower visitors and flowers of exotic plants, which occurred more frequently in disturbed habitats. However, this general pattern masked different responses between the two main alien flower visitors. Apis mellifera exploited almost exclusively the flowers of a subset of herbaceous exotic plants that thrive under disturbance, whereas B. ruderatus visited equally flowers of both exotic and native plants in both disturbed and undisturbed habitats. We did not find any strong evidence that flowers of exotic plants were more generalist than those of native plants, or that exotic flower visitors were more generalist than their native counterparts. Our results suggest that alien plant species could facilitate the invasion of at least some exotic flower visitors to disturbed habitats. Because flowering plants as well as flower visitors benefit from this mutualism, this association may enhance, through a positive feedback, successful establishment of both exotic partners.

Rapid ecological replacement of a native bumble bee by invasive species.

Despite rising global concerns over the potential impacts of non-native bumble bee (Bombus spp) introductions on native species, large-scale and long-term assessments of the consequences of such introductions are lacking. Bombus ruderatus and Bombus terrestris were sequentially introduced into Chile and later entered Argentinas Patagonian region. A large-scale survey in Patagonia reveals that, in 5 years post-arrival, the highly invasive B terrestris has become the most abundant and widespread Bombus species, and its southward spread is concurrent with the geographic retraction of the only native species, Bombus dahlbomii. Furthermore, a 20-year survey of pollinators of the endemic herb Alstroemeria aurea in northern Patagonia indicates that B ruderatus and B terrestris have replaced B dahlbomii, formerly the most abundant pollinator. Although the declines underlying mechanisms remain unknown, the potential roles of exploitative competition and pathogen co-introduction cannot be ruled out. Given that in...

Alien parasite hitchhikes to Patagonia on invasive bumblebee

The worldwide trade in bumblebees can lead to the spread of diseases, which in turn has been claimed as a factor in bumblebee decline. Populations of the introduced Bombus terrestris, which invaded NW Patagonia, Argentina, in 2006, harbor the highly pathogenic protozoan Apicystis bombi. We asked whether A. bombi had been co-introduced with B. terrestris, and if so, whether spillover occurred to the two resident bumblebee species in the region: the introduced European Bombus ruderatus and the native Bombusdahlbomii. We searched for A. bombi by means of PCR in samples of B. ruderatus and B. dahlbomii collected before and after the invasion of B. terrestris and in samples of the latter. We found no A. bombi in samples of B. ruderatus and B. dahlbomii collected before B. terrestris invasion, whereas post invasion, A. bombi was present in all 3 species. The identity of the parasite was established by sequencing the 18S region, which was identical for the three bumblebee species and also matched the European sequence, confirming it to be A. bombi. This is the first report of A. bombi in B. ruderatus and B. dahlbomii. Moreover, our results suggest that Patagonia had been free of A. bombi until this parasite was co-introduced with B. terrestris, and spilled over in situ to these two previously resident species. Finally, our findings provide indirect circumstantial evidence of a potential link between the population collapse and geographic retraction of B. dahlbomii and the introduction of this novel parasite.

Trait matching of flower visitors and crops predicts fruit set better than trait diversity

Understanding the relationships between trait diversity, species diversity and ecosystem functioning is essential for sustainable management. For functions comprising two trophic levels, trait matching between interacting partners should also drive functioning. However, the predictive ability of trait diversity and matching is unclear for most functions, particularly for crop pollination, where interacting partners did not necessarily co-evolve. World-wide, we collected data on traits of flower visitors and crops, visitation rates to crop flowers per insect species and fruit set in 469 fields of 33 crop systems. Through hierarchical mixed-effects models, we tested whether flower visitor trait diversity and/or trait matching between flower visitors and crops improve the prediction of crop fruit set (functioning) beyond flower visitor species diversity and abundance. Flower visitor trait diversity was positively related to fruit set, but surprisingly did not explain more variation than flower visitor species diversity. The best prediction of fruit set was obtained by matching traits of flower visitors (body size and mouthpart length) and crops (nectar accessibility of flowers) in addition to flower visitor abundance, species richness and species evenness. Fruit set increased with species richness, and more so in assemblages with high evenness, indicating that additional species of flower visitors contribute more to crop pollination when species abundances are similar.Synthesis and applications. Despite contrasting floral traits for crops world-wide, only the abundance of a few pollinator species is commonly managed for greater yield. Our results suggest that the identification and enhancement of pollinator species with traits matching those of the focal crop, as well as the enhancement of pollinator richness and evenness, will increase crop yield beyond current practices. Furthermore, we show that field practitioners can predict and manage agroecosystems for pollination services based on knowledge of just a few traits that are known for a wide range of flower visitor species. Despite contrasting floral traits for crops world-wide, only the abundance of a few pollinator species is commonly managed for greater yield. Our results suggest that the identification and enhancement of pollinator species with traits matching those of the focal crop, as well as the enhancement of pollinator richness and evenness, will increase crop yield beyond current practices. Furthermore, we show that field practitioners can predict and manage agroecosystems for pollination services based on knowledge of just a few traits that are known for a wide range of flower visitor species. Editors Choice

Effects of anthropogenic habitat disturbance on local pollinator diversity and species turnover across a precipitation gradient

Anthropogenic habitat disturbance can have profound effects on multiple components of forest biotas including pollinator assemblages. We assessed the effect of small-scale disturbance on local richness, abundance, diversity and evenness of insect pollinator fauna; and how habitat disturbance affected species turnover across the landscape and overall diversity along a precipitation gradient in NW Patagonia (Argentina). We evaluated the effect of disturbance on overall pollinator fauna and then separately for bees (i.e. Apoidea) and non-bee pollinators. Locally, disturbed habitats had significantly higher pollinator species richness and abundances than undisturbed habitats for the whole pollinator assemblage, but not for bees or non-bees separately. However, significant differences in species richness between habitats vanished after accounting for differences in abundance between habitat types. At a local scale Shannon–Weaver diversity and evenness did not vary with disturbance. A β diversity index indicated that, across forest types, species turnover was lower between disturbed habitats than between undisturbed habitats. In addition, rarefaction curves showed that disturbed habitats as a whole accumulated fewer species than undisturbed habitats at equivalent sample sizes. We concluded that small patches of disturbed habitat have a negligible effect on local pollinator diversity; however, habitat disturbance reduced β diversity through a homogenization of the pollinator fauna (in particular of bees) across the landscape.

Extremely frequent bee visits increase pollen deposition but reduce drupelet set in raspberry

Summary 1. Production of many flowering crops often benefits from elevated pollinator diversity and abundance. Nevertheless, the opposite relationship may arise if bees impair fruit or seed production and/or quality by damaging flowers during visitation, despite transferring pollen. 2. We assessed pollination and drupelet set (i.e. the number of drupelets per fruit) in 16 raspberry Rubus idaeus fields along a gradient of bee abundance in north-west Patagonia, Argentina. Using pollen supplementation, we also tested whether drupelet set was pollen limited in a subset of six fields. 3. Managed Apis mellifera and the invasive bumblebee Bombus terrestris accounted for 50% and 45% of all bee visits, respectively, to raspberry flowers. Pollen loads on stigmas increased with visit frequency of all bees combined and particularly with visitation by A. mellifera, but not by B. terrestris. Drupelet set was not pollen limited along the gradient of bee abundance. 4. Instead, drupelet set decreased with the proportion of damaged styles, which varied more strongly with the frequency of visits by B. terrestris than by A. mellifera. In fields with the highest bee frequency of visits ( � 300 visits flower � 1 day � 1 ), � 80% of styles were damaged in flowers and these developed into fruits with � 30% fewer drupelets compared to flowers in fields with the lowest bee visitation rates ( � 4 visits flower � 1 day � 1 ). 5. Synthesis and applications. Extreme bee visitation, particularly by Bombus terrestris, damaged the styles of raspberry flowers, precluding ovule fertilization by deposited pollen and limiting crop production by reducing drupelet set. Only a few bee visits are required to maximize fruit production in raspberry plants, therefore, pollinator management in north-west Patagonia should focus principally on reducing the abundance of the invasive bumblebee B. terrestris and secondarily controlling the number of honeybee hives in nearby cultivated fields. Although mainstream pollinator management relies on the assumption that more visits enhance fruit set, high bee visitation rates can be detrimental for fruit development and, consequently, for crop yield.

Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease.

The worldwide spread of diseases is considered a major threat to biodiversity and a possible driver of the decline of pollinator populations, particularly when novel species or strains of parasites emerge. Previous studies have suggested that populations of introduced European honeybee (Apis mellifera) and bumblebee species (Bombus terrestris and Bombus ruderatus) in Argentina share the neogregarine parasite Apicystis bombi with the native bumblebee (Bombus dahlbomii). In this study we investigated whether A. bombi is acting as an emergent parasite in the non-native populations. Specifically, we asked whether A. bombi, recently identified in Argentina, was introduced by European, non-native bees. Using ITS1 and ITS2 to assess the parasite’s intraspecific genetic variation in bees from Argentina and Europe, we found a largely unstructured parasite population, with only 15% of the genetic variation being explained by geographic location. The most abundant haplotype in Argentina (found in all 9 specimens of non-native species) was identical to the most abundant haplotype in Europe (found in 6 out of 8 specimens). Similarly, there was no evidence of structuring by host species, with this factor explaining only 17% of the genetic variation. Interestingly, parasites in native Bombus ephippiatus from Mexico were genetically distant from the Argentine and European samples, suggesting that sufficient variability does exist in the ITS region to identify continent-level genetic structure in the parasite. Thus, the data suggest that A. bombi from Argentina and Europe share a common, relatively recent origin. Although our data did not provide information on the direction of transfer, the absence of genetic structure across space and host species suggests that A. bombi may be acting as an emergent infectious disease across bee taxa and continents.