Effects of Florivory on Floral Visitors and Reproductive Success of Sagittaria lancifolia (Alismataceae) in a Mexican Wetland.

Florivores consume floral structures with negative effects on plant fitness and pollinator attraction. Several studies have evaluated these consequences in hermaphroditic plants, but little is known about the effects on monoecious and dioecious species. We characterize the florivory and its effects on floral visitors and reproductive success in a monoecious population of Sagittaria lancifolia. Five categories of florivory were established according to the petal area consumed. Visits were recorded in male and female flowers within the different damage categories. Reproductive success was evaluated through fruit number and weight, as well as the number of seeds per fruit. Our results show that the weevil Tanysphyrus lemnae is the main florivore, and it mainly damages the female flowers. Hymenoptera were recorded as the most frequent visitors of both male and female flowers. Male and female flowers showed differences in visit frequency, which decreases as flower damage increases. Reproductive success was negatively related to the level of damage. We found that florivory is common in the population of S. lancifolia, which can exert a strong selective pressure by making the flowers less attractive and reducing the number of seeds per fruit. Future studies are needed to know how florivores affect plant male fitness.

Rasgos funcionales de frutos con importancia particular para los dispersores de semillas en el bosque seco tropical

Introducción: La frugivoría es un proceso ecológico determinante para la estructuración y regeneración de los bosques. En los trópicos, donde la diversidad de plantas y animales frugívoros es alta, las relaciones interespecíficas son complejas y requieren estudio. Objetivo: Identificar las especies de plantas ecológicamente importantes en dos redes de interacción, y el papel de los rasgos funcionales de los frutos en esas interacciones en un bosque seco. Métodos: Recolectamos 10 frutos por planta de 10 plantas de cada especie de interés en un bosque seco colombiano, calculamos el índice de importancia de las plantas a partir de la relevancia de aves y mamíferos frugívoros en la estructura de las redes. Esta relevancia se relaciona directamente con el potencial del animal como dispersor efectivo de semillas. Utilizamos modelos lineales generalizados para estimar el tamaño, color, estrato, y tipo de pulpa, en el índice. Resultados: Las plantas más importantes son especies de los géneros Miconia, Ficus, Cecropia, Bursera, Casearia y Trichilia, también identificadas como recursos importantes para los frugívoros de los trópicos en otros estudios. Las plantas con frutos carnosos, rojos y de menor tamaño son los mejores para dispersores de semillas. El índice de importancia de las plantas tiene alta variación; esto sugiere que un conjunto de especies frugívoras beneficiadas por cada especie de planta tiene una contribución diferenciada en procesos ecológicos derivados de la dispersión de semillas. Conclusiones: Programas de restauración para este tipo de bosque tropical seco debería incluir una variedad de plantas, incluyendo especies con frutos pequeños, rojos y carnosos.

Introduction: Frugivory is a pivotal ecological process for the structure and regeneration of forests. In the tropics, where the diversity of plants and frugivorous animals is high, interspecific relationships in the interaction networks are complex and need study. Objective: To identify ecologically important plant species in two interaction networks, and the role of functional fruit traits in those interactions in a dry forest. Methods: We collected 10 fruits per plant from 10 plants of each species of interest in a Colombian dry forest, we calculated the Plant Importance Index based on the bird and mammal frugivores relevance for network structure. This relevance is directly related to the animal's potential as effective seed dispersers. We used generalized linear models to estimate the effect of fruit size, color, stratum, and type of pulp, on the index. Results: The most important plants are species of the genera Miconia, Ficus, Cecropia, Bursera, Casearia and Trichilia, also identified as important resources for tropical frugivores in other studies. Plants with small, red, and fleshy fruits are the best for seed dispersers. The plant importance index has a high variation; this suggests that the set of frugivore species benefited by each plant species has a differential contribution to the ecological processes derived from seed dispersal. Conclusions: Restoration programs for this kind of tropical dry forest should include a variety of plants, including species with small, red, and fleshy fruits.

On the adequacy of fruit removal as a proxy for fitness in studies of bird-mediated phenotypic selection.

PREMISE: In fleshy-fruited plants, fruit removal is widely used as a proxy for plant reproductive success. Nevertheless, this proxy may not accurately reflect the number of seeds dispersed, an assumed better proxy for total fitness (fruit removal × mean number of seeds dispersed per fruit). METHODS: We examined under what circumstances fruit removal can be reliable as a proxy for total fitness when assessing bird-mediated selection on fruit traits. In three populations of the Blue Passionflower (Passiflora caerulea), we used the number of fruits pecked per plant as a surrogate for fruit removal to estimate phenotypic selection on fruit and seed traits, and simulations of the effect of the fruit-seed number trade-off on the number of fruits removed. RESULTS: Fruit removal was a good indicator of fitness, accounting for 55 to 68% of the variability in total fitness, measured as total number of seeds removed. Moreover, multivariate selection analyses on fruit crop size, mean fruit diameter and mean seed number using fruit removal as a fitness proxy yielded similar selection regimes to those using total fitness. Simulations showed that producing more fruits, a lower number of seeds per fruit, and a higher variability in seed number can result in a negative relationship between fruit removal and total fitness. CONCLUSIONS: Our results suggest that fruit removal can be reliably used as a proxy for total fitness when (1) there is a weak fruit number-seed number trade-off, (2) fruit crop size and fruit removal correlate positively, and (3) seed number variability does not largely exceed fruit number variability.

Atlantic flower-invertebrate interactions: A data set of occurrence and frequency of floral visits.

Encounters between flowers and invertebrates are key events for the functioning of tropical forests. Assessing the structure of networks composed of the interactions between those partners leads to a better understanding of ecosystem functioning and the effects of environmental factors on ecological processes. Gathering such data is, however, costly and time-consuming, especially in the highly diverse tropics. We aimed to provide a comprehensive repository of available flower-invertebrate interaction information for the Atlantic Forest, a South American tropical forest domain. Data were obtained from published works and "gray literature," such as theses and dissertations, as well as self-reports by co-authors. The data set has ~18,000 interaction records forming 482 networks, each containing between one and 1061 interaction links. Each network was sampled for about 200 h or less, with few exceptions. A total of 641 plant genera within 136 different families and 39 orders were reported, with the most abundant and rich families being Asteraceae, Fabaceae, and Rubiaceae. Invertebrates interacting with these plants were all arthropods from 10 orders, 129 families, and 581 genera, comprising 2419 morphotypes (including 988 named species). Hymenoptera was the most abundant and diverse order, with at least six times more records than the second-ranked order (Lepidoptera). The complete data set shows Hymenoptera interacting with all plant orders and also shows Diptera, Lepidoptera, Coleoptera, and Hemiptera to be important nodes. Among plants, Asterales and Fabales had the highest number of interactions. The best sampled environment was forest (~8000 records), followed by pastures and crops. Savanna, grasslands, and urban environments (among others) were also reported, indicating a wide range of approaches dedicated to collecting flower-invertebrate interaction data in the Atlantic Forest domain. Nevertheless, most reported data were from forest understory or lower strata, indicating a knowledge gap about flower-invertebrate interactions at the canopy. Also, access to remote regions remains a limitation, generating sampling bias across the geographical range of the Atlantic Forest. Future studies in these continuous and hard-to-access forested areas will yield important new information regarding the interactions between flowers and invertebrates in the Atlantic Forest. There are no copyright restrictions on the data set. Please cite this data paper if the data are used in publications and teaching events.

Clinal versus disruptive latitudinal variation in fruit traits of a South American mistletoe.

Fruit traits have historically been interpreted as plant adaptations to their seed dispersers. On the other hand, different environmental factors, which vary spatially and temporally, can shape fruit-trait variation. The mistletoe Tristerix corymbosus has a latitudinal distribution along the South American Pacific rim that encompasses two different biomes, the matorral of central Chile and the temperate forest that extends south of the matorral. This mistletoe shows contrasting fruiting phenology (spring vs summer), fruit color (yellow vs green), and seed dispersers (birds vs marsupial) in these two biomes. We characterized geographic variation of morphological and nutritional fruit traits of T. corymbosus to evaluate which macroecological factor, biome or latitude, better explains spatial variation in these variables. For each of 22 populations, we obtained environmental data (temperature, precipitation, and canopy cover), measured fruit and seed morphology traits (size, shape, and weight), and pulp moisture and nutritional content (fiber, protein, fat, carbohydrates, ash, and caloric content). Patterns of variation for each variable were described by fitting and comparing five different simple models varying in slope, intercept or both. Fruit morphology showed a clear biome-related disruptive pattern, seed morphological traits were unrelated to either biome or latitude, whereas nutritional variables showed diverse patterns. Different environmental factors seem to affect fruit development and phenology, determining the observed fruit characteristics, with seed dispersers playing a minor role in shaping these patterns. More generally, the contrasting plant-seed disperser associations we addressed can be interpreted as the outcome of an ecological-fitting rather than of a coevolutionary process.

Mechanisms underlying interaction frequencies and robustness in a novel seed dispersal network: lessons for restoration.

As human-caused extinctions and invasions accumulate across the planet, understanding the processes governing ecological functions mediated by species interactions, and anticipating the effect of species loss on such functions become increasingly urgent. In seed dispersal networks, the mechanisms that influence interaction frequencies may also influence the capacity of a species to switch to alternative partners (rewiring), influencing network robustness. Studying seed dispersal interactions in novel ecosystems on O'ahu island, Hawai'i, we test whether the same mechanisms defining interaction frequencies can regulate rewiring and increase network robustness to simulated species extinctions. We found that spatial and temporal overlaps were the primary mechanisms underlying interaction frequencies, and the loss of the more connected species affected networks to a greater extent. Further, rewiring increased network robustness, and morphological matching and spatial and temporal overlaps between partners were more influential on network robustness than species abundances. We argue that to achieve self-sustaining ecosystems, restoration initiatives can consider optimal morphological matching and spatial and temporal overlaps between consumers and resources to maximize chances of native plant dispersal. Specifically, restoration initiatives may benefit from replacing invasive species with native species possessing characteristics that promote frequent interactions and increase the probability of rewiring (such as long fruiting periods, small seeds and broad distributions).

From insect-plant interactions to ecological networks / Das interações inseto-planta às redes ecológicas

Abstract Since its inception, biodiversity has largely been understood as species diversity and assessed as such. Interactions among species or functional groups are gradually becoming part of an expanded concept of biodiversity. As a case study of the development of a research program in biodiversity, we summarize our multi-decade studies on interactions of Asteraceae and flowerhead-feeding insects in Brazil. Initially, host species were treated as independent replicates in order to assess the local and turnover components of their herbivore diversity. Research then expanded into sampling entire interactive communities of host plants and their associated herbivores in different localities and regions, enabling new research lines to be pursued. Interaction diversity could be assessed and factored into spatial and among-host components, suggesting a new field of interaction geography. Second, host specialization, a key component of interaction diversity, was reframed considering simultaneously relatedness and local availability of plant hosts. Third, with the influence of complex network theory, community-wide species interactions were probed for topological patterns. Having identified the modular structure of these plant-herbivore systems, later we demonstrated that they fit a compound hierarchical topology, in which interactions are nested within large-scale modules. In a brief survey of research funded by Fapesp, especially within the Biota-Fapesp program, we highlight several lines of internationally recognized research on interaction diversity, notably on plant-frugivore and plant-pollinator interactions, together with new theoretical models. The interplay of field studies with new theoretical and analytical approaches has established interaction diversity as an essential component for monitoring, conserving and restoring biodiversity in its broader sense.

Resumo Desde seu início, a biodiversidade geralmente tem sido entendida e avaliada principalmente como diversidade de espécies. Interações entre espécies ou grupos funcionais vêm sendo incorporadas em um conceito expandido de biodiversidade. Como um estudo de caso da evolução de um programa de pesquisa em biodiversidade, resumimos aqui nossos estudos das interações de Asteráceas com insetos endófagos em capítulos no Brasil, desenvolvidos por várias décadas. Inicialmente a diversidade de herbívoros foi estimada em diferentes espécies hospedeiras, tratando-as como réplicas independentes para estimar os componentes locais e de substituição da diversidade dos insetos associados. Posteriormente, passamos a amostrar comunidades interativas de plantas e insetos associados em diferentes localidades e regiões, o que abriu novas linhas de investigação. A diversidade de interações, agora fatorada em componentes espaciais e inter-hospedeiras, sugere um novo campo, a geografia de interações. Em segundo lugar, um componente essencial da diversidade de interações, a especialização trófica, foi redefinida como função da contiguidade filogenética bem como da disponibilidade local de plantas hospedeiras. Terceiro, sob influência da teoria de redes complexas, foram investigados padrões topológicos de comunidades interativas. Identificamos a estrutura modular dessas comunidades de plantas e herbívoros; posteriormente, demonstramos a topologia hierárquica dessas interações, composta por módulos internamente aninhados. Numa revisão sucinta de pesquisas sustentadas pela Fapesp, especialmente no programa Biota-Fapesp, destacamos diversas linhas de pesquisa sobre diversidade de interações que alcançaram reconhecimento internacional, tais como interações de plantas e frugívoros ou polinizadores, além de novos modelos teóricos. A conjugação de estudos de campo com novas abordagens teóricas e analíticas firmou a diversidade de interações como um componente essencial para monitorar, conservar e restaurar a biodiversidade em seu sentido mais amplo.

Environmental niche and functional role similarity between invasive and native palms in the Atlantic Forest.

Invasive species can significantly affect native species when their niches are similar. Ecological and morphological similarities between the invasive Australian palm, Archontophoenix cunninghamiana, and the native palm from the Brazilian Atlantic Forest, Euterpe edulis, suggest that they have similar environmental requirements and functional roles (i.e., the function a species performs in an ecosystem). This similarity raises concerns about how the invasive palm could impact the native species in the present and future. We used spatial (species occurrences) and ecological information (frugivory events) to characterize the environmental niche and functional role of the two palms and assess their overlap. In addition, we predicted the potential area of occurrence of each palm within the Brazilian Atlantic Forest under current and future climate conditions.We estimated the environmental conditions used by the invasive plant based on its native distribution only, and based on all areas where the species is able to establish across the globe. We found that the environmental niches of the two palm species overlap up to 39%, which corresponds to 50% of the current geographic distribution of E. edulis in the Atlantic Forest. In the areas where the two species potentially co-occur, the impact of the invasive species on the native should be influenced by the invasive species interactions with frugivores. We found that the frugivory functional role of the two palms was similar (84% overlap) which suggest that A. cunninghamiana might disrupt the seed dispersal of the native palm. However, co-occurrence between the palms may decline with future climate change, as the potentially environmental suitable area for the invasive palm is predicted to decline by 10% to 55%. Evaluating the similarity in both the environmental niche, of the native and global extent, and the functional role of native and invasive plants provides a detailed understanding of the potential impact of invasive species on native species now and in the future.

Florivory by lizards on Tacinga inamoena (K.Schum.) N.P.Taylor & Stuppy (Cactaceae) in the Brazilian Caatinga / Florivoria por lagartos em Tacinga inamoena (K.Schum.) N.P.Taylor & Stuppy (Cactaceae) na Caatinga brasileira

Abstract: Florivory can alter plant reproductive success by damaging sexual reproductive structures and disrupting plant-pollinator interactions through decreased flower attractiveness. Here, we report new records of the cactus Tacinga inamoena flower consumption by the Tropidurus hispidus lizard in the Brazilian Caatinga. We monitored 53 flowers from 11 T. inamoena individuals with camera traps over a 1-year period, totalling 450 camera-days of sample effort. We detected four florivory events. In three of these events, flowers were entirely consumed or had their reproductive structures severely damaged, leading to no fruit formation. Florivory events occurred in the morning, right after anthesis, in flowers near the ground, and lizards did not climb the cactus. Our results suggest that T. hispidus florivory on T. inamoena could have a negative impact on fruit set, since the consumed flowers were entirely destroyed. However, the long-term effects of florivory by lizards on T. inamoena reproductive success in the Caatinga still needs to be elucidated.

Resumo: A florivoria pode alterar o sucesso reprodutivo da planta através de danos às estruturas reprodutivas sexuais e interrupção das interações planta-polinizador por meio da diminuição da atratividade das flores. Aqui, relatamos novos registros de consumo de flores da cactácea opuntióide Tacinga inamoena pelo lagarto Tropidurus hispidus na Caatinga brasileira. Nós monitoramos 53 flores de 11 indivíduos de T. inamoena com armadilhas fotográficas por um período de um ano, totalizando 450 dias-câmera de esforço amostral. Detectamos quatro eventos de florivoria. Em três desses eventos, as flores foram totalmente consumidas ou tiveram suas estruturas reprodutivas severamente danificadas, não levando à formação de frutos. Os eventos de florivoria ocorreram pela manhã, logo após a antese, em flores próximas ao solo, e os lagartos não escalaram o cacto. Nossos resultados sugerem que a florivoria de T. hispidus em T. inamoena pode ter um impacto negativo na frutificação, uma vez que as flores consumidas foram totalmente destruídas. No entanto, os efeitos a longo prazo da florivoria por lagartos sobre o sucesso reprodutivo de T. inamoena na Caatinga ainda precisam ser elucidados.

Individual specialization in the use of space by frugivorous bats.

Natural populations are not homogenous systems but sets of individuals that occupy subsets of the species' niche. This phenomenon is known as individual specialization. Recently, several studies found evidence of individual specialization in animal diets. Diet is a critical dimension of a species' niche that affects several other dimensions, including space use, which has been poorly studied under the light of individual specialization. In this study, which harnesses the framework of the movement ecology paradigm and uses yellow-shouldered bats Sturnira lilium as a model, we ask how food preferences lead individual bats of the same population to forage mainly in different locations and habitats. Ten individual bats were radiotracked in a heterogeneous Brazilian savanna. First, we modelled intraspecific variation in space use as a network of individual bats and the landscape elements visited by them. Second, we developed two novel metrics, the spatial individual specialization index (SpatIS) and the spatial individual complementary specialization index (SpatICS). Additionally, we tested food-plant availability as a driver of interindividual differences in space use. There was large interindividual variation in space use not explained by sex or weight. Our results point to individual specialization in space use in the studied population of S. lilium, most probably linked to food-plant distribution. Individual specialization affects not only which plant species frugivores consume, but also the way they move in space, ultimately with consequences for seed dispersal and landscape connectivity.

As populações naturais não são sistemas homogêneos, mas grupos de indivíduos que ocupam subconjuntos do nicho da espécie. Esse fenômeno é conhecido como especialização individual. Recentemente, vários estudos encontraram evidências de especialização individual na dieta de diferentes espécies de animais. A dieta é uma dimensão crítica do nicho de uma espécie que afeta várias outras dimensões, incluindo o uso do espaço, que foi pouco estudado à luz da especialização individual. No presente estudo, utilizando o paradigma da ecologia do movimento e morcegos Sturnira lilium como modelo, nós buscamos compreender como as preferências alimentares levam os indivíduos de uma mesma população a forragear em diferentes locais e habitats. Dez indivíduos foram rastreados por radiotelemetria em uma área heterogênea de Cerrado. Primeiro, modelamos a variação intraespecífica no uso do espaço como uma rede formada pelos indivíduos e pelos elementos da paisagem visitados por eles. Segundo, desenvolvemos duas novas métricas, o índice de especialização individual espacial (SpatIS) e o índice de especialização individual complementar espacial (SpatICS). Além disso, testamos a disponibilidade de plantas-alimento como um fator determinante das diferenças entre os indivíduos no uso do espaço. Houve grande variação interindividual no uso do espaço não explicada por sexo ou peso. Nossos resultados apontam para a especialização individual no uso do espaço na população estudada de S. lilium, provavelmente ligada à distribuição de plantas-alimento. Concluímos que a especialização individual afeta não apenas quais espécies de plantas os animais frugívoros consomem, mas também a maneira como eles se movem no espaço, o que em última análise tem consequências para a dispersão de sementes e a conectividade da paisagem.

Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed-dispersing ants.

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy-fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.

The Dispersion of Diaspores of Protium icicariba (Burseraceae) - a Networked or Multifactorial System?

The adaptive radiation of the angiosperms was strongly affected by fruit and seed dispersal since the establishment of the seedlings is a fundamental process for the recruitment of juveniles to the populations. Among the species of Burseraceae, seeds with fleshy attachments and high caloric value suggest mammaliochory as an ancestral dispersal way. In Protium icicariba, at the same time as there is a visual pattern typical of ornithochory, with a report of effective demonstration, the diaspores present the highest levels of essential oils of the whole plant, suggesting other dispersion processes by olfactory guided vectors. This work aims to monitor the diasporic dispersal process in P. icicariba in situ, aiming to identify dispersers and to investigate the role of the essential oil in the dispersion of diaspores of this plant species. The natural dispersion was monitored in situ, in weekly campaigns throughout eight months, using visual and photographic records, in daily shifts of six hours, distributed along the dawn, morning, afternoon, dusk, and night. We used both direct observation and continuous picture capturing along 43 days with photographic traps. Mature diaspores removed from pseudocapsules were pooled to determine potential dispersers. Artificial models of the diaspores, in white and green colors, were also used to test hypotheses on the role of scent in the dispersion, added 1%, weight/weight, of the essential oil extracted from the mature diaspores, which chemical composition determined by gas chromatography coupled to mass spectrometry. Besides, the analysis of stomach contents of lizards collected in adjacent area was also performed. In daytime and nighttime monitoring in nature, no vertebrates were recorded dispersing diaspores. The most common was the primary wind-facilitated autochory of diaspores to the substrate, near the plant matrices. Secondarily, workers of the ant species Atta robusta can remove the pseudoarils or move the pyrenes to the anthills. The lizard species Tropidurus torquatus ingests pyrenes with the pseudoarils, and the sclerified pericarp of the pyrene is potentially resistant to chemical action of the digestive juices. Ants and lizards have also accessed the caves with natural diaspores. Concerning the artificial diaspore models, ants accessed, indistinctly, white and the green models that contained essential oils. The lizards accessed the white models, with or without essential oils, and showed insignificant access to green ones, with or without essential oil. The ingestion of pyrenes by lizards was also confirmed through analysis of stomach contents. The aggregate spatial pattern of P. icicariba at the study site, associated with clumps, may be derived from germination in the substrate near the matrices, or in the anthills or after diaspora defecation and / or regurgitation of the lizard, which is a species strongly associated with clumps of this vegetation. As the access to the diaspores by ants and lizards depends on the primary autochory, and no impediments to the germination near to the matrix plant were found, the dispersion is compatible with a multifactorial characteristic of the diplochory.

Bees may drive the reproduction of four sympatric cacti in a vanishing coastal mediterranean-type ecosystem.

BACKGROUND: Sympatric congeneric plants might share pollinators, or each species might avoid competition by evolving specialized traits that generate partitions in pollinator assemblages. In both cases, pollen limitation (a decrease in the quality and quantity of compatible reproductive pollen) can occur, driving the plant mating system to autogamy as a mechanism of reproductive assurance. We assessed the relationships between pollinator assemblages and mating systems in a group of sympatric congeneric plants. We attempted to answer the following questions: (i) How similar are pollinator assemblages among sympatric cactus species? (ii) Which mating systems do sympatric cactus species use? METHODS: We studied sympatric Eriosyce taxa that inhabit a threatened coastal strip in a mediterranean-type ecosystem in central Chile. We performed field observations on four taxa and characterized pollinators during the years 2016 and 2017. We estimated differences in the pollinator assemblages using the Bray-Curtis index. To elucidate the mating systems, we conducted hand-pollination experiments using three treatments: manual cross-pollination, automatic self-pollination, and control (unmanipulated individuals). We tested differences in seed production for statistical significance using Kruskal-Wallis analysis. RESULTS: Eriosyce subgibbosa showed a distinctive pollinator assemblage among the sympatric species that we studied (similarity ranged from 0% to 8%); it was visited by small bees and was the only species that was visited by the giant hummingbird Patagona gigas. Pollinator assemblages were similar between E. chilensis (year 2016 = 4 species; 2017 = 8) and E. chilensis var. albidiflora (2016 = 7; 2017 = 4); however, those of E. curvispina var. mutabilis (2016 = 7; 2017 = 6) were less similar to those of the aforementioned species. E. curvispina var. mutabilis showed the highest interannual variation in its pollinator assemblage (18% similarity). Reproduction in E. subgibbosa largely depends on pollinators, although it showed some degree of autogamy. Autonomous pollination was unfeasible in E. chilensis, which depended on flower visitors for its reproductive success. Both E. chilensis var. albidiflora and E. curvispina var. mutabilis showed some degree of autogamy. DISCUSSION: We observed differences in pollinator assemblages between E. subgibbosa and the remaining Eriosyce taxa, which depend on hymenopterans for pollen transfer. Pollinator assemblages showed considerable interannual variation, especially those of E. subgibbosa (ornithophilous syndrome) and E. curvispina var. mutabilis (melitophilous syndrome). Autogamous reproduction in these taxa may act as a reproductive assurance mechanism when pollinator availability is unpredictable. Our study contributes to improving our understanding of the reproductive systems of ecological interactions between threatened species in a Chilean mediterranean-type ecosystem.

A gradient of pollination specialization in three species of Bolivian Centropogon.

PREMISE: Closely related plant species with overlapping ranges often experience competition for pollination services. Such competition can select for divergence in floral traits that attract pollinators or determine pollen placement. While most species in Centropogon (Campanulaceae: Lobelioideae) have flowers that suggest adaptation to bat or hummingbird pollination, actual pollinators are rarely documented, and a few species have a mix of traits from both pollination syndromes. We studied the pollination biology of a "mixed-syndrome" species and its co-occurring congeners to examine the relationship between floral traits and visitation patterns for Centropogon. METHODS: Fieldwork at two sites in Bolivian cloud forests involved filming floral visitors, quantifying pollen transfer, and measuring floral traits. Stamen exsertion, which determines pollen placement, was measured from herbarium specimens across the geographic range of these species to test for character displacement. RESULTS: Results show a generalization gradient, from primarily bat pollination in white-flowered Centropogon incanus, to bat pollination with secondary hummingbird pollination in the cream-flowered C. brittonianus, to equal reliance on both pollinators in the red-flowered, mixed-syndrome C. mandonis. Pollen transfer between these species is further reduced by differences in stamen exsertion that are accentuated in zones of sympatry, a pattern consistent with character displacement. CONCLUSIONS: Our results demonstrate that key differences in floral color and shape mediate a gradient of specialization in Bolivian Centropogon. Interspecific pollen transfer is further reduced by potential character displacement of a key trait. Broadly, our results have implications for understanding the hyper-diversity of Andean cloud forests, in which multiple species of the same genus frequently co-occur.

The influence of spatial sampling scales on ant-plant interaction network architecture.

Despite great interest in metrics to quantify the structure of ecological networks, the effects of sampling and scale remain poorly understood. In fact, one of the most challenging issues in ecology is how to define suitable scales (i.e., temporal or spatial) to accurately describe and understand ecological systems. Here, we sampled a series of ant-plant interaction networks in the southern Brazilian Amazon rainforest in order to determine whether the spatial sampling scale, from local to regional, affects our understanding of the structure of these networks. To this end, we recorded ant-plant interactions in adjacent 25 × 30 m subplots (local sampling scale) nested within twelve 250 × 30 m plots (regional sampling scale). Moreover, we combined adjacent or random subplots and plots in order to increase the spatial sampling scales at the local and regional levels. We then calculated commonly used binary and quantitative network-level metrics for both sampling scales (i.e., number of species and interactions, nestedness, specialization and modularity), all of which encompass a wide array of structural patterns in interaction networks. We observed increasing species and interactions across sampling scales, and while most network descriptors remained relatively constant at the local level, there was more variation at the regional scale. Among all metrics, specialization was most constant across different spatial sampling scales. Furthermore, we observed that adjacent assembly did not generate more variation in network descriptor values compared to random assembly. This finding indicates that the spatially aggregated distribution of species/individuals and abiotic conditions does not affect the organization of these interacting assemblages. Our results have a direct impact on our empirical and theoretical understanding of the ecological dynamics of species interactions by demonstrating that small spatial sampling scales should suffice to record some patterns commonly found in ant-plant interaction networks in a highly diverse tropical rainforest.

Effects of howler monkey reintroduction on ecological interactions and processes.

Rewilding has been an increasingly popular tool to restore plant-animal interactions and ecological processes impaired by defaunation. However, the reestablishment of such processes has seldom been assessed. We investigated the restoration of ecological interactions following the reintroduction of the brown howler monkey (Alouatta guariba) to a defaunated Atlantic forest site. We expected the reintroduction to restore plant-animal interactions and interactions between howlers and dung beetles, which promote secondary seed dispersal. We estimated the number of interactions expected to be restored by the reintroduction to provide the baseline interaction richness that could be restored. We followed the reintroduced howler monkeys twice a week for 24 months (337 hours total) to assess their diet. We used howler monkey dung in secondary seed dispersal experiments with 2484 seed mimics to estimate the removal rates by dung beetles and collected the beetles to assess community attributes. We compared the potential future contribution of howler monkeys and other frugivores to seed dispersal based on the seed sizes they disperse in other areas where they occur. In 2 years, howler monkeys consumed 60 animal-dispersed plant species out of the 330 estimated. Twenty-one dung beetle species were attracted to experimentally provided dung; most of them were tunnelers, nocturnal, and large-sized (>10 mm). On average 30% (range 0-100%) of the large seed mimics (14 mm) were moved by dung beetles. About 91% of the species consumed by howlers (size range 0.3-34.3 mm) overlapped in seed size with those removed by dung beetles. In our study area, howler monkeys may consume more large-seeded fruit species than most other frugivores, highlighting their potential to affect forest regeneration. Our results show reintroductions may effectively restore ecological links and enhance ecological processes.

Patrones de herbivoría en Vassobia breviflora (Solanaceae): variación en el daño foliar y selección natural mediada por herbívoros / Patterns of herbivory in Vassobia breviflora (Solanaceae): variation in foliar damage and natural selection mediated by herbivorous

Resumen La selección mediada por herbívoros moldea la evolución de los caracteres defensivos en las plantas. El conocimiento acerca del rol de los herbívoros como mediadores de selección es escaso y más aún si se consideran los grupos funcionales de herbívoros. Los objetivos de este trabajo fueron (1) describir la variación en rasgos foliares entre poblaciones, entre plantas dentro de una población y a nivel sub-individual (intra-planta), (2) explorar la relación entre la variación en el nivel de herbivoría y rasgos foliares, (3) determinar la relación entre rasgos foliares y patrones de daño y (4) estimar los regímenes de selección por diferentes grupos funcionales de herbívoros. Realizamos este estudio en cuatro poblaciones de Vassobia breviflora en el noroeste de Argentina (Yungas). Los rasgos foliares considerados fueron: tamaño, área foliar (af), forma (relación longitud/ancho de la hoja; laf) y proporción de área foliar removida (pafr) (N = 1 582 hojas, 57 plantas). Los herbívoros consumieron 15.6 % del área foliar y 76.8 % de la variación en la pafr ocurrió a nivel sub-individual. El patrón de daño fue dominado por herbívoros cortadores (70 %), seguido de un patrón de herbivoría punteada (22 %), 5 % mixto y 1 % minador. Se detectó selección no lineal para laf (γii = -0.180, EE = 0.76, P < 0.05), y selección correlacional entre el daño cortador y af (γij = -1.297, SE = 0.62, P < 0.05) y entre el daño punteado y af (γij= -1.130, SE=0.76, P < 0.05). La selección natural favoreció plantas con hojas pequeñas y alta remoción foliar y hojas grandes con menor daño y se detectó selección en contra de hojas grandes con mayor daño. Además, deducido de la relación entre el tipo de daño y la adecuación relativa, la selección favorecería el daño punteado por sobre el cortador. Las plantas resolverían el conflicto con los herbívoros según el tipo de daño y la selección natural regularía el despliegue foliar como una estrategia para lidiar con la diversidad de herbívoros.(AU)

Abstract Herbivore mediated-selection shapes the evolution of defensive plant traits. Knowledge about the role of herbivores as mediators of selection is scarce and even more if herbivore functional groups are considered. The objectives of this work were (1) to describe the variation in foliar traits between populations and both between and intra-plants within a population, (2) to explore the relationship between the variation in the herbivory level and foliar traits, (3) to determine the relationship between leaf traits and damage patterns and (4) estimate the selection regimes by different herbivore functional groups. We conducted this study in four populations of Vassobia breviflora in Northwestern Argentina (Yungas). The foliar traits considered were size, leaf area (af), shape (leaf length / width ratio; laf) and proportion of leaf area removed (pafr) (N = 1 582 leaves, 57 plants). The herbivores consumed 15.6 % of the leaf area and 76.8 % of the variation in the pafr occurred at the sub-individual level. The damage pattern was dominated by cutter herbivores (70 %), followed by a dotted herbivory pattern (22 %), mixed 5 % and 1 % miner. Nonlinear selection was detected for laf (γii = -0.180; EE = 0.76; P < 0.05), and correlational selection between the cutter damage and af (γij = -1.297; SE = 0.62; P < 0.05) and between the dotted damage and af (γij = -1.130; SE = 0.76; P < 0.05). Natural selection favored plants with small leaves and high foliar removal and large leaves with less damage and selection against larger leaves with greater damage was detected. In addition, deduced from the relationship between the damage type and the relative fitness, the selection would favor the dotted damage over the cutter one. The plants would resolve the conflict with the herbivores according to the damage type and natural selection would regulate the foliar display as a strategy to deal with the herbivore diversity.(AU)

Evolution of pollination by frugivorous birds in Neotropical Myrtaceae.

Bird pollination is relatively common in the tropics, and especially in the Americas. In the predominantly Neotropical tribe Myrteae (Myrtaceae), species of two genera, Acca and Myrrhinium, offer fleshy, sugary petals to the consumption of birds that otherwise eat fruits, thus pollinating the plants in an unusual plant-animal interaction. The phylogenetic position of these genera has been problematic, and therefore, so was the understanding of the evolution of this interaction. Here we include new sequences of Myrrhinium atropurpureum in a comprehensive molecular phylogeny based on a balanced sample of two plastid and two nuclear markers, with the aim of providing the historical framework of pollination by frugivorous birds in Myrteae. We developed 13 flower and inflorescence characters that comprehensively depict the macroscopic morphological components of this interaction. Bayesian and parsimony phylogenies concur in placing both Acca and Myrrhinium in a clade with Psidium species; with Myrrhinium sister to Psidium. Mapping of morphological characters indicated some degree of convergence (e.g., fleshy petals, purplish display) but also considerable divergence in key characters that point to rather opposing pollination strategies and also different degrees of specialization in Acca versus Myrrhinium. Pollination by frugivorous birds represents a special case of mutualism that highlights the evolutionary complexities of plant-animal interactions.

Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant-plant mutualistic networks in the Caatinga, a Brazilian dry forest.

Anthropogenic disturbance and climate change might negatively affect the ecosystem services provided by mutualistic networks. However, the effects of such forces remain poorly characterized. They may be especially important in dry forests, which (1) experience chronic anthropogenic disturbances (CADs) as human populations exploit forest resources, and (2) are predicted to face a 22% decline in rainfall under climate change. In this study, we investigated the separate and combined effects of CADs and rainfall levels on the specialization of mutualistic networks in the Caatinga, a seasonally dry tropical forest typical of north-eastern Brazil. More specifically, we examined interactions between plants bearing extrafloral nectaries (EFNs) and ants. We analysed whether differences in network specialization could arise from environmentally mediated variation in the species composition, namely via the replacement of specialist by generalist species. We characterized these ant-plant networks in 15 plots (20 × 20 m) that varied in CAD intensity and mean annual rainfall. We quantified CAD intensity by calculating three indices related to the main sources of disturbance in the Caatinga: livestock grazing (LG), wood extraction (WE) and miscellaneous resource use (MU). We determined the degree of ant-plant network specialization using four metrics: generality, vulnerability, interaction evenness and H2 '. Our results indicate that CADs differentially influenced network specialization: we observed positive, negative, and neutral responses along LG, MU and WE gradients, respectively. The pattern was most pronounced with LG. Rainfall also shaped network specialization, markedly increasing it. While LG and rainfall were associated with changes in network species composition, this trend was not related to the degree of species specialization. This result suggests that shifts in network specialization might be related to changes in species behaviour, not species composition. Our study highlights the vulnerability of such dry forest ant-plant networks to climate change. Moreover, dry forests experience highly heterogeneous anthropogenic disturbances, creating a geographic mosaic of selective forces that may shape the co-evolution of interactions between ants and EFN-bearing plants.

Indirect effects of ecosystem engineering combine with consumer behaviour to determine the spatial distribution of herbivory.

Ecosystem engineers alter environments by creating, modifying or destroying habitats. The indirect impacts of ecosystem engineering on trophic interactions should depend on the combination of the spatial distribution of engineered structures and the foraging behaviour of consumers that use these structures as refuges. In this study, we assessed the indirect effects of ecosystem engineering by a wood-boring beetle in a neotropical mangrove forest system. We identified herbivory patterns in a dwarf mangrove forest on the archipelago of Twin Cays, Belize. Past wood-boring activity impacted more than one-third of trees through the creation of tree holes that are now used, presumably as predation or thermal refuge, by the herbivorous mangrove tree crab Aratus pisonii. The presence of these refuges had a significant impact on plant-animal interactions; herbivory was more than fivefold higher on trees influenced by tree holes relative to those that were completely isolated from these refuges. Additionally, herbivory decreased exponentially with increasing distance from tree holes. We use individual-based simulation modelling to demonstrate that the creation of these herbivory patterns depends on a combination of the use of engineered tree holes for refuge by tree crabs, and the use of two behaviour patterns in this species-site fidelity to a "home tree," and more frequent foraging near their home tree. We demonstrate that understanding the spatial distribution of herbivory in this system depends on combining both the use of ecosystem engineering structures with individual behavioural patterns of herbivores.