Article

Comparing seed dispersal effectiveness by frugivores at the community level

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Abstract

Seed dispersal effectiveness (SDE) is the contribution of dispersers to plant recruitment and is estimated as the product of the number of seeds dispersed (quantity) and the probability of recruitment of each dispersed seed (quality). Although SDE is a key concept in seed dispersal ecology, few studies estimate SDE and none has a community approach. Oceanic islands, with simple communities, are ideal for this purpose. In this study, we compared the SDE of the main types of dispersers (lizards and passerine birds) at the community level in a given habitat. We estimated SDE using a stochastic simulation model parameterized with empirical data on quantity and quality components measured throughout the recruitment process. Although lizards are highly frugivorous and their density was c. 20 times higher than that of birds, lizards and birds dispersed a similar quantity of seeds. This may be due to lower intake of seeds by lizards due to their slower metabolism (c. 20 times lower than birds). This low metabolic rate limits the importance of lizards as seed dispersers, but it is compensated by extraordinarily high lizard densities in the study area (c. 9600 individuals/km2). High densities of lizards are typical of islands, and this helps to explain why dispersal by lizards seems mainly an island phenomenon. Birds and lizards showed functional complementarity, especially regarding seed dispersal distribution patterns. In fact, lizards dispersed more seeds in shrublands and open sites, and birds in woodlands and beneath canopies, with their joint contribution helping to maximize recruitment. Lizards provided higher SDE than birds for 7 out of 11 plant species. The disperser with a higher quantity for a given plant generally had the higher quality, and plants could be classified as bird- or lizard-dependent for dispersal. This dependence increased when considering SDE instead of dispersal quantity only. Moreover, quality was a better predictor of SDE than quantity, which should be considered when parameterizing interaction networks, as this might affect inferences about their architecture.

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... However, low functional equivalence has been found in other Canarian plant species that require the service of opportunistic vertebrates for other types of mutualism, such as seed dispersal. In these cases, birds and lizards occupy so disparate positions in the landscape of dispersal effectiveness, that species are regarded as mostly bird dependent or lizard dependent ( González-Castro et al. 2015). Outside the Macaronesian Region, the inclusion of opportunistic birds and lizards in pollinator assemblages is relatively frequent in insular floras around the world (Olesen & Valido 2004). ...
... The interaction between the dispersal patterns of birds and lizards generates a wider range in pollination effectiveness that assures plant reproduction and, at the same time, a wider variation in the reproductive consequences. Further, the importance of lizards as mutualists may be even higher in plant populations where birds are scarce but lizards reach high densities, such as arid habitats with reduced vegetation cover (e.g., Traveset & Sáez 1997;Olsson et al. 2000;Hansen et al. 2007;Valido et al. 2011;Siverio & Rodríguez-Rodríguez 2012;González-Castro et al. 2015). Thus, a pollinator important in one plant population may be less important in another, and this spatial variation in mutualistic assemblages surely alters landscapes of pollination effectiveness circumstantially (i.e. ...
... Plant-pollinator interactions are diverse and complex, being difficult to draw general conclusions and predictions, especially when we do not consider life-history traits of interacting species. The life history of the different systems of plant-animal mutualisms has proven to be important to understand their dynamics (e.g., Paige & Whitham 1987;Brittain & Potts 2011;González-Castro et al. 2015). In our case, the opportunistic nectarivorous behaviour of birds and lizards and their contrasting life forms helped us understand their consequences on plant reproductive success. ...
Thesis
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The consequences of mutualistic plant-animal interactions on plant reproductive success depend on the animal’s effectiveness and the context in which the mutualism occurs. The present thesis is about the interplay between these two aspects in the mutualism of pollination. We try to meet the challenge with a particular group of pollinators, opportunistic nectar-feeding vertebrates, in a particular context, oceanic islands. Due to their intrinsic ecological conditions, oceanic islands favour the appearance of depauperate and disharmonic assemblages of opportunistic pollinators, whose effectiveness and level of context dependence may differ significantly from those of continental systems. In the concrete case of the Canary Islands, passerine birds and lacertid lizards are frequent floral visitors of native flora, but their pollination ecology has remained almost unknown. For this reason, the present thesis follows a dual objective: first to experimentally demonstrate the effectiveness of birds and lizards as pollinators (chapters 2-3) and analyse the potential differences between both functional groups (chapter 4), to then understand how their benefits on plant fitness vary under the presence of antagonists (chapters 5-6).
... Most plant species, especially in temperate and boreal regions, are dispersed by birds and mammals (Albrecht et al., 2013;. Frugivore species within a community may complement their seed dispersal services not only by specializing on different fleshy-fruited plant species (González-Castro et al., 2015;González-Varo et al., 2014), but also by contributing differently to seed arrival to different microhabitats and by dispersing seeds over short or long distances within the dispersal kernel McConkey & Brockelman, 2011;Rumeu et al., 2020). In addition, sympatric frugivore species may contribute differently to the seed rain across the fruiting season (González-Varo et al., 2019). ...
... All of these factors can have direct consequences on the quantity and quality of the seed dispersal services provided by each species (González-Varo et al., 2019;Jordano et al., 2007). This spatio-temporal complementarity in seed dispersal services may be essential for plant recruitment and, yet, is still poorly understood (but see González-Castro et al., 2015;González-Varo et al., 2019). ...
... The quantity of dispersed seeds has been traditionally considered a better surrogate of the total effect of frugivores on plants than the quality of seed dispersal (Vázquez et al., 2005; but see also González-Castro et al., 2015). Therefore, many studies have focused on fruit removal rates as a proxy for the effect of different frugivore species on plant recruitment (e.g. ...
Article
Endozoochory is an important ecosystem function that, in temperate and boreal regions, is carried out mainly by birds and mammals. Due to their different quantitative and qualitative contributions to seed dispersal, these animals usually differ in their effectiveness as seed dispersers. However, there is still little information about how spatio‐temporal differences in frugivory between birds and mammals may create complementarity in their seed dispersal services. We investigated the complementarity of seed dispersal services provided by avian and mammalian seed dispersers of bilberry Vaccinium myrtillus in an alpine ecosystem, the Tatra Mountains (Poland). We collected bird droppings and mammal scats containing bilberry seeds in coniferous forests and alpine meadows. Birds were identified by DNA barcoding techniques while mammals were visually assigned in the field. We analysed the effects of habitat, microhabitat and timing of seed dispersal on the quantitative contributions of each species to the total seed rain and conducted ex situ germination experiments to assess the quality of the seed dispersal services. At least 13 bird and three mammal species dispersed bilberry seeds in the Tatra Mountains. Two species of thrushes—song thrushes Turdus philomelos and fieldfares T. pilaris, brown bears Ursus arctos and red foxes Vulpes vulpes were the most effective dispersers. Quantitative and qualitative contributions to seed dispersal differed between birds and mammals. Mammals, particularly brown bears, dispersed the majority of bilberry seeds in both habitats. The total seed rain provided by birds and mammals differed according to the habitat, microhabitat and timing of seed dispersal. Birds dispersed most seeds in the middle of the fruiting season and within the forest, while seed dispersal by mammals peaked in the upper meadows and at the end of the season. Seeds defecated by birds had higher probability to germinate as their droppings contained less seeds and were defecated in more suitable microhabitats than seeds defecated by mammals. Synthesis. Despite differences in the quantity and quality of seed dispersal, both bird and mammal species are effective bilberry dispersers. Complementary seed dispersal by these two groups guarantees the arrival of bilberry seeds to different microhabitats suitable for germination and during the entire fruiting season, maximizing the chances of bilberry seedling recruitment. La endozoocoria es una función ecosistémica esencial que en regiones templadas y boreales es llevada a cabo principalmente por aves y mamíferos. Debido a diferencias en la cantidad y calidad de los procesos dispersivos que proporcionan, estos animales difieren en su efectividad como dispersores de semillas. Sin embargo, existe todavía poca información sobre cómo las diferencias espacio‐temporales en frugivoría entre aves y mamíferos generan complementariedad en los procesos de dispersión de semillas llevados a cabo por estos dos grupos de animales. En este trabajo investigamos la complementariedad de los servicios de dispersión de semillas proporcionados por consumidores de frutos de arándano Vaccinium myrtillus en un ecosistema alpino, los montes Tatra (Polonia). Durante la época de fructificación del arándano recogimos excrementos de aves y mamíferos tanto en bosques de coníferas como en prados alpinos. Asignamos en el campo cada excremento de mamífero a una especie y extrajimos material genético de los excrementos de ave en el laboratorio para su posterior identificación. Analizamos los efectos del hábitat (bosque o prado), el microhábitat (sustrato de deposición de los excrementos) y el periodo dentro de la época de fructificación (de julio a octubre) en las contribuciones de cada especie a la lluvia de semillas. Además, realizamos experimentos de germinación ex‐situ para evaluar la calidad de los servicios dispersivos proporcionados por cada especie. Al menos trece especies de aves y tres de mamíferos dispersaron semillas de arándano en los montes Tatra. El zorzal común Turdus philomelos, el zorzal real T. pilaris, el oso pardo Ursus arctos y el zorro rojo Vulpes vulpes fueron los dispersores más efectivos. Aves y mamíferos difirieron en sus contribuciones cuantitativas y cualitativas a la dispersión de semillas. Los mamíferos, en particular el oso pardo, dispersaron la mayoría de las semillas en ambos hábitats. La lluvia de semillas proporcionada por aves y mamíferos difirió además según el hábitat, el microhábitat y el periodo. Las aves dispersaron la mayoría de las semillas al comienzo y mitad de la época de fructificación y dentro del bosque, mientras que la dispersión de semillas por parte de los mamíferos alcanzó su punto máximo en los prados alpinos y al final de la temporada. Las semillas defecadas por aves tuvieron una mayor probabilidad de germinar ya que en general sus excrementos contenían menos semillas y fueron encontrados en microhábitats más adecuados para la germinación. Síntesis: A pesar de diferencias tanto en la cantidad como en la calidad de las semillas dispersadas, distintas especies de aves y mamíferos son dispersoras efectivas del arándano. La complementariedad en los procesos dispersivos proporcionados por estos dos grupos garantiza la llegada de semillas de arándano a diferentes microhábitats aptos para la germinación y a lo largo de toda la época de fructificación, lo que maximiza las posibilidades de germinación y establecimiento de nuevas plántulas. Despite differences in the quantity and quality of seed dispersal, both bird and mammal species are effective bilberry dispersers. Complementary seed dispersal by these two groups guarantees the arrival of bilberry seeds to different microhabitats suitable for germination and during the entire fruiting season, maximizing the chances of bilberry seedling recruitment.
... Moreover, species with similar SDE values suggest that these have similar consequences for the interaction, and may be thus considered functional equivalent. 7 Despite the increasing number of studies assessing quantity and quality components of SDE in birds, [13][14][15][16][17] studies have only made qualitative judgements about whether bird species are functional equivalent, based on the relative position and clustering of species onto the SDE landscape. 12,14,18 Therefore, a method to identify functional equivalent species within frugivore assemblages is still lacking. ...
... 7 Despite the increasing number of studies assessing quantity and quality components of SDE in birds, [13][14][15][16][17] studies have only made qualitative judgements about whether bird species are functional equivalent, based on the relative position and clustering of species onto the SDE landscape. 12,14,18 Therefore, a method to identify functional equivalent species within frugivore assemblages is still lacking. Here, I apply a statistical method based on niche theory to identify functional equivalent species in terms of SDE. ...
... This is because plantfrugivore interactions have been extensively studied by recording foraging visits during observations on focal plants. 14,15,26,37,39 Nevertheless, intraspecific SDE may be quantified from individual birds, which allows generalizing the framework regardless of the method used in the field. Sources of bird intraspecific variation in SDE, such as sexual dimorphism (males vs females), age (adults vs juveniles), and individual specialization (generalists vs specialists), have implications for the interaction. ...
Article
Seed dispersal by birds is a pivotal ecosystem function worldwide; yet, the rapid and ongoing global biodiversity loss poses a major threat to this essential ecosystem service. Seed dispersal effectiveness (SDE) is a key outcome of the interaction, represented by the product of seed dispersal quantity (number of seed dispersed) and quality (probability of recruitment of dispersed seeds). Therefore, identifying functional equivalent species in terms of SDE should become a key issue for bird conservation, since the effects of local extinctions on seed dispersal services may be weakened by remaining equivalent species. However, a method to quantitatively identify functional equivalent species in frugivorous bird assemblages is still lacking. To estimate SDE overlap between seed dispersers and assess whether two species may be functionally equivalent, I apply a novel nonparametric niche overlap index based on kernel functions and null models to test its statistical significance. For each bird species, I account for intraspecific variation in seed dispersal effectiveness to obtain a distribution of seed dispersal effectiveness values, an often neglected source of variation in seed dispersal assemblages. Non-significant differences in seed dispersal effectiveness overlap support the hypothesis that two species are functional equivalent, thus playing similar functional roles. The model proposed is applicable to any other quantity or quality component and is independent from the method or sampling design used to quantify SDE. The identification of functional equivalent species in seed dispersal assemblages adds to the theoretical framework of seed dispersal effectiveness and offers new insights into the ecology of the seed dispersal service provided by birds.
... Rother et al., 2016). Frugivores may vary in size, feeding behavior, mobility, digestive capacity, habitat requirements and home range, all of which influence the number of seeds ingested, seed treatment and finally, the quality of dispersal (Wheelwright, 1985;Owen-Smith, 1988;Jordano, 2000;Morales et al., 2013;González-Castro et al., 2015;Blendinger, 2017). It is particularly difficult to disentangle the role of different species in highly diversified frugivore assemblages with poor empirical data available, such as is typical from most tropical locations. ...
... For instance, the low availability of food resources may force some frugivores to feed on non-prefered fruits in some habitats or years, affecting the SDE of plants (Pizo et al., 2005;Calviño-Cancela and Martín-Herrero, 2009;Schupp et al., 2010;Perea et al., 2013;Lavabre et al., 2016). At different locations, plants may receive visits from a set of dispersers that differs in relative abundance or composition (Pizo, 1997;Perea et al., 2013;Blendinger, 2017), affecting quantity and quality of seed dispersal (Vázquez et al., 2005;Schupp et al., 2010;González-Castro et al., 2015). Likewise, spatial variation in environmental conditions such as soil type, humidity and shading can also affect seed germination and seedling recruitment. ...
... Since the effects of ants on nest soil properties that benefit seedling performance are more commonly found in vegetation growing under dry climate and poor soil conditions (Farji-Brener and Werenkraut, 2017), we expect that ants show a higher contribution to SDE in savanna than in forest (Hoffmann et al., 2004). Finally, we expect that ecological specialization, if important in our system, may lead to a positive correlation between quantity and quality components of SDE (González-Castro et al., 2015). We compared the number of seeds dispersed by each one of several bird and ant species in the two habitats and their possible delayed consequences combining experimental and modeling approaches. ...
Article
Diversified assemblages of frugivores interact with fruits/seeds in tropical environments. Species within assemblages vary largely in body size, abundance, seed treatment and places of seed deposition, with possible delayed consequences for seed dispersal and plant regeneration. The variable outputs of the interaction may be magnified when considering different habitats and diplochoric plants that include more than one agent in subsequent steps of dispersal. Here we compared the contribution of birds and ants to the seed dispersal effectiveness (SDE) of two species of Erythroxylum shrubs that grow in Atlantic forest and Cerrado savannas in Brazil. We compared the number of seeds dispersed by each one of 16 bird and 30 ant species and their delayed consequences for seed germination and seedling survival combining experimental and modeling approaches. We observed shifts in the role of different dispersal agents between habitats, with birds being more important in the forest while ants are highlighted in the savanna. Quantity and quality components of SDE were not correlated, but large body size emerged as an important trait driving the quantity (birds) and quality (ants) components of SDE. A high diversified assemblage of dispersal agents does not always result in redundant effects for SDE, with some species consistently providing better dispersal than others and several opportunities for complementary effects. Therefore, even in diversified assemblages operating in diplochoric dispersal systems, there is the opportunity for ecological specialization.
... Here we experimentally assessed the impact of body-size reduction in the species Gallotia galloti (endemic to Tenerife and La Palma, Canary Islands) on the seed germination patterns of two fleshy-fruited plant species Rubia fruticosa (Rubiaceae) and Withania aristata (Solanaceae). These two native plant species are locally abundant at lowlands and are mainly dispersed by Gallotia lizards and a few passerine bird species (Sylvia atricapilla, S. melanocephala, Turdus merula, and Erithacus rubecula) (González-Castro et al., 2015). For testing the hypothesis that intra-specific downsizing of Gallotia lizards may trigger negative impacts on seed dispersal, seed germination curves and the germination percentage of seeds defecated by large-bodied and small-bodied individuals were compared for the two plant species. ...
... Average diameter of fruits is 9.6 mm (Valido and Nogales, 1994), average seed diameter is 3.8 ± 0.36 mm (mean ± SD; present study) and seed mass is 0.01 g (Valido and Nogales, 1994). Fruits of these two species are often consumed by Canarian lizards in the lowland shrubs and the thermophilous woodland of the Canaries (Rodríguez et al., 2008;González-Castro et al., 2015). ...
... In fact, the effect of the gut passage was negative, as indicated by a faster germination and a higher germination percentage for control seeds. This is not surprising considering the similar results in previous studies for the same plant species and vegetation (González-Castro et al., 2015; but see contrasting results in Valido and Nogales, 1994 for W. aristata in xerophytic shrublands). The observed pattern may be explained as due to the digestive and mechanical action of lizard guts on seed coats, reducing germinability. ...
... In general, lizards tend to consume plant material in a generalist way (Rodríguez, Nogales, Rumeu, & Rodríguez, 2008) and preferentially use open microhabitats. In contrast, birds select fruits and often feed on uncommon species (Carlo & Morales, 2016;González-Castro, Yang, & Carlo, 2019), tending to use covered areas (González-Castro, Calviño-Cancela, & Nogales, 2015). Therefore, we expected that the two types of dispersers would provide distinct community-level dispersal services. ...
... In contrast, Gallotia galloti shows a generalist foraging behaviour long retention times and preferentially uses open areas (González-Castro, Calviño-Cancela, et al., 2015). For such a reason, this study is focused on comparison between two clearly different types of seed dispersers: lizards and birds. ...
... We adapted the model developed by González-Castro, Calviño-Cancela, et al. (2015), in order to parameterize the behavioural rules of frugivores based on the data available. The previous version was a stochastic transition probability model that connected all stages of plant recruitment, from fruit production to 1-year-old seedlings. ...
Article
The behavioural complementarity of fruit‐eating animals is thought to exert a key role in plant community assembly. However, a mechanistic understanding of the causal links between the two processes is still lacking. This study assesses if complementarity between dispersers in feeding and microhabitat‐use behaviour enhances community‐scale dispersal services, resulting in a more diverse community of seedlings. We used a Bayesian approach to connect a comprehensive database of seed dispersal effectiveness at a community scale with a transition probability model that accounts for behavioural complementarity. Our model system was the thermosclerophyllous shrubland of the Canary Islands. There, fleshy‐fruited plants rely on two types of frugivores: lizards and birds. Lizards consumed all plant species and preferentially used open areas; whereas birds foraged for small single‐seeded fruits and dispersed their seeds beneath plants. Through feeding on different sets of plants, they generated a rich seed‐rain community. By diversifying the microhabitat of deposition, more species could find suitable recruitment sites. Distinct foraging and microhabitat‐use choices led to complementary dispersal services. Lizards ensured that all plant species were present in the seedling community, while birds promoted a more even distribution of them. As a result, diversity in the community of seedlings was enhanced. Overall, our work underscores that behavioural complementarity promotes diversity in the early‐regenerating plant communities. These enhanced dispersal services rely on the presence of all functional groups. Thus, in communities where frugivores display unique behaviours, preserving a diverse community of dispersers should be a conservation target.
... Gut passage of seeds by frugivores typically increases germination, although existing studies that focus on a subset of plant-frugivore species pairs within a network have shown that the magnitude and sign of the effect can vary substantially among frugivore and plant species (Genrich et al., 2016;Traveset, Robertson, & Rodríguez-Pérez, 2007;Traveset & Verdú, 2002). Recent studies emphasize the need to adopt a community-level focus to understand the degree of this variation and the sources that cause it (González-Castro, Calviño-Cancela, & Nogales, 2015;Nogales et al., 2017). Oceanic islands, which typically have lower species diversity than mainland locations, offer tractable settings to study mutualistic interactions at a community scale (Kaiser-Bunbury et al., 2010). ...
... Oceanic islands, which typically have lower species diversity than mainland locations, offer tractable settings to study mutualistic interactions at a community scale (Kaiser-Bunbury et al., 2010). Recent studies in the Balearic and Galapagos islands have compared germination of seeds collected from scat to seeds removed from fruits to assess the effects of two or more frugivore functional groups on multiple plant species (González-Castro et al., 2015;Nogales et al., 2017), greatly advancing our understanding of community-level variation in gut passage effects among the functional groups of seed dispersers present at a study location. ...
... So long as the distinction between seed dispersers and seed predators was in place (which in this case involved complete seed predation, which may often not be the case; Shiels, 2011), we would have reached appropriate inferences by grouping the dispersers in this system a priori as "passerines/fruit dove," "small birds/large birds," or more simply "birds." The grouping of species into functional groups is already widely used in seed dispersal research, especially for considering differences in effectiveness of different groups of dispersers (González-Castro et al., 2015;Nogales et al., 2017). Our results emphasize that functional groupings for gut passage effects should be based on digestive morphology and diet rather than loosely on phylogeny and body size, which would have grouped the Alopecoenas ground dove and Ptilinopus fruit dove in this study. ...
Article
Full-text available
1.Current understanding of mutualistic networks is grounded largely in data on interaction frequency, yet mutualistic network dynamics are also shaped by interaction quality—the functional outcomes of individual interactions on reproduction and survival. The difficulty of obtaining data on functional outcomes has resulted in limited understanding of functional variation among a network's pairwise species interactions, of the study designs that are necessary to capture major sources of functional variation, and of predictors of functional variation that may allow generalization across networks. 2.In this community‐scale study, we targeted a key functional outcome in plant‐frugivore networks: the impact of frugivore gut passage on seed germination. We used captive frugivore feeding trials and germination experiments in an island ecosystem, attaining species‐level coverage across all extant native frugivores and the plants they consume to 1) assess sources of functional variation, 2) separate effects of pulp removal from those of scarification via gut passage, and 3) test trait‐based correlates of gut passage effect sizes. 3.We found antagonistic seed predation effects of a frugivore previously assumed to be a seed disperser, highlighting the need to consider functional outcomes rather than interaction frequency alone. The other frugivores each exhibited similar impacts for individual plant species, with benefits primarily caused by pulp removal rather than scarification, supporting the use of animal functional groups in this context. In contrast, plant species varied widely in impacts of gut passage on germination. Species with smaller seeds and more frugivore partners had larger benefits of gut passage, showing promise for network metrics and functional traits to predict functional variation among plants. 4.Synthesis. Combining network and demographic approaches, we assessed the degree and sources of variation in a key functional outcome of plant‐frugivore interactions across an entire network. Using a detailed study design, our work shows how simpler study designs can capture primary sources of functional variation and that functional traits and network metrics may allow generalization across networks. Efficiently measuring and generalizing sources of functional variation within mutualistic networks will strengthen our ability to model network dynamics and predict mutualist responses to global change. This article is protected by copyright. All rights reserved.
... One method to achieve this goal is to combine different species of seed dispersers that share similar traits into functional groups (e.g. Dennis & Westcott, 2006;Jordano et al., 2007;Moran & Catterall, 2010;González-Castro, Calviño-Cancela & Nogales, 2015). A frequent problem, though, is large intraspecific variation in morphological, physiological, and behavioural traits (Bolnick et al., 2003;Sih, Bell & Johnson, 2004). ...
... Such variation is often treated as random noise that needs to be eliminated or controlled statistically in attempts to identify 'true' patterns. However, mounting evidence suggests that differences among individuals should be embraced as a potential driver of patterns in population and community ecology (Violle et al., 2012;Wolf & Weissing, 2012;González-Varo & Traveset, 2016;Pennisi, 2016;Moran, Wong & Thompson, 2017). Thus, dependence on species averages is recognized as a limitation of current frameworks of plant-seed disperser interactions (Schupp et al., 2017). ...
... The key point is that if some individuals contribute disproportionately to seed dispersal or are more likely to provide rare dispersal outcomes, then relying on averages will provide not only an incomplete picture of dispersal but will likely move us away from understanding its mechanistic underpinning (Benton, Plaistow & Coulson, 2006;McConkey & O'Farrill, 2015;Poisot, Stouffer & Gravel, 2015;González-Varo & Traveset, 2016). There are several reasons why this is likely to happen. ...
Article
Full-text available
Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context-dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed-dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed-dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex-specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best-documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed-dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed-dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal-mediated seed dispersal.
... The dominant frugivorous animals in this community are the resident passerines Sylvia atricapilla, Sylvia melanocephala, Erithacus rubecula, Turdus merula and the endemic lizard Gallotia galloti. The study site is described in detail in González-Castro et al. (2015a). ...
... An interaction frequency network was built by combining data from faeces and regurgitations of frugivorous animals and data from seed traps (González-Castro et al. 2015a). In the case of passerines, we estimated the number of interactions as following: ...
... To estimate the number of seeds dispersed per hectare by birds and lizards ( N N p b p l � & ), we randomly placed 1 m 2 seed traps (n = 80) over the study area, covering all habitat and microhabitat types and checking them monthly (González-Castro et al. 2015a). Traps were 2 cm deep, made of green plastic mesh (1 mm aperture) to retain faeces (and regurgitations) of all frugivores and provide good drainage. ...
Article
Interaction frequency is the most common currency in quantitative ecological networks, although interaction quality can also affect benefits provided by mutualisms. Here, we evaluate if interaction quality can modify network topology, species' role and whether such changes affect community vulnerability to species loss. We use a well-examined study system (bird–lizard and fleshy-fruited plants in the ‘thermophilous' woodland of the Canary Islands) to compare network and species-level metrics from a network based on fruit consumption rates (interaction frequency, IF), against networks reflecting functional outcomes: a seed dispersal effectiveness network (SDE) quantifying recruitment, and a fruit resource provisioning network (FRP), accounting for the nutrient supply of fruits. Nestedness decreased in the FRP and the SDE networks, due to the lack of association between fruit consumption rates and 1) nutrient content and; 2) recruitment at the seed deposition sites, respectively. The FRP network showed lower niche overlap due to resource use complementarity among frugivores. Interaction evenness was lower in the SDE network, in response to a higher dominance of lizards in the recruitment of heliophilous species. Such changes, however, did not result in enhanced vulnerability against extinctions. At the plant species level, strength changed in the FRP network in frequently consumed or highly nutritious species. The number of effective partners decreased for species whose seeds were deposited in unsuitable places for recruitment. In frugivores, strength was consistent across networks (SDE vs IF), showing that consumption rates outweighed differences in dispersal quality. In the case of lizards, the increased importance of nutrient-rich species resulted in a higher number of effective partners. Our work shows that although frequency strongly impacts interaction effects, accounting for quality improves our inferences about interaction assembly and species role. Thus, future studies including interaction outcomes from both partners' perspectives will provide valuable insights about the net effects of mutualistic interactions.
... Plant species often interact with several dispersers and those dispersers are likewise interacting with many species of plants. Therefore, disperser roles may differ among plant species such as when a plant relies on a group of dispersers for long-distance seed dispersal [9,10] while other plants receive little or no benefit from those same dispersers. Taking a community approach to seed dispersal studies will clarify the changing dispersal patterns for a broad array of plant -animal interactions and allow development of empirical approaches that efficiently characterize key sources of variation in dispersal. ...
... To overcome the difficulties of studying all speciesspecific interactions within a community, efforts have focused on patterns of dispersal for different plant and animal functional types [9][10][11][12][13]. These efforts have started to reveal some community-level patterns such as how disperser body size and plant seed mass influence the dispersal process [10,12,14]. ...
... To overcome the difficulties of studying all speciesspecific interactions within a community, efforts have focused on patterns of dispersal for different plant and animal functional types [9][10][11][12][13]. These efforts have started to reveal some community-level patterns such as how disperser body size and plant seed mass influence the dispersal process [10,12,14]. However, clumping species into functional groups may mask important differences in seed dispersal performed by dispersers of the same functional type or dispersal may vary independently of a given plant functional trait [15]. ...
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Frugivores play differing roles in shaping dispersal patterns yet seed dispersal distance is rarely quantified across entire communities. We model seed dispersal distance using gut passage times and bird movement for the majority (39 interactions) of known bird–tree interactions on the island of Saipan to highlight differences in seed dispersal distances provided by the five avian frugivores. One bird species was found to be a seed predator rather than a disperser. The remaining four avian species dispersed seeds but differences in seed dispersal distance were largely driven by interspecific variation in bird movement rather than intraspecific variation in gut passage times. The median dispersal distance was at least 56 m for all species-specific combinations, indicating all species play a role in reducing high seed mortality under the parent tree. However, one species—the Micronesian Starling—performed 94% of dispersal events greater than 500 m, suggesting this species could be a key driver of long-distance dispersal services (e.g. linking populations, colonizing new areas). Assessing variation in dispersal patterns across this network highlights key sources of variation in seed dispersal distances and suggests which empirical approaches are sufficient for modelling how seed dispersal mutualisms affect populations and communities.
... Dispersion can vary from a null random dispersion (Figure 1a), to a uniform (regular, even, over-dispersed) dispersion, where effectiveness values are separated from each other on the landscape more than expected by random processes (Figure 1b), and a clumped (aggregated, patchy) dispersion, where the effectiveness values cluster in statistically distinct groups having similar values of effectiveness ( Figure 1c). Clumped spatial patterns indicate that there are distinct groups of species that have similar effects on the fitness of their partner, revealing the occurrence of functional equivalence within clustered groups of interacting organisms (Calviño-Cancela & Martín-Herrero, 2009;González-Castro et al., 2015;Palacio, 2019). In contrast, over-dispersed effectiveness landscapes indicate that different interacting organisms have very distinct effects on the fitness of their partner, and consequently they are not interchangeable. ...
... Variation in per-visit efficiency (QLC) is a precondition for specialisation (Schemske & Horvitz, 1984). (González-Castro et al., 2015), a feature resulting from natural selection having shaped those traits that preferentially attract the highest quality interacting species (similar to Stebbins (1970)'s 'most effective pollinator principle'). In contrast, a negative component correlation is likely associated with generalised interactions (Calviño-Cancela & Martín-Herrero, 2009;González-Castro et al., 2015;Palacio, 2019). ...
... (González-Castro et al., 2015), a feature resulting from natural selection having shaped those traits that preferentially attract the highest quality interacting species (similar to Stebbins (1970)'s 'most effective pollinator principle'). In contrast, a negative component correlation is likely associated with generalised interactions (Calviño-Cancela & Martín-Herrero, 2009;González-Castro et al., 2015;Palacio, 2019). ...
Article
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Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (quantity component) multiplied by the probability that an immediate outcome results in a new individual (quality component). These components form a two-dimensional effectiveness landscape with each species’ location determined by its values of quantity (x-axis) and quality (y-axis). We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness values: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components. We illustrate this approach using a large dataset on synzoochory, seed dispersal by seed-caching animals. The synzoochory landscape was clumped, with effectiveness determined primarily by the quality component, and with quantity and quality positively correlated. We suggest this type of landscape structure is common in generalised coevolved mutualisms, where multiple functionally equivalent, high-quality partners exert similarly strong selection. Presumably, only those organisms located in high-quality regions will impact the evolution of their partner. Exploring properties of effectiveness landscapes in other mutualisms will provide new insight into the evolutionary and ecological consequences of mutualisms.
... Consequently, the optimal representation of network links should reflect the bi-directional nature of its effects (Figure 1b). Although quantifying reciprocal effects is straightforward in interactions involving deaths and births, such as host-parasitoid networks, for other interaction types (e.g., plant-pollinator ) measuring demographic changes for all interaction partners could be difficult and time-consuming González-Castro et al. 2015). ...
... A number of studies have explored the relationship between the structure of multitrophic systems and ecosystem functioning, finding some promising -albeit usually idiosyncratic-results, and often coming from simple food web systems with unclear relevance for more complex ecosystems (Thompson et al. 2012;Poisot et al. 2013;Soliveres et al. 2016;Wang and Brose 2018). Also, in studies of plant-seed disperser networks, estimating the seed dispersal function requires not only data on plant-frugivore interactions, but also on the seed dispersal distance and seed viability (González-Castro et al. 2015;Donoso et al. 2016;Acevedo-Quintero et al. 2020), the latter usually not available. ...
Article
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Species coexisting in ecological communities interact in multiple ways to form complex networks. We review the growing literature on ecological interaction networks to address several key issues about this conceptual and methodological approach. We start by asking the most basic question: Why study networks and whether a network approach is (or is not) useful to understand the ecology of interacting species, the functioning and stability of the communities they belong to, and their response to global change drivers. We also discuss the multiple meanings of network nodes as individuals, populations and species, the different ways of quantifying node roles, the multiple meanings of links as presence/absence of interactions, per capita interaction strengths and species-level effects, and the available approaches to study networks with different types of interactions. Then, we review the structural patterns emerging in ecological interaction networks and the mechanisms driving network structure and function, identifying both what we already know and the knowledge gaps that we still need to fill in. We also discuss sampling effects and their influence in distorting observed network patterns. Finally, we review how different drivers of global environmental change influence the structure, dynamics and stability of ecological networks. With this review we hope to offer a balanced overview of what we have learned in the study of ecological interaction networks and point to several key avenues of research for the next decade.
... In this way, the mutualism effectiveness concept (Schupp et al., 2010(Schupp et al., , 2017 permits the assessment of intra-and inter-species variability in interaction effectiveness. This approach has been previously used to study the relative contribution of many species in one system (e.g., Rodríguez-Rodríguez et al., 2013;Rother et al., 2016), but to the best of our knowledge it has not been used to compare the effectiveness of mutualistic interactions across habitats (but see González-Castro et al., 2015;Nogales et al., 2017). Mutualism effectiveness can be assessed using effectiveness landscapes (i.e., an abstract representation of the quantitative and qualitative interaction components) that provide a more accurate representation of individual contributions to the total effect. ...
... Thinking in more generalist systems (where redundant species occur), we expect to find F.E. Fontúrbel et al. Perspectives in Plant Ecology, Evolution and Systematics 28 (2017) 87-95 compensation among species in addition to potential quantity-quality compensation as those described here, keeping in mind that sub-optimal plant recruitment may occur as result of effectiveness differences among redundant species (Calviño-Cancela and Martin-Herrero, 2009;González-Castro et al., 2015). The way such compensation occurs in redundant mutualistic systems (i.e., if they are context-dependent or independent regarding the nature of the compensation and the net costbenefit balance) is yet to be assessed in terms of mutualistic effectiveness (Schupp, 2007). ...
Article
Most flowering plants depend on biotic pollination and seed dispersal for reproductive success. Pollination and seed dispersal are generalized mutualistic interactions, in which species with different effectiveness levels participate. However, anthropogenic habitat disturbance may hamper the impact of mutualists, jeopardizing plant establishment and recruitment. Important as it is, the effect of habitat transformation on the joint contribution of pollinators and seed dispersers to plant reproduction remains little explored. To assess the effects of habitat transformation on the effectiveness of pollination and seed dispersal processes, we studied a highly specialized system that consists of a hemiparasitic mistletoe, one hummingbird pollinator, and one marsupial seed disperser species that inhabit native and transformed habitats in southern Chile. Pollination and seed dispersal effectiveness landscapes were highly variable and did not differ between habitats. Pollinator visitation and fruit removal were higher at the transformed habitat whereas seed disperser visitation and fruit set were higher at the native habitat, probably due to differences in structure and resource availability between habitats. In consequence, and contrary to our expectations, the coupled outcome of pollination and seed dispersal was higher at the transformed habitat, suggesting that persistence of the tripartite mutualism in the overall system is benefitted from the presence of a native understory vegetation that attracts pollinators and seed dispersers and compensates for the often detrimental effects of habitat transformation.
... These results indicate that quality is more critical than quantity for hemi-epiphytic figs. The degree of effects of quality and quantity components on total SDE differs with seed dispersers, plants, environment, and also methodology [53,54]. In other areas and other plants, dispersers usually have higher effectiveness either quantitatively or qualitatively [53,54], whereas binturongs showed high values in both components. ...
... The degree of effects of quality and quantity components on total SDE differs with seed dispersers, plants, environment, and also methodology [53,54]. In other areas and other plants, dispersers usually have higher effectiveness either quantitatively or qualitatively [53,54], whereas binturongs showed high values in both components. The seed deposition microsite is the most critical factor for survival of hemi-epiphytic figs, so total SDE was biased toward quality. ...
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Ficus species are keystone plants in tropical rainforests, and hemi-epiphytic figs play a notably important role in forest ecosystems. Because hemi-epiphytic figs have strict germination requirements, germination and establishment stages regulate their populations. Despite the ecological importance of hemi-epiphytic figs in the rainforests, seed dispersal systems by fig-eating animals under natural conditions remain unknown because of the difficulty in tracing the destiny of dispersed seeds in the canopy. Therefore, seed dispersal effectiveness (SDE) has never been evaluated for hemi-epiphytic figs. We evaluated the SDE of hemi-epiphytic figs using qualitative and quantitative components by three relatively large-sized (> 3 kg) arboreal and volant animals in Bornean rainforests that largely depend on fig fruits in their diets: binturongs Arctictis binturong, Mueller’s gibbons Hylobates muelleri, and helmeted hornbills Rhinoplax vigil. The SDE values of binturongs was by far the highest among the three study animals. Meanwhile, successful seed dispersal of hemi-epiphytic figs by gibbons and helmeted hornbills is aleatory and rare. Given that seed deposition determines the fate of hemi-epiphytic figs, the defecatory habits of binturongs, depositing feces on specific microsites in the canopy, is the most reliable dispersal method, compared to scattering feces from the air or upper canopy. We showed that reliable directed dispersal of hemi-epiphytic figs occurs in high and uneven canopy of Bornean rainforests. This type of dispersal is limited to specific animal species, and therefore it may become one of the main factors regulating low-success hemi-epiphytic fig recruitment in Bornean rainforests.
... This has a strong potential for interaction compensation; models that allow a potential partner to rescue a species that has otherwise lost mutualists find increased robustness to coextinction (Kaiser-Bunbury, Muff, et al., 2010). Still, these models do not consider the opposite, anticompensating effect-that interactions with co-occurring partners can be lost in an altered network (Gilljam, Curtsdotter, & Ebenman, 2015). In the networks studied here, we found that anticompensating rewiring occurred more frequently than did compensating rewiring. ...
... Similar dynamics have been recently explored theoretically in the context of trophic networks. Gilljam et al. (2015) used dynamical models where trophic rewiring can be compensatory or anticompensatory to show that rewiring, when adaptive, increases coextinction risk. Thus network rewiring may not buffer ecosystems from coextinction in nature as it does in network models that assume consistently compensatory rewiring (Ramos Jiliberto et al., 2012;Staniczenko, Lewis, Jones, & Reed-Tsochas, 2010;Thierry et al., 2011;Valdovinos et al., 2013). ...
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Following defaunation, the loss of interactions with mutualists such as pollinators or seed dispersers may be compensated through increased interactions with remaining mutualists, ameliorating the negative cascading impacts on biodiversity. Alternatively, remaining mutualists may respond to altered competition by reducing the breadth or intensity of their interactions, exacerbating negative impacts on biodiversity. Despite the importance of these responses for our understanding of the dynamics of mutualistic networks and their response to global change, the mechanism and magnitude of interaction compensation within real mutualistic networks remains largely unknown. We examined differences in mutualistic interactions between frugivores and fruiting plants in two island ecosystems possessing an intact or disrupted seed dispersal network. We determined how changes in the abundance and behavior of remaining seed dispersers either increased mutualistic interactions (contributing to "interaction compensation") or decreased interactions (causing an "interaction deficit") in the disrupted network. We found a "rich-get-richer" response in the disrupted network, where remaining frugivores favored the plant species with highest interaction frequency, a dynamic that worsened the interaction deficit among plant species with low interaction frequency. Only one of five plant species experienced compensation and the other four had significant interaction deficits, with interaction frequencies 56-95% lower in the disrupted network. These results do not provide support for the strong compensating mechanisms assumed in theoretical network models, suggesting that existing network models underestimate the prevalence of cascading mutualism disruption after defaunation. This work supports a mutualist biodiversity-ecosystem functioning relationship, highlighting the importance of mutualist diversity for sustaining diverse and resilient ecosystems.
... Tropical networks also appear to be less modular than temperate ones, which might be due to a lower preponderance of seasonal effects structuring tropical interactions (Schleuning et al. 2014). Yet, such a relationship between modularity and latitude was absent once accounting for spatial autocorrelation, and a nested pattern with latitude was not found either (Sebastián- González et al. 2015). ...
... Yet, only recently has seed fate begun being incorporated in networks by quantifying the proportion of intact seeds present in animal droppings (Heleno et al. 2013). Studies that quantify seed dispersal effectiveness (sensu Schupp et al. 2010) and estimate seedling recruitment are still very rare (González-Castro et al. 2015;Donoso et al. 2016) with only some attempts in tropical ecosystems (Muñoz et al. 2016;Pigot et al. 2016). ...
Chapter
Seed dispersal mediated by animals is a pivotal ecological interaction in the tropics. Despite a long tradition of tropical seed dispersal studies, only recently the drivers of the structure of seed dispersal networks are beginning to be uncovered at macroecological scales. The knowledge on tropical seed dispersal comes mainly from avian dispersal studies in the Neotropics while other frugivores and tropical regions are strongly understudied. The networks sampled with a combination of visitation census and seed recovery from feces seem more reliable of the number of detected links and web asymmetry than networks based on a single method. Our review reveals that keystone species in most networks share a set of functional traits likely influenced by species phylogeny. Woody plants bearing small berries (in the Melastomataceae, Myrtaceae, Moraceae, and Urticaceae families) were the most frequent keystone plants whereas two groups of keystone animals could be identified, namely: small obligate frugivores (Pipridae and Thraupidae) and large animals including a variety of taxonomic groups such as cracids, rodents, monkeys, and megafauna. Large keystone species tend to face a higher extinction risk leading to a concern on the sustainability of the dispersal services they provide, mainly to large-seeded plant species that are essential to ecosystem functioning.
... The contribution of primates to forest regeneration (Seed dispersal effectiveness: SDE) includes quantitative as well as qualitative aspects [27,28]. Here, the quantity denotes the total number of seeds that monkeys take and carry, depending on the feeding behavior [28]. ...
... The quality of seed dispersal is influenced by several factors: the level of seed damage, the length of time that seeds remain in the gut, the spatial extent of their movements, and the ability of seeds to germinate after being defecated [27,28]. Our results specify that the Tibetan macaques are important seed predators that provide potential value for seed dispersal. ...
Article
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There are numerous ecological and evolutionary implications for the ability of frugivores to predate on fruits and consume or disperse their seeds. Tibetan macaques, which are considered important seed predators, typically feed on fruits or seeds. However, systematic research into whether they have a seed dispersal function is still lacking. Endozoochory allows seeds to disperse over greater distances by allowing them to remain in the animal's digestive tract. Consumption of fruit may not imply effective seed dispersal, and the physical characteristics of seeds (e.g., size, weight, specific gravity, etc.) may influence the dispersal phase's outcome. We conducted feeding experiments with three captive Tibetan macaques (Macaca thibetana) and nine plant seeds to determine the influence of seed characteristics on Tibetan macaques' early stages of seed dispersal. The results revealed that the percentage of seed destruction (PSD) after ingestion was 81.45% (range: 15.67-100%), with the PSD varying between plant species. Among the three passage time parameters, the transit time (TT) (mean: 18.8 h and range: 4-24 h) and the time of seed last appearance (TLA) (mean: 100.4 h and range: 48-168 h) differed significantly between seed species, whereas the mean retention time (MRT) (mean: 47.0 h and range: 32-70.3 h) did not. In terms of model selection, PSD was influenced by seed size, weight, volume, and specific gravity; TT was influenced by seed-to-shell investment rate, weight, volume, and specific gravity; and TLA was influenced only by seed size. These findings imply that seeds with a smaller size, specific gravity, volume, and greater weight pass more easily through the monkeys' digestive tracts. Particularly, seeds with a mean cubic diameter (MCD) of <3 mm had a higher rate of expulsion, larger volume, and weight seeds pass faster, while smaller remained longer. Tibetan macaques, as potential seed dispersers, require specific passage time and passage rates of small or medium-sized seeds. Larger and heavier seeds may be more reliant on endozoochory. Tibetan macaques have the ability to disperse seeds over long distances, allowing for gene flow within the plant community.
... No passado, os répteis foram considerados como animais de pouca importância ecológica (Zim & Smith 1953), e essa visão ainda é atualmente bem enraizada nas sociedades humanas (Miranda 2017 Castro et al. 2015). Por fim, alguns répteis têm sido considerados como "engenheiros" de ecossistemas, porque modificam a estrutura de hábitats, o que pode gerar efeitos positivos para outras espécies. ...
... Nogales et al. (2017) compared the number of seeds dispersed and effect of gut treatment by reptile vs. bird frugivores in the Galápagos. González-Castro et al. (2015) combined the number of seeds dispersed with condition of seeds after dispersal and seedling emergence/ survival probabilities to compare SDE for birds and lizards. As these studies illustrate, different dispersers contribute in different ways to the template constraining an eventual plant community. ...
Article
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Seed dispersal enables plants to reach hospitable germination sites and escape natural enemies. Understanding when and how much seed dispersal matters to plant fitness is critical for understanding plant population and community dynamics. At the same time, the complexity of factors that determine if a seed will be successfully dispersed and subsequently develop into a reproductive plant is daunting. Quantifying all factors that may influence seed dispersal effectiveness for any potential seed-vector relationship would require an unrealistically large amount of time, materials and financial resources. On the other hand, being able to make dispersal predictions is critical for predicting whether single species and entire ecosystems will be resilient to global change. Building on current frameworks, we here posit that seed dispersal ecology should adopt plant functional groups as analytical units to reduce this complexity to manageable levels. Functional groups can be used to distinguish, for their constituent species, whether it matters (i) if seeds are dispersed, (ii) into what context they are dispersed and (iii) what vectors disperse them. To avoid overgeneralization, we propose that the utility of these functional groups may be assessed by generating predictions based on the groups and then testing those predictions against species-specific data. We suggest that data collection and analysis can then be guided by robust functional group definitions. Generalizing across similar species in this way could help us to better understand the population and community dynamics of plants and tackle the complexity of seed dispersal as well as its disruption.
... No passado, os répteis foram considerados como animais de pouca importância ecológica (Zim & Smith 1953), e essa visão ainda é atualmente bem enraizada nas sociedades humanas (Miranda 2017 Castro et al. 2015). Por fim, alguns répteis têm sido considerados como "engenheiros" de ecossistemas, porque modificam a estrutura de hábitats, o que pode gerar efeitos positivos para outras espécies. ...
... This occurs because large-bodied animals are being especially hard-hit by anthropogenic disturbances, and very often, altered ecosystems only retain small-to medium-sized species or individuals (Dirzo et al. 2014;Young et al. 2016;Pérez-Méndez 2016;Pérez-Méndez et al. 2018). This is especially critical in poor-richness ecosystems, such as insular or high mountain assemblages, where functional redundancy among dispersers is quite low (McConkey and Brockelman 2011;McConkey and Drake 2015;González-Castro et al. 2015). Under these scenarios, by predating on remaining small primary consumers, top predators may be the only group of animals that can move seeds at large distances. ...
Chapter
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Plants, unlike animals, are organisms with a sessile adult stage, and consequently they need external vectors for moving their propagules (mainly seeds) away from mother plants. The movement of seeds is a central process in the life cycle of plants called seed dispersal (Howe and Smallwood 1982). This process determines the spatial pattern of seed deposition, over which post-dispersal processes such as predation, germination, or seedling survival will act (Nathan and Muller-Landau 2000). Seed dispersal will therefore influence significantly the probability that a single seed becomes an adult individual of the plant population. The advantages of moving away from source plants are multiple. From a demographic point of view, seed dispersal enables to escape seeds to high mortality in the vicinity of maternal plants, where the probability of predation or pathogen infection increases exponentially (Janzen 1970; Connell 1971). In addition, dispersal facilitates the arrival of seeds to suitable microhabitats for germination and survival of seedlings, the colonization of new habitats, and the range expansion of plant populations (Howe and Smallwood 1982). From a genetic point of view, together with pollination, seed dispersal shapes patterns of gene flow within and among plant populations, influencing the characteristics and the cohesiveness of genetic pools at local and regional scales (Loveless and Hamrick 1984). Thus, as whole, seed dispersal will influence the demogenetic features of plant populations, conditioning the regeneration dynamics and the adaptability and resilience of plant populations in changing landscapes.
... Self-fertilization is possible, but depresses its reproductive success (Rodríguez-Rodríguez and Valido 2011;and present study). Mature fruits are reddish-orange ovoid-shaped berries, containing many seeds, and are consumed mainly by native birds and lizards (Valido 1999;González-Castro et al. 2015), and also by introduced rats (Valido et al. 2011;this study). ...
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Islands harbor a considerable portion of global biodiversity and endemic biota, and also are the recipients of the largest proportional numbers of alien invaders. Such invaders may jeopardize the performance of native species, through either their direct or indirect effects. In this study, we investigated the reproductive ecology of the endemic scrambling perennial herb Canarina canariensis in remnants of the former thermosclerophyllous woodland of Tenerife (Canary Islands), assessing how two widespread alien invasive species, the honeybee (Apis mellifera) and the black rat (Rattus rattus), affect its reproductive success. Apis mellifera visits its flowers whereas the black rat consumes both its flowers and fruits. Here, we compared the pollination effectiveness of different animal guilds (vertebrates vs insects) by means of selective exclosures and determined the level of floral herbivory. Three bird species (Phylloscopus canariensis, Cyanistes teneriffae and Sylvia melanocephala), a lizard (Gallotia galloti) and two insects (A. mellifera and the butterfly Gonepteryx cleobule) were the main flower visitors. Phylloscopus canariensis was the most frequent visitor in the early flowering season whereas A. mellifera predominated in the flowers during mid and late flowering periods. Birds increased fruit set, whilst lizards and insects had a negligible effect. Rats consumed about 10% of the flowers and reduced fruit set to one third. Besides contributing little to plant reproduction, A. mellifera might interfere with bird pollination by depleting flowers of nectar. We conclude that both alien species can threaten C. canariensis reproduction and hence population sustainability in the thermosclerophyllous vegetation. Apis mellifera, in particular, may become especially detrimental if apiculture keeps expanding, or if this bee becomes active earlier in the season due to global warming.
... Although seed dispersal is key to maintaining plant diversity, seed dispersal by reptiles (saurochory) is sometimes regarded as a rare phenomenon (Valido and Olesen, 2007). This notion is challenged by growing evidence of reptiles as seed dispersers (González-Castro et al., 2015), especially because of the tendency for most reptiles to gulp fruits whole, which provides little opportunity for seed damage. ...
Article
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Earth's tropical ecosystems have witnessed several extinctions and a dramatic reduction of the range and abundance of large reptile species, which is directly related to the rise of early and modern humans. The occurrence of such extinctions, range reduction, species loss, and the consequences for several paramount ecosystem processes are poorly documented compared to other large vertebrate species. Here, I reviewed the literature on the ecological processes performed by large tropical reptile species and their human-induced widespread demise in order to determine knowledge gaps and encourage a paradigm shift in understanding on the interactiveness of such species. The interactions and species involved indicate that large abundant reptiles in the tropics are important in ecological processes, and can consequently have an important role in ecosystem function through gene dispersal, nutrient cycling, trophic action, and ecosystem engineering. These important interactions performed by reptiles are not solely performed by few species, or geographically restricted to islands, but instead present a pattern that repeatedly occurs in large reptiles distributed over tropical ecosystems. The observed tendency of reptiles to be tightly involved in these ecological interactions has important implications for the ecology of tropical ecosystems. Lost and current ecological processes performed by large reptiles may be orders of magnitude higher than what is currently perceived, and the misleading baseline of those processes must be addressed otherwise we risk losing species and services that are dependent of such interactions. To fix this bias I suggest: (a) Increase information spreading about Pleistocene-Holocene reptile extinctions using popular media; (b) Improved exchange between the research field of megafauna effects in ecosystems and herpetologists working with large reptiles; (c) Increase research effort on anthropogenic reptile extinctions and their potential to predict future losses; (d) Address the knowledge gaps, as human-reptile conflict, chelonian seed dispersal and nutrient movement; (e) Increase quantitative research on large reptile population ecology, density, and abundance. (f) address the potentially present or lost ecosystem effects of extant and extinct reptile species. Although the importance of reptiles in most tropical ecosystems has been perceived as negligible, this study shows that this may be a misleading paradigm.
... No passado, os répteis foram considerados como animais de pouca importância ecológica (Zim & Smith 1953), e essa visão ainda é atualmente bem enraizada nas sociedades humanas (Miranda 2017 Castro et al. 2015). Por fim, alguns répteis têm sido considerados como "engenheiros" de ecossistemas, porque modificam a estrutura de hábitats, o que pode gerar efeitos positivos para outras espécies. ...
... Empirical evaluations of predictions stemming from network analyses are challenging because they require that the actual ecological processes in question (e.g. seed dispersal or pollination) are assessed simultaneously for many species in the community (Gonzalez-Castro et al. 2015;Ruggera et al. 2016;Ballantyne et al. 2017). Furthermore, even if comprehensive databases are available, there are inherent pitfalls when evaluating the ecological consequences of network properties. ...
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Network metrics are widely used to infer the roles of mutualistic animals in plant communities and to predict the effect of species' loss. However, their empirical validation is scarce. Here we parameterized a joint species model of frugivory and seed dispersal with bird movement and foraging data from tropical and temperate communities. With this model, we investigate the effect of frugivore loss on seed rain, and compare our predictions to those of standard coextinction models and network metrics. Topological coextinction models underestimated species loss after the removal of highly linked frugivores with unique foraging behaviours. Network metrics informed about changes in seed rain quantity after frugivore loss. However, changes in seed rain composition were only predicted by partner diversity. Nestedness, closeness, and d’ specialisation could not anticipate the effects of rearrangements in plant–frugivore communities following species loss. Accounting for behavioural differences among mutualists is critical to improve predictions from network models. In this work we test if frequently used network metrics can predict the vulnerability of plant communities to extinctions and detect frugivores of disproportionate importance. For this, we simulated scenarios of frugivores’ loss in a model able to predict frugivory in six communities. Unlike network metrics, in our model pairwise interactions emerged from frugivores’ foraging and movement decisions. Network metrics informed about quantitative changes in the seed rain but frequently failed to predict composition outcomes. This was partly because they could not anticipate rewiring dynamics after frugivores' loss. Thus, incorporating animal behavior will be critical in the development and performance of the new generation of network metrics.
... Despite the change in species composition along the successional gradient and the absence of some large frugivores (i.e., Ortalis poliocephala) in early seral stages, other large generalist birds, such as Calocitta formosa, were common at these sites. These generalist birds tend to be functionally redundant in seed-dispersal services [86,87], which suggests that at each seral stage of the study area, this ecological service may be being provided. However, the effectiveness of seed dispersal by these species is unknown, so studies focused on evaluating this aspect will be required in the future. ...
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Tropical dry forests (TDFs) are affected by land-use changes. These modifications impact their composition and arboreal structure, as well as the availability of food for several bird groups. In this study, we evaluated the foraging preferences in zoochorous trees of fruit-eating birds during the dry season of the year in three successional stages (early, intermediate, and mature) of TDFs in southern Mexico. The fruits of these trees are important in the diet of several birds during the dry season, a period during which food resources are significantly reduced in TDFs. We estimated foliar cover (FC) and foliage height diversity (FHD) of zoochorous trees in 123 circular plots. These variables were recognized as proxies of food availability and tree productivity. Foraging preferences were evaluated at the community level, by frugivore type, and by bird species. We evaluated the effect of the structural variables and the fruit size of zoochorous plants on fruit removal by birds and related the bird body mass and fruit size removed in the successional gradient. A total of 14 zoochorous tree species and 23 fruit-eating bird species were recorded along the successional gradient. Intermediate and mature stages showed greater fruit removal. The birds removed mainly B. longipes fruits across the three successional stages. The FHD and fruit size were important drivers in the selection of zoochorous trees and fruit removal by fruit-eating birds. Fruit size and bird body mass were positively related along the successional gradient. The results suggest that fruit removal by fruit-eating birds in the successional gradient can promote the demographic dynamics of several zoochorous tree species, especially of Bursera spp. along the TDFs.
... However, illegal poaching and habitat loss have reduced the population significantly, making this species functionally extinct on Saipan (U.S. Fish and Wildlife Service 2009). Lizards are known to be important frugivores in some island systems but their ability to move seeds long distances is restricted by their limited mobility (Olesen & Valido 2003;González-Castro et al. 2015). The non-native Emerald Tree Skink (Lamprolepis smaragdina) occurs on Saipan and is known to consume fruit (E. ...
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Vertebrate frugivores enhance tropical forest regeneration by dispersing seeds into degraded areas. However, the importance of individual species as dispersers may vary within a community. Management and restoration would benefit from understanding which species are critical in moving native seeds into degraded habitats. We compared habitat composition of bird start and end locations for movement intervals based on mean gut passage times for the avian frugivore community on the island of Saipan. The proportion of movement intervals that began in intact, native forest varied among species, with Golden White-eyes having the highest proportion. However, this species tended to remain in intact forest and only rarely crossed into degraded habitats. Bridled White-eyes and Mariana Fruit Doves exhibited slightly higher rates of crossing from intact forest to degraded habitats, suggesting an ability to disperse native seeds to degraded areas. White-throated Ground Doves were never recorded crossing from intact forest to degraded habitats. Despite having a low proportion of movement intervals beginning in intact forest, Micronesian Starlings showed a higher proportion and absolute number of movements from intact forest to degraded habitats, due to their propensity to move frequently, across long distances, and across habitat types. In this species-poor frugivore network, seed dispersal into degraded habitats appears highly dependent on one species within the community. Regeneration of degraded lands may be severely hindered if this key disperser is lost.
... Consequently, frugivores may disperse seeds unevenly by occupying preferred microhabitats, which will create contagious spatial distributions of dispersed seeds (Schupp et al., 2002). Ultimately, a nucleation process of this nature affects seed survival and seedling establishment, as well, subsequently, as the structure and dynamics of plant populations and communities (Howe and Smallwood, 1982;Wang and Smith, 2002;Nathan, 2006;Clark et al., 2007;González-Castro et al., 2015). ...
... Moreover, the two-dimensional representation of all possible combinations of the quantitative and qualitative components in a community, known as "effectiveness landscapes" (Schupp et al., 2010), has proven useful. Some authors have used it to study the functional equivalence or contribution of particular groups (González-Castro, Calviño-Cancela, & Nogales, 2015) or species (Blendinger, 2017) to different functions. For instance, Hervías-Parejo & Traveset (2018) compared the pollination effectiveness of insects and opportunistic Galapagos birds. ...
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Interactions among organisms can be defined by two main features: a quantitative component (i.e. frequency of occurrence) and a qualitative component (i.e. success of the interaction). Measuring properly these two components at the community level, can provide a good estimate of the ecosystem functions mediated by biotic interactions. Although this approach has been frequently applied to evaluate the eco-evolutionary consequences of mutualistic relationships, it has never been extended to the predation function and the associated pest control ecosystem service. Here, we introduce a simple measure that accounts for the quantitative and the qualitative components of predation interactions, and facilitates a precise characterization of this ecosystem function at the community level, while accounting for variations at species and individual levels. This measure arises as a fine indicator of predation pressure, and provides great opportunities to better understand how different components of predation and pest control potential vary across environmental gradients.
... To date, this sort of integrative information has been gathered in systems of moderate species richness (e.g. Donoso, García, Rodríguez-Pérez, & Martínez, 2016;González-Castro, Calviño-Cancela, & Nogales, 2015) but not in species-rich systems such as tropical forest. ...
Article
Networks of mutualistic interactions between animals and plants are considered a pivotal part of ecological communities. However, mutualistic networks are rarely studied from the perspective of species‐specific roles, and it remains to be established whether those animal species more relevant for network structure also contribute more to the ecological functions derived from interactions. Here, we relate the contribution to seed dispersal of vertebrate species with their topological role in frugivore‐plant interaction networks. For one year in two localities with remnant patches of Colombian tropical dry forest, we sampled abundance, morphology, behavior, and fruit consumption from fleshy‐fruited plants of various frugivore species. We assessed the network topological role of each frugivore species by integrating their degree of generalization in interactions with plants with their contributions to network nestedness and modularity. We estimated the potential contribution of each frugivore species to community‐wide seed dispersal, on the basis of a set of frugivore ecological, morphological and behavioral characteristics important for seed dispersal, together with frugivore abundance and frugivory degree. The various frugivore species showed strong differences in their network structural roles, with generalist species contributing the most to network modularity and nestedness. Frugivores also showed strong variability in terms of potential contribution to seed dispersal, depending on the specific combinations of frugivore abundance, frugivory degree and the different traits and behaviors. For both localities, the seed dispersal potential of a frugivore species responded positively to its contribution to network structure, evidencing that the most important frugivore species in the network topology were also those making the strongest contribution as seed dispersers. Contribution to network structure was correlated with frugivore abundance, diet, and behavioral characteristics. This suggests that the species‐level link between structure and function is due to the fact that the occurrence of frugivore‐plant interactions depends largely on the characteristics of the frugivore involved, which also condition its ultimate role in seed dispersal.
... No passado, os répteis foram considerados como animais de pouca importância ecológica (Zim & Smith 1953), e essa visão ainda é atualmente bem enraizada nas sociedades humanas (Miranda 2017 Castro et al. 2015). Por fim, alguns répteis têm sido considerados como "engenheiros" de ecossistemas, porque modificam a estrutura de hábitats, o que pode gerar efeitos positivos para outras espécies. ...
... Reductions in the quality of seed dispersal may occur at species-level, when interactions of high-quality seed dispersers are quantitatively compensated by non-equivalent (i.e. complementary), low-quality seed dispersers [22][23][24]. In addition, reductions in seed dispersal quality can occur within species, when individuals of a certain frugivore are present in both, old-growth and degraded forests, but the seed dispersal quality is reduced in the latter one; referred to as 'cryptic functional loss' of species [25]. ...
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Forest degradation changes the structural heterogeneity of forests and species communities, with potential consequences for ecosystem functions including seed dispersal by frugivorous animals. While the quantity of seed dispersal may be robust towards forest degradation, changes in the effectiveness of seed dispersal through qualitative changes are poorly understood. Here, we carried out extensive field sampling on the structure of forest microhabitats, seed deposition sites and plant recruitment along three characteristics of forest microhabitats (canopy cover, ground vegetation and deadwood) in Europe’s last lowland primeval forest (Białowieża, Poland). We then applied niche modelling to study forest degradation effects on multi-dimensional seed deposition by frugivores and recruitment of fleshy-fruited plants. Forest degradation was shown to (i) reduce the niche volume of forest microhabitat characteristics by half, (ii) homogenize the spatial seed deposition within and among frugivore species, and (iii) limit the regeneration of plants via changes in seed deposition and recruitment. Our study shows that the loss of frugivores in degraded forests is accompanied by a reduction in the complementarity and quality of seed dispersal by remaining frugivores. By contrast, structure-rich habitats, such as old-growth forests, safeguard the diversity of species interactions, forming the basis for high-quality ecosystem functions.
... For example, while it has been shown that granivorous birds, large herbivores and seed-catching birds and rodents can also disperse a non-negligible proportion of viable seeds, the net effect of these interactions on plant fitness is still hard to quantify (Feldman et al., 1999;Heleno et al., 2011;Albert et al., 2015, see also Baltzinger et al., this volume). Recent studies already started to incorporate the effect of seed passage through the dispersers gut on germination to refine the measures of interaction outcome in seed dispersal networks , and also estimating seedling survival (González-Castro et al., 2015). These are very important steps towards effectively closing the seed dispersal loop (sensu Wang and Smith, 2002) in community level studies, i.e. to estimate the seed dispersal effectiveness of all pairwise interactions in a given community, and to fully understand the impacts of plant invasions on native seed dispersal. ...
Chapter
This book contains 23 chapters divided into seven parts. Part I reviews the key hypotheses in invasion ecology that invoke biotic interactions to explain aspects of plant invasion dynamics; and reviews models, theories and hypotheses on how invasion performance and impact of introduced species in recipient ecosystems can be conjectured according to biotic interactions between native and non-native species. Part II deals with positive and negative interactions in the soil. Part III discusses mutualistic interactions that promote plant invasions. Part IV describes antagonistic interactions that hinder plant invasions, while part V presents the consequences of plant invasions for biotic interactions among native species. In part VI, novel techniques and experimental approaches in the study of plant invasions are shown. In the last part, biotic interactions and the management of ecosystems invaded by non-native plants are discussed.
... In Hawaii, fruits of the alien species Rubus rosifolius consumed by captured black rats showed 100% seed survival after food mastication and gut passage (Shiels 2010). In any case, seed dispersal services provided by the black rat on oceanic islands depend upon its dispersal effectiveness, which includes the number of seeds dispersed, seedling emergence and seedling survival (González-Castro et al. 2015). Unfortunately, there are no data on post-dispersal stages in the Canaries. ...
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The black rat (Rattus rattus) is an alien species that causes severe impact on island ecosystems, floras and faunas. The main aim of this study was to determine the plant and animal contributions to black rat diet in a pristine misty laurel forest area on La Palma (Canary Islands). Our working hypothesis was that this rat equally consumes plants and animals (fully omnivorous animal) wherever it is introduced, including pristine habitats. A total of 483 droppings collected from the terrain were first morphologically examined using a stereomicroscope, which showed high plant consumption (presence in 92.4% of droppings), followed by invertebrates (46.0%) and vertebrates (31.2%). DNA-based analyses revealed even higher proportions of plants (97%) and invertebrates (79%), while fine-scale sequence searches (DNA barcoding) in the GenBank (BLAST tool) provided a preliminary identification of 44 plants and 12 invertebrate taxa. To gain more in-depth insight into plant identification, we built up a local DNA reference collection (58 species), improving accuracy (30 species confirmed) compared to GenBank searches (25 species). Contingency analyses (chi-square and G-test) only showed significant differences in droppings between plant sequences and toxic plant presence. This study confirms that the black rat is here an omnivorous animal but with a strong plant diet component, including an intriguingly high number of toxic plants. Interestingly, despite rodents chewing on fruits and usually crushing seeds, 66 intact Rubus seeds (Rosaceae) were found in 15 droppings (3.1%). All these results suggest that black rats consume any plant types, including fruits and seeds that can be locally dispersed such as native brambles.
... The pattern of seed arrival to open sites is common for seeds dispersed by lizards (see also e.g. [10,30]). Lizards are ectotherms and need to spend more time in open areas to absorb sun radiation [41]. ...
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The accelerating rate of vertebrate extinctions and population declines threatens to disrupt important ecological interactions, altering key ecosystem processes such as animal seed dispersal. The study of highly specialized mutualistic interactions is crucial to predict the consequences of population declines and extinctions. Islands offer unique opportunities to study highly specialized interactions, as they often have naturally depauperated faunas and are experiencing high rates of human-driven extinctions. In this study, we assess the effect of seed dispersal on seedling recruitment of Ephedra fragilis (Ephedraceae) on a Mediterranean island ecosystem. We used field data and stochastic simulation modeling to estimate seed fate and recruitment patterns of this pioneer shrub typical of arid and semiarid areas, andto estimate the dependence of recruitment on the lizard Podarcis lilfordi (Lacertidae), its only known seed disperser. Ephedra fragilis recruitment highly depended on lizards: lizards produced 3.8 times more newly-emerged seedlings than non-dispersed seeds and no seedlings from undispersed seeds survived the study period. Seed dispersal by lizards was mostly to open sites, which was key for the increased success observed, while undispersed seeds, falling under mother plants, suffered higher predation and lower seedling emergence andsurvival. The ability of this pioneer shrub to get established in open ground is crucial for vegetation colonization and restoration, especially on degraded lands affected by desertification, where they act as nurse plants for other species. Lizards are key in this process, which has important consequences for community structure and ecosystem functioning.
... Such high 422 reciprocity would appear characteristic of many seed dispersal systems and other generalised, resource-based mutualisms (Wheelwright & Orians 1982;Ollerton 2006). Yet, 424 reciprocity in a mutualistic system could be compromised whenever there are large differences between partners quality (i.e., fruit energetic content, or recruitment probabilities 426 for different dispersers), as occurs for example in systems with highly heterogeneous frugivore assemblages (González-Castro et al. 2015;García-Rodríguez et al. 2021). ...
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Mutualistic interactions among free-living species generally involve weak links and highly asymmetric dependence among partners, yet our understanding of factors beyond their emergence is still limited. Using individual-based interactions of a super-generalist fleshy-fruited plant with its frugivore assemblage we estimate the Resource Provisioning Effectiveness (RPE) and Seed Dispersal Effectiveness (SDE) to assess the balance in the exchange of resources. Plants were highly dependent on a few super-generalist frugivore species, while these interacted with most individual plants, resulting in strong asymmetries in mutual dependence. Both RPE and SDE were mainly driven by interaction frequency. Despite highly asymmetric dependences, the strong reliance on quantity largely determined high reciprocity in rewards between partners (i.e., higher energy provided, more seedlings recruited), not obscured by minor variations in the quality of animal or plant service. We anticipate reciprocity will emerge in low-intimacy mutualisms where the mutualistic outcome largely relies upon interaction frequency.
... For example, while it has been shown that granivorous birds, large herbivores and seed-catching birds and rodents can also disperse a non-negligible proportion of viable seeds, the net effect of these interactions on plant fitness is still hard to quantify (Feldman et al., 1999;Heleno et al., 2011;Albert et al., 2015, see also Baltzinger et al., this volume). Recent studies already started to incorporate the effect of seed passage through the dispersers gut on germination to refine the measures of interaction outcome in seed dispersal networks , and also estimating seedling survival (González-Castro et al., 2015). These are very important steps towards effectively closing the seed dispersal loop (sensu Wang and Smith, 2002) in community level studies, i.e. to estimate the seed dispersal effectiveness of all pairwise interactions in a given community, and to fully understand the impacts of plant invasions on native seed dispersal. ...
Chapter
This book contains 23 chapters divided into seven parts. Part I reviews the key hypotheses in invasion ecology that invoke biotic interactions to explain aspects of plant invasion dynamics; and reviews models, theories and hypotheses on how invasion performance and impact of introduced species in recipient ecosystems can be conjectured according to biotic interactions between native and non-native species. Part II deals with positive and negative interactions in the soil. Part III discusses mutualistic interactions that promote plant invasions. Part IV describes antagonistic interactions that hinder plant invasions, while part V presents the consequences of plant invasions for biotic interactions among native species. In part VI, novel techniques and experimental approaches in the study of plant invasions are shown. In the last part, biotic interactions and the management of ecosystems invaded by non-native plants are discussed.
Article
Seed dispersal effectiveness (SDE) is one of the best parameters for estimating the benefit that a plant obtains from a dispersal agent. SDE includes quantitative and qualitative components. Previous avian studies of SDE estimation have been conducted mainly in temperate shrub lands or in tropical forests; data are limited for temperate forests, especially, the quality of seed-deposition sites. In this study, we estimated the SDE of birds for Wild Cherry Cerasus jamasakura and Giant Dogwood Cornus controversa fruits in a temperate Japanese forest. These trees prefer sunny sites so we focused on the light conditions at seed-deposition sites and categorized three microhabitat types: forest-gap, forest-edge, and forest-interior. We observed avian seed removal at fruiting trees, conducted a bird census to estimate microhabitat selectivity and collected bird-dispersed seeds. We then counted seedling emergence. Finally, we constructed generalized linear mixed models that combined bird census and dispersed seed data to identify influential seed disperser(s) for each tree species. Frugivorous behavior was recorded for eight avian species for C. jamasakura and 12 for C. controversa. Of these birds, one for the former, and two for the latter preferentially selected forest-gap or forest-edge trees during each fruiting period. The density of dispersed seeds and seedlings was higher in the forest-gap or forest-edge. Additionally, the frequency with which Japanese White-eye Zosterops japonicus visited was a significant variable for seed density in each microhabitat. The results suggested that microhabitat selectivity may affect the density of dispersed seeds in each microhabitat. Furthermore, a bird with a high quantitative SDE may not necessarily also have a high qualitative SDE. Thus, it is important to estimate qualitative and quantitative SDE by focusing especially on the seed-deposition site for each bird in order to evaluate the actual SDE in temperate forests.
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Abstract Invasive non‐native species can alter animal‐mediated seed dispersal interactions and ultimately affect the stability of recipient communities. The degree of such disturbances, however, is highly variable and depends on several factors, two of which have received little attention: the relative timing of native and non‐native fruiting phenologies, and the associated variation in relative resource availability across the fruiting period. Both are likely to alter plant‐seed disperser interactions threatened by biological invasions. Here we investigated the impact of plant invasions on the seasonal dynamics of frugivory and seed dispersal networks across a large‐scale experimental setup and a plant invasion gradient on a tropical island. We recorded fruit and frugivore abundances, and plant‐frugivore interactions across 8 inselbergs (i.e. rocky outcrops) with different levels of plant invasion during 10 months on the island of Mahé, Seychelles. By combining four sampling methods of plant‐frugivore interactions we constructed quantitative seed dispersal networks at all sites across two 5‐month seasons: the on‐peak and off‐peak fruiting season. Our findings showed that, by fruiting mostly synchronously with natives, non‐native plants compete with natives for dispersal services, predominantly carried out by native frugivores. Variation in native seed dispersal was driven by plant invasion and seasonality. Specifically, native seed dispersal declined with the degree of invasion; dispersal frequency increased with fruit abundance more strongly during the off‐peak fruiting season; and networks became increasingly specialised during off‐peak. These results indicated that during the main fruiting peak seed dispersal services were saturated, which likely intensified the competition between native and non‐native fruits. When resources were scarce during off‐peak fruiting season, native and non‐native frugivores were more selective in their fruit choice at sites dominated by non‐native plants. We showed that native plant and frugivore populations and native seed dispersal interactions were more vulnerable in invaded plant communities, where non‐native plants compete with natives for dispersal services potentially reducing native recruitment. As invasive non‐native plants dominate many ecosystems worldwide, particularly on islands, our findings showed that controlling plant invasions in vulnerable native communities can be critical to maintain native ecosystem functions and biodiversity.
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Background Anti‐laminin‐332 mucous membrane pemphigoid is a chronic severe pemphigoid disease characterized by autoantibodies to laminin‐332. At present no commercial assay is available to demonstrate anti‐laminin‐332 antibodies and diagnosis relies on in‐house techniques with limited sensitivities. Objectives In order to move, keratinocytes cultured in vitro secrete laminin‐332 to attach to the culture dish. That way, they leave behind a unique footprint trail of laminin‐332. We aimed at developing a sensitive and specific laboratory assay to determine anti‐laminin‐332 autoantibodies in patient serum based on binding of patient IgG to these unique footprints. Methods Normal human keratinocytes were grown on glass coverslips and incubated with patient or control serum for 1 hour. The binding of IgG was then investigated by immunofluorescence. After validating the test for its ability to identify anti‐laminin‐332 autoantibodies it was converted into a daily available test based on binding of IgG to dried coverslips that can be stored frozen. The staining patterns of sera from anti‐laminin‐332 pemphigoid patients were then compared to those of sera of patients with other autoimmune bullous diseases and normal human sera. Results IgG of all anti‐laminin‐332 pemphigoid sera (n=16) bound to laminin‐332 footprints while all normal human controls (n=55) were negative. From the sera of patients with other diseases (n=72) four sera tested positive. The footprint assay was also positive for sera that were negative by salt‐split skin analysis demonstrating that it is a very sensitive technique. Conclusions The keratinocyte footprint assay is a fast and specific assay to confirm or rule out the presence of anti‐laminin‐332 autoantibodies. This article is protected by copyright. All rights reserved.
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1.Insects are key laboratory models for research on the fitness effects, genetics, and plasticity of senescence. It was long believed that insects almost never survive long enough to senesce in the wild, but it is now clear that senescence occurs and can exact substantial fitness costs in natural insect populations. Yet, given the practical challenges of obtaining longitudinal field‐data on small, motile animals, we still know remarkably little about the evolution, expression, and fitness consequences of senescence in wild insects. 2.We argue that the study of senescence in wild insects is important because many insights and hypotheses based on laboratory experiments must be tested in natural populations. 3.Examples of research areas where conclusions from laboratory studies could be misleading include the roles of candidate senescence genes, the effects of nutrition and dietary restriction on lifespan and senescence patterns, and the roles of viability selection and sexual selection in shaping senescence through trade‐offs and antagonistic pleiotropy. 4.Several emerging model species (such as antler flies, crickets, damselflies, dragonflies, and butterflies) offer opportunities for field research on senescence using a range of observational and experimental techniques, as well as new genomic approaches. 5.Insects provide valuable and increasingly tractable models for research on senescence in natural populations. We believe that such work will shed light on many important questions in ecology and evolutionary biology. This article is protected by copyright. All rights reserved.
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This paper proposes an overall solution to the two‐layer model predictive control (MPC) for the integrating controlled variables in the process model. The scheme includes three modules, i.e., the open‐loop prediction module, the steady‐state target calculation (SSTC) module, and the dynamic control module. Based on the real‐time output measurements and past inputs, the open‐loop prediction module predicts the future outputs in the presence of disturbances. The economic optimization of SSTC is comprised of the feasibility stage and the economics stage, considering constraints of multi‐priority ranks. The dynamic control module receives the steady‐state targets from SSTC and calculates the control signals. The optimization problems of SSTC and dynamic control operate with the same frequency. This overall method guarantees the consistency of three modules with respect to the model, the constraints, and the targets. The simulation example illustrates that steady‐state targets are adjusted dynamically after the occurrence of disturbances, and offset‐free control is achieved. This article is protected by copyright. All rights reserved.
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Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.
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Deciphering the mechanisms that drive variation in biomass production across plant communities of contrasting species composition and diversity is a main challenge of biodiversity-ecosystem functioning research. Niche complementarity and selection effect have been widely investigated to address biodiversity-productivity relationships. However, the overlooking of the specific role played by key species have limited so far our capacity to comprehensively assess the relative importance of other potential drivers of biodiversity effects. Here, we conducted a grassland diversity-productivity experiment to test how four potential facets of biodiversity effects, namely species richness, functional diversity, species identity and the relaxation of intraspecific competition, account for variations in above and root biomass production. We grew six plant species in monoculture, as well as in every combinations of two, three and six species. Plant density was kept constant across the richness gradient but we additionally grew each species in half-density monoculture to estimate the strength of intraspecific competition for each studied species. We characterized eight functional traits, including root traits, related to nutrient and light acquisition and computed both the functional dissimilarity and the community weighted mean (CWM) of each trait. We further partitioned aboveground biodiversity effect into complementarity and selection effects. We observed strong positive biodiversity effects on both aboveground and root biomass as well as strong positive complementarity effect. These arose largely from the presence of a particular species (Plantago lanceolata) and from CWM trait values more than from a higher functional dissimilarity in plant mixtures. P. lanceolata displayed the highest intraspecific competition, which was strongly relaxed in species mixtures. By contrast, the presence of Sanguisorba minor negatively affected the productivity of plant mixtures, this species suffering more from interspecific than intraspecific competition. This study provides strong evidences that the search for key species is critical to understand the role of species diversity on ecosystem functioning and demonstrates the major role that the balance between intraspecific and interspecific competition plays in biodiversity-ecosystem functioning relationships. Developing more integrative approaches in community and ecosystem ecology can offer opportunities to better understand the role that species diversity plays on ecosystem functioning.
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Many plants rely on fruit consuming animals (frugivores) to disperse their seed. Successful dispersal is influenced inter alia by quantity of seeds dispersed, dispersal distance, nature of seed deposition and post-depositional seed predation. The germination potential of the seed is commonly enhanced through physical or chemical scarification while the ingested fruit is processed in the gastrointestinal tract. Most discussions of animal-mediated seed dispersal are vector-centric and explore in depth the minutiae or the consumption by species or examine mutualistic networks. This paper provides a framework that conceptualises the effect of animal-mediated seed dispersal in terms of net benefits to the plant. These benefits, viewed in terms of a dispersed plant’s presence in the landscape, are codified as suisubstitution (new term), intensification, expansion, and colonisation. Only vectors with an ability to traverse and utilise multiple ecological landscapes provide true net colonisation benefits to a plant species. This is particularly essential in this later period of the Anthropocene where ecological landscapes have become increasingly fragmented and are being augmented or replaced by novel ecosystems. https://www.sciencedirect.com/science/article/pii/S0367253019305389
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Mutualistic interactions form the basis for many ecological processes and are often analyzed within the framework of ecological networks. These interactions can be sampled with a range of methods and first analyses of pollination networks sampled with different methods showed differences in common network metrics. However, it is yet unknown if metrics of seed dispersal networks are similarly affected by the sampling method and if different methods detect a complementary set of frugivores. This is necessary to better understand the (dis‐)advantages of each method and to identify the role of each frugivore for the seed dispersal process. Here, we compare seed removal networks based on the observation of 2189 frugivore visits on ten focal plant species with seed deposition networks constructed by DNA barcoding of plant seeds in 3094 frugivore scats. We were interested in whether both methods identify the same disperser species and if species‐level network metrics of plant species were correlated between network types. Both methods identified the same avian super‐generalist frugivores, which accounted for the highest number of dispersed seeds. However, only with DNA barcoding, we detected elusive but frequent mammalian seed dispersers. The overall networks created by both methods were congruent but the plant species' degree, their interaction frequency and their specialization index (d′) differed. Our study suggests that DNA barcoding of defecated and regurgitated seeds can be used to construct quantitative seed deposition networks similar to those constructed by focal observations. To improve the overall completeness of seed dispersal networks it might be useful to combine both methods to detect interactions by both birds and mammals. Most importantly, the DNA barcoding method provides information on the post‐dispersal stage and thus on the qualitative contribution of each frugivore for the plant community thereby linking species interactions to regeneration dynamics of fleshy‐fruited plant species.
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Effective seed dispersal is essential to plant reproductive success. In this study, we evaluated the fruiting phenology, fruit traits, and seed dispersal of the endangered globose cactus Melocactus lanssensianus in the Brazilian Caatinga over 1-year period. We carried out monthly phenological monitoring, focal observations, and germination experiments, to identify the effective seed dispersers of this cactus. M. lanssensianus exhibited a continuous, non-seasonal fruiting pattern, with peaks during both the dry and rainy seasons. We observed seed dispersal by Tropidurus semitaeniatus and T. hispidus lizards. In 116 h of focal observations, lizards made 76 visits during different times of day, with a mean dispersal distance of 5 m. Both lizard species showed more frugivory interactions in the dry season, with peak visits in water-stressed months. We collected 132 intact and viable seeds from 29 fecal samples, specifically from T. semitaeniatus (N = 20 scats; 122 seeds) and from T. hispidus (N = 9 scats; 10 seeds). Germination experiments with seeds consumed by T. semitaeniatus, washed seeds and control seeds revealed that 85% of seeds found in T. semitaeniatus feces germinated compared to 41% of the control seeds. Frequency, pattern of visits and germination rates indicate T. semitaeniatus is an effective seed disperser of M. lanssensianus. Continuous production of fleshy fruits and environmental conditions of the Caatinga ecosystem favor the close dependent mutualistic interaction reported here.
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Modelling seed dispersal by animals seems straightforward; we need a way to keep track of the position on the animal through time and a clock for how long seeds travel with it. Mathematical models show how changing seed retention parameters can result in very different seed dispersal kernels, including fat-tailed ones. When movement is more realistic, in the sense that it is tied to the spatial distribution of resources, agent-based models result in both seed consumption and dispersal kernels varying according to the neighborhoods of focal plants. In general, agent-based models are built in ways that lead to overparameterization and poor predictive capacity. Considering several emergent properties that one wishes to capture and building a hierarchy of models varying in complexity should improve our understanding of the important mechanisms behind particular patterns. Progress in hierarchical data analysis tools allows fitting joint-species models in which species-level movement and foraging parameters are modelled as a function of species traits and their phylogenetic relationships. Overall, there has been great progress in data collection and modelling of seed dispersal by animals but we still need a better understanding of seed retention times, and of how bird physiology influences fruit choice. Further improvements in our ability to understand and predict seed dispersal by animals would probably also require considering individual personalities, as well as within and among species interactions. As our capacity to collect data bring us into the realm of big data and big models, important progress in mechanistic modelling of seed dispersal by animals should be achieved by close collaborations merging ecology, behavior, physiology, mathematics, computation and statistics.
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Alien invasive plant species are a major problem globally, threatening ecosystem functioning and biodiversity. Native bird species facilitate their spread through mutualistic relationships. Studies of seed dispersal of alien invasive plants are important for effective management. In the present study, we investigated the role of native bird species in the potential dispersal of the highly invasive shrub Lantana camara in KwaZulu-Natal, South Africa. We observed a total of 56 native bird species visiting fruiting L. camara with only 28 (50 %) species consuming the fruit. Visitation frequencies were significantly higher for small and medium-sized frugivorous species. The dark-capped bulbul Pycnonotus tricolor was the frugivorous bird species most observed visiting and is likely the main potential native avian disperser of L. camara. Interestingly, two non-frugivorous birds, the white-bellied sunbird Cinnyris talatala and the white-browed scrub-robin Cercotrichas leucophrys showed relatively high visitation frequencies to L. camara. Our study showed that L. camara benefits from seed dispersers and pollinators for seed reproduction and spread. These results emphasise the importance of evaluating the role of native bird species in the dispersal of alien invasive species.
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Renewable electricity is a key enabling step in the decarbonisation of energy. Europe is at the forefront of renewable deployment and this has dramatically increased the weather-sensitivity of the continent’s power systems. Despite the importance of weather to energy systems, and widespread interest from both academia and industry, the meteorological drivers of European power systems remain difficult to identify and poorly understood. This study presents a new and generally applicable approach, Targeted Circulation Types (TCTs). TCTs, in contrast to standard meteorological weather-regime or circulation-typing schemes, convolve the weather-sensitivity of an impacted system of interest (in this case, the electricity system) with the intrinsic structures of the atmospheric circulation to identify its meteorological drivers. A new 38-year reconstruction of daily electricity demand and renewable supply across Europe is used to identify the winter time large-scale circulation patterns of most interest to the European electricity grid. TCTs provide greater explanatory power for power system variability and extremes compared to standard meteorological typing. Two new pairs of atmospheric patterns are highlighted, both of which have marked and extensive impacts on the European power system. The first pair resembles the meridional surface pressure dipole of the North Atlantic Oscillation but shifted eastward into Europe and noticeably strengthened, while the second pair is weaker and corresponds to surface pressure anomalies over central southern and eastern Europe. While these gross qualitative patterns are robust features of the present European power systems, the detailed circulation structures are strongly affected by the amount and location of renewables installed.
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The first wave of human colonists spread across the Pacific from 4000 to 1000 years ago. That they caused many extinctions is well known from fossil finds. We estimate how many fossil species were missed - the answer is roughly half - and so estimate the true extinction rate. The first colonists exterminated roughly half the species on each island group. Some of these extinctions are falsely attributed to the first colonists, because intensive collection often began a half century after the damage initiated by European discovery. Even taken at face value, these recent extinctions are too few. Many species are so critically endangered that we know neither whether they still survive or how to save them. Interestingly, there are fewer recent extinctions and currently endangered species in the islands of the western Pacific, which were the islands occupied first by humans. We suggest that the species sensitive to human occupation died out long ago in these areas. If so, these islands would have lost even more than half of their bird species.
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We examined the effect of frugivorous bats and birds on the population dynamics of the giant columnar cactus Neobuxbaumia tetetzo in the Tehuacan Valley, Mexico. Because successful seedling establishment occurs only beneath the canopies of shrubs and trees, we hypothesized that seed dispersal is a key process in the maintenance of its populations. We determined the dispersal effectiveness of different frugivores, considering the quantity and quality components of seed dispersal. We also evaluated the potential effects of each frugivore species on the finite rate of increase of N. tetetzo populations by modifying the fecundity values of a Lefkovitch matrix model. The bat Leptonycteris curasoae had the highest effectiveness whereas the bird Carpodacus mexicanus had the lowest. The estimated finite rates of increase calculated to evaluate the effects of frugivores on the population dynamics of the cactus differ marginally from unity, except when the effect of the bat L. curasoae was analyzed. Our results suggest that the bat Leptonycteris curasoae could be considered the legitimate dispersal agent of N. tetetzo, dispersing seeds directly to safe sites, and thus representing a key species in the ecology of this columnar cactus.
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FORUM is intended for new ideas or new ways of interpreting existing information. Itprovides a chance for suggesting hypotheses and for challenging current thinking onecological issues. A lighter prose, designed to attract readers, will be permitted. Formalresearch reports, albeit short, will not be accepted, and all contributions should be concisewith a relatively short list of references. A summary is not required.
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A high number of tree species, low density of adults of each species, and long distances between conspecific adults are characteristic of many low-land tropical forest habitats. I propose that these three traits, in large part, are the result of the action of predators on seeds and seedlings. A model is presented that allows detailed examination of the effect of different predators, dispersal agents, seed-crop sizes, etc. on these three traits. In short, any event that increases the efficiency of the predators at eating seeds and seedlings of a given tree species may lead to a reduction in population density of the adults of that species and/or to increased distance between new adults and their parents. Either event will lead to more space in the habitat for other species of trees, and therefore higher total number of tree species, provided seed sources are available over evolutionary time. As one moves from the wet lowland tropics to the dry tropics or temperate zones, the seed and seedling predators in a habitat are hypothesized to be progressively less efficient at keeping one or a few tree species from monopolizing the habitat through competitive superiority. This lowered efficiency of the predators is brought about by the increased severity and unpredictability of the physical environment, which in turn leads to regular or erratic escape of large seed or seedling cohorts from the predators.
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This is the second edition of a multi-author book first published in 1992. It deals with all aspects of plant regeneration by seeds, including reproductive allocation, seed dispersal and predation, longevity, dormancy and germination. All chapters have been updated, and four new chapters added on seed size, seedling establishment, the role of gaps, and regeneration from seed after fire.
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We evaluate whether species interaction frequency can be used as a surrogate for the total effect of a species on another. Because interaction frequency is easier to estimate than per-interaction effect, using interaction frequency as a surrogate of total effect could facilitate the large-scale analysis of quantitative patterns of species-rich interaction networks. We show mathematically that the correlation between interaction frequency (I) and total effect (T) becomes more strongly positive the greater the variation of I relative to the variation of per-interaction effect (P) and the greater the correlation between I and P. A meta-analysis using data on I, P and T for animal pollinators and seed dispersers visiting plants shows a generally strong, positive relationship between T and I, in spite of no general relationship between P and I. Thus, frequent animal mutualists usually contribute the most to plant reproduction, regardless of their effectiveness on a per-interaction basis.
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Mutualistic disruptions, such as those promoted by the loss of seed dispersers, can have negative effects on the plant regeneration of those species that strongly depend upon them. In order to adequately assess how plant communities are affected by such disruptions, we need to know the importance of the dispersal phase, both in its quantitative and qualitative components. We examined this in the narrow interaction between the shrub Daphnerodriguezii and its (only) disperser, the lizard Podarcislilfordi. We quantified fruit removal and the effect of fruit/seed-size selection, seed treatment in the disperser’s guts and seed deposition patterns on seedling emergence and survival. In the only locality in which lizards persist, they removed most fruits and showed preference for larger ones in one of the two study years. Seed treatment in lizard’s guts had no effect on germination, although it tended to reduce the effect of seed size on germination (differences between large vs. small seeds in seed germination were higher for non-ingested seeds). Probability of seedling emergence, but not survival, was higher in the locality with lizards. Dispersed seeds under heterospecific shrubs showed higher seedling survival than those under conspecifics in all localities, especially the year with higher rainfall. Our findings support that the movement of seeds to nurse shrubs by lizards is the most important component of the seed dispersal process in the only remaining locality where both species coexist. Keywords Daphnerodriguezii -Mutualism disruption- Podarcislilfordi -Saurochory-Seed ingestion-Seed size-Seedling emergence and survival
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Aim Species richness of insect herbivores feeding on exotic plants increases with abundance as well as range size of the host in the area of introduction. The formation of these herbivore assemblages requires a certain amount of time, and the richness of insect faunas should also increase with the length of time an exotic plant has been present in the introduced range. Location Central Europe. Methods We analysed the variation in species richness of leaf-chewing Lepidoptera larvae and sap-sucking Auchenorrhyncha (Hemiptera) associated with 103 exotic woody plant species in Germany in relation to time since introduction, range size, growth form (trees versus shrubs), biogeographical origin (distance from Central Europe) and taxonomic isolation of the host plant (presence or absence of a native congener in the introduced area). Results Using simple correlation analyses we found for Lepidoptera and Auchenorrhyncha that species richness increased with time since introduction of the host plant. For the Lepidoptera the increase of species richness with time since introduction remained significant even after removing the effects of all other independent variables. Main conclusions Our results provide some evidence that assemblages of insects on exotic plants do not reach saturation within a time scale of few hundred years. This contrasts with previous findings for crop plants.
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Although it is well established that many insects, birds and mammals serve as important pollinators and seed dispersers of flowering plants, the role of lizards in these processes has traditionally been considered as rare and less important. However, recent work shows both that their role as mutualistic agents has been underestimated and also reveals a striking pattern – that pollination and seed dispersal by lizards is most common on islands. We argue that this island phenomenon occurs because island lizards reach very high densities (density compensation) and experience a lower predation risk than do those on the mainland and, consequently, can expand their diet to include nectar, pollen and fruit. Although further empirical evidence is needed to confirm this explanation, such relationships could be ideal systems with which to study fundamental ecological problems, such as niche shifts, ecological release and competition.
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The mutually beneficial interactions between plants and their animal pollinators and seed dispersers have been paramount in the generation of Earth’s biodiversity. These mutualistic interactions often involve dozens or even hundreds of species that form complex networks of interdependences. Understanding how coevolution proceeds in these highly diversified mutualisms among free-living species presents a conceptual challenge. Recent work has led to the unambiguous conclusion that mutualistic networks are very heterogeneous (the bulk of the species have a few interactions, but a few species are much more connected than expected by chance), nested (specialists interact with subsets of the species with which generalists interact), and built on weak and asymmetric links among species. Both ecological variables (e.g., phenology, local abundance, and geographic range) and past evolutionary history may explain such network patterns. Network structure has important implications for the coexistence and stability of species as well as for the coevolutionary process. Mutualistic networks can thus be regarded as the architecture of biodiversity.
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Growth in seed dispersal studies has been fast-paced since the seed disperser effectiveness (SDE) framework was developed 17 yr ago. Thus, the time is ripe to revisit the framework in light of accumulated new insight. Here, we first present an overview of the framework, how it has been applied, and what we know and do not know. We then introduce the SDE landscape as the two-dimensional representation of the possible combinations of the quantity and the quality of dispersal and with elevational contours representing isoclines of SDE. We discuss the structure of disperser assemblages on such landscapes. Following this we discuss recent advances and ideas in seed dispersal in the context of their impacts on SDE. Finally, we highlight a number of emerging issues that provide insight into SDE. Overall, the SDE framework successfully captures the complexities of seed dispersal. We advocate an expanded use of the term dispersal encompassing the multiple recruitment stages from fruit to adult. While this entails difficulties in estimating SDE, it is a necessary expansion if we are to understand the central relevance of seed dispersal in plant ecology and evolution.
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We summarize the recent information on field metabolic rates (FMR) of wild terrestrial vertebrates as determined by the doubly labeled water technique. Allometric (scaling) relationships are calculated for mammals (79 species), reptiles (55 species), and birds (95 species) and for various taxonomic, dietary, and habitat groups within these categories. Exponential equations based on body mass are offered for predicting rates of daily energy expenditure and daily food requirements of free-ranging mammals, reptiles, and birds. Significant scaling differences between various taxa, dietary, and habitat groups (detected by analysis of covariance with P < or = 0.05) include the following: (a) The allometric slope for reptiles (0.889) is greater than that for mammals (0.734), which is greater than that for birds (0.681); (b) the slope for eutherian mammals (0.772) is greater than that for marsupial mammals (0.590); (c) among families of birds, slopes do not differ but elevations (intercepts) do, with passerine and procellariid birds having relatively high FMRs and gallinaceous birds having low FMRs; (d) Scleroglossan lizards have a higher slope (0.949) than do Iguanian lizards (0.793); (e) desert mammals have a higher slope (0.785) than do nondesert mammals; (f) marine birds have relatively high FMRs and desert birds have low FMRs; and (g) carnivorous mammals have a relatively high slope and carnivorous, insectivorous, and nectarivorous birds have relatively higher FMRs than do omnivores and granivores. The difference detected between passerine and nonpasserine birds reported in earlier reviews is not evident in the larger data set analyzed here. When the results are adjusted for phylogenetic effects using independent contrasts analysis, the difference between allometric slopes for marsupials and eutherians is no longer significant and the slope difference between Scleroglossan and Iguanian lizards disappears as well, but other taxonomic differences remain significant. Possible causes of the unexplained variations in FMR that could improve our currently inaccurate FMR prediction capabilities should be evaluated, including many important groups of terrestrial vertebrates that remain under- or unstudied and such factors as reproductive, thermoregulatory, social, and predator-avoidance behavior.
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We present a general framework for characterizing the ecological and societal consequences of biodiversity loss and applying it to the global avifauna. To investigate the potential ecological consequences of avian declines, we developed comprehensive databases of the status and functional roles of birds and a stochastic model for forecasting change. Overall, 21% of bird species are currently extinction-prone and 6.5% are functionally extinct, contributing negligibly to ecosystem processes. We show that a quarter or more of frugivorous and omnivorous species and one-third or more of herbivorous, piscivorous, and scavenger species are extinction-prone. Furthermore, our projections indicate that by 2100, 6-14% of all bird species will be extinct, and 7-25% (28-56% on oceanic islands) will be functionally extinct. Important ecosystem processes, particularly decomposition, pollination, and seed dispersal, will likely decline as a result.
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Long-distance dispersal (LDD) of plants poses challenges to research because it involves rare events driven by complex and highly stochastic processes. The current surge of renewed interest in LDD, motivated by growing recognition of its critical importance for natural populations and communities and for humanity, promises an improved, quantitatively derived understanding of LDD. To gain deep insights into the patterns, mechanisms, causes, and consequences of LDD, we must look beyond the standard dispersal vectors and the mean trend of the distribution of dispersal distances. “Nonstandard” mechanisms such as extreme climatic events and generalized LDD vectors seem to hold the greatest explanatory power for the drastic deviations from the mean trend, deviations that make the nearly impossible LDD a reality.
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Frugivores are highly variable in their contribution to fruit removal in plant populations. However, data are lacking on species-specific variation in two central aspects of seed dispersal, distance of dispersal and probability of dispersal among populations through long-distance transport. We used DNA-based genotyping techniques on Prunus mahaleb seeds dispersed by birds (small- and medium-sized passerines) and carnivorous mammals to infer each seed's source tree, dispersal distance, and the probability of having originated from outside the study population. Small passerines dispersed most seeds short distances (50% dispersed <51 m from source trees) and into covered microhabitats. Mammals and medium-sized birds dispersed seeds long distances (50% of mammals dispersed seeds >495 m, and 50% of medium-sized birds dispersed seeds to >110 m) and mostly into open microhabitats. Thus, dispersal distance and microhabitat of seed deposition were linked through the contrasting behaviors of different frugivores. When the quantitative contribution to fruit removal was accounted for, mammals were responsible for introducing two-thirds of the immigrant seeds into the population, whereas birds accounted for one-third. Our results demonstrate that frugivores differ widely in their effects on seed-mediated gene flow. Despite highly diverse coteries of mutualistic frugivores dispersing seeds, critical long-distance dispersal events might rely on a small subset of large species. Population declines of these key frugivore species may seriously impair seed-mediated gene flow in fragmented landscapes by truncating the long-distance events and collapsing seed arrival to a restricted subset of available microsites.
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Aim The genetic structure of many plant species is heavily dependent on their pollinators and seed dispersers, and can thus be altered if either of the associated mutualistic interactions is disrupted. In this study we assess the genetic diversity and structure and infer the seed/pollen gene-flow patterns among insular populations of Daphne rodriguezii, a shrub pollinated and dispersed by animals that has lost its only disperser (the lizard Podarcis lilfordi) in most of its populations. Location The island of Menorca and the islet of Colom (Balearic Islands, Western Mediterranean). Methods To assess the contribution of gene flow via pollen and seeds to the genetic structure of D. rodriguezii we used amplified fragment length polymorphisms (AFLPs; seeds and pollen) and plastid DNA sequences (cpDNA; seeds). We sampled individuals from all population nuclei of the species (12–19 adults per population): one population in Colom, where the plant–lizard interaction persists, and four in Menorca, where the seed dispersal mutualism disappeared with the extinction of the lizard. Results The highest heterozygosity values were found in Colom and in its closest population (Favàritx), whereas values were lower in the smallest Menorcan populations, which also had higher relatedness among individuals. We found distinct genetic signals between AFLP and cpDNA analyses. While AFLP markers showed low differentiation between populations, cpDNA showed a clear differentiation between them. Main conclusions Our results point to negative impacts of the disperser loss on genetic diversity and relatedness in the smaller and more isolated populations. They also suggest an old isolation by seeds, probably occurring well before the extinction of the lizard (c. 2000 years ago). Gene flow was maintained via pollination; however, the seed disperser loss may ultimately hinder pollinator-mediated gene flow, as a result of reduced probabilities of effective pollination among increasingly distant and scarce individuals.
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In this paper, we present results on germination patterns of the seed dispersal system of an endemic Macaronesian plant (Rubia fruticosa). Seeds from this plant are mainly dispersed by endemic lizards and native warblers; therefore, we included three different treatments: control seeds, seeds extracted from lizards and seeds found in warbler droppings. Seeds from the same pool of every treatment were germinated in two different seasons, one in autumn, coinciding with the arrival of the first rains, and another in spring, coinciding with the arrival of the dry season. A clear differential pattern of germination success was observed between the two seasons. Seeds planted in autumn achieved a higher percentage of germination than those sown in spring in all treatments. The great robustness of these results seems to indicate that germination timing is strongly selected in R. fruticosa and this evolutionary trend probably extends to other vascular plants growing in xeric coastal environments of the Macaronesian islands.
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We studied, for the first time, the effect of insularity on plant-seed disperser networks at both the community and species level. We focused on the Mediterranean shrubland, comparing different biogeographical scenarios (insular and continental) that share the same basic species composition. The study was conducted on one mainland (south-eastern Spain) and four island localities: two in the Canary Islands (oceanic origin) and two in the Balearic Islands (continental origin). We built qualitative (presence/absence of interaction) and quantitative seed dispersal networks (number of consumed fruits) and used different descriptor parameters, such as connectance, nestedness, interaction asymmetry and various interaction diversity indices that describe their topology. To assemble the interaction networks, we used data on the presence of different species of fruits in systematically collected droppings of the different seed dispersers; seeds in droppings were identified by means of a binocular lens whereas a microscope was used to identify pericarp tissue remains. We found that island networks were smaller and less complex (a lower number of observed links than expected for their size) than the mainland network. As expected, connectance was higher within islands than on the mainland. By contrast, nestedness was consistently high at all sites, although relative nestedness (which accounts for network size) was lower within islands, whether continental or oceanic. At both community and species level (especially for animals) interactions tended to be more specialized and symmetric within the islands. The lower species number and greater specialization in insular seed dispersal systems appears to lead to the prevalence of more symmetric interactions than those found on the mainland. This indicates that insular mutualistic interactions and interacting species are more vulnerable than mainland ones to disturbances, as previous work has suggested that asymmetrical interactions facilitate the maintenance of biodiversity and act as a resilience mechanism against species extinction.
Article
Investigations on vertebrate seed dispersal systems in the Mediterranean show that extremely efficient plant-disperser mutualisms do not require, and thus are not evidence for, mutual evolutionary adjustments of participants. Current Mediterranean dispersal systems have apparently been shaped by means of 1. trophic and behavioral adaptations of birds morphologically preadapted to pre-existing plant resources, and 2. disperser-mediated processes of habitat-shaping occurring at an ecological time scale. These processes depend on differential recruitment of plant species as a function of disperser preferences, rather than on adjustments based on evolutionary processes. On the plant side, there is a prevalence of historical and phylogenetic effects, which reflects a series of ecological limitations inherent to the interactions between plants and dispersal agents that constrain plant adaptation to dispersers. To test adaptive hypotheses and explanations, future investigations on Mediterranean plant-disperser systems should concentrate more on the animal than on the plant side of the interaction.
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I studied the thermoregulatory behavior of a field population of the Canarian lizard Gallotia galloti, using null hypotheses based on (1) the measurement of operative temperatures available in full sun land in the shade (T-e), and (2) the distribution of randomly positioned models with respect to sun and shade. The activity curve of the lizard population was unimodal, with a pronounced peak in the morning and lower (though roughly constant) levels at later times of day. Activity levels were positively correlated with the difference between T-e in the sun and T-e in the shade, but negatively correlated with T-e in the shade. The distribution of lizards into sun-shade categories was highly selective relative to paper models, with an overall daily selectivity pattern that was symmetrical around midday (selection of sunlit perches early and late in the day, shade seeking at midday, and random distribution at intermediate hours). The low dispersion of hourly mean operative temperatures at lizard perching sites relative to random locations of models (average values calculated weighting mean T(e)s with frequencies of sun-shade use and sun-shade availability) suggested a high degree of thermoregulatory precision. Dark, adult males basked for longer periods than juveniles, whereas subadults/females showed intermediate basking times, which suggests that body size and color differences may play a role in behavioral thermoregulation by these lizards.