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Comparing seed dispersal effectiveness by frugivores at the community level
Ecology
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.
... The lower species richness of island communities compared to continental ones makes such an endeavour more tractable on islands. There are an increasing number of studies based on the SDE framework in insular areas (e.g., González-Castro et al., 2015a;McConkey & Drake, 2015;Nogales et al., 2017;Muñoz-Gallego et al., 2019;Nakabayashi et al., 2019). ...
... SDE studies worldwide are progressively increasing the number of animal species characterized (e.g., Howe, 1977;Reid, 1989;Graham et al., 1995;Jordano & Herrera, 1995;Stevenson 2000;Jordano & Schupp, 2000;Calviño-Cancela & Martín-Herrero, 2009;Li et al., 2016;Camargo et al. 2016). And, to our knowledge, the most comprehensive studies that have undertaken the challenge of studying many members at a plant community level (i.e., focusing on the dispersal service provided by animals to the many fleshy-fruited species in a local plant community) have been made on islands (Carlo et al., 2003;González-Castro et al., 2015a;McConkey & Drake, 2015;Nogales et al., 2017). ...
... By and large, the use of the SDE conceptual framework to estimate dispersal by frugivores on islands has revealed high complementarity (i.e., low redundancy) among vertebrate dispersers. This pattern suggests that plants could be vulnerable to the decline or extinction of their most crucial disperser group (González-Castro et al., 2015a;McConkey & Drake, 2015;Morán-López et al., 2020), perhaps as a result of earlier frugivore losses. It can explain the severe consequences of disperser loss for plant reproductive success which have been reported from different archipelagos (Meehan et al., 2002;Rodríguez-Pérez & Traveset, 2010;McConkey & Drake, 2006;Chimera & Drake 2010, 2011Pérez-Méndez et al., 2016). ...
We provide an overview of the current state of knowledge of island frugivory and seed dispersal and identify knowledge gaps that are important for fundamental research on—and applied conservation of—island ecosystems. We conducted a systematic literature search of frugivory and seed dispersal on islands, omitting large, continental islands. This revealed a total of 448 studies, most (75%) published during the last two decades, especially after 2010. Nearly 65% of them were focused on eight archipelagos. There is a paucity of studies in Pacific archipelagos near Asia and Australia, and in the Indian Ocean. Data on island frugivory and seed dispersal are diverse but highly uneven in geographic and conceptual coverage. Despite their limited biodiversity, islands are essential reservoirs of endemic plants and animals and their interactions. Due to the simplicity of insular ecosystems, we can assess the importance of seed dispersal theory and mechanisms at species and community levels. These include the ecological and biogeographical meaning and prevalence of non-standard mechanisms of seed dispersal on islands; the seed dispersal effectiveness and the relative roles of different frugivore guilds (birds and reptiles being the most important); and patterns of community organization and their drivers as revealed by interaction networks. Island systems are characterized by the extinction of many natives and endemics, and high rates of species introductions. Therefore, understanding how these losses and additions alter seed dispersal processes has been a prevailing goal of island studies and an essential foundation for the effective restoration and conservation of islands.
... Quantifying seed dispersal by frugivores is crucial for expanding our understanding of the complex dispersal systems of plants [28]. Seed dispersal effectiveness by frugivores depends on both the "quantity" and "quality" of dispersal [29]. The quantity focuses on the frequency and intensity of animals' visits to the mother plant, which is quantified by the volume of visits and the amount of fruit or seeds removed within a specific time [18,30]. ...
... Seed dispersal effectiveness by frugivores depends on both quantity and quality [29]. In terms of quantity, a higher frequency of animal visits results in a greater number of seeds dispersed per visit, thereby increasing the seed dispersal range and the chances of plant population renewal [56,57]. ...
... Within seed dispersal networks, various animal groups display unique characteristics in the efficient dispersal of seeds, resulting in variations in their contributions to the reproduction of plants [29]. In this study, six different types of animals were observed visiting the ground fruits of M. sieversii (Figure 3). ...
The success of plant reproduction is highly dependent on effective seed dispersal. This study aimed to evaluate the potential seed dispersal effectiveness of cattle for Malus sieversii. The impact of cattle on the dispersal quantity and dispersal quality of M. sieversii seeds was explored based on camera trapping, GPS tracking, and germination trials. The results showed that, on average, cattle visited M. sieversii trees 477.33 times during a two-month observation period. Out of these visits, 315 were specifically for fruit removal. The fruit removal rate per cattle visit was as high as 96.67%. Additionally, cattle were able to disperse M. sieversii seeds up to a maximum distance of 533.67 m, with an average dispersal distance of 134.62 m. The average distance of cattle movement was recorded as 176.95 m/h, with peak activity observed during 11:00–13:00 and 19:00–21:00. The germination rate of M. sieversii seeds that passed through the digestive tract of cattle was significantly higher than that of control seeds. Finally, the emergence rate and survival rate of seeds dispersed by cattle to forest edges and gaps were significantly higher than those dispersed to understory. These findings suggest that cattle can serve as effective long-distance dispersers of M. sieversii seeds and may play a crucial role in the regeneration and expansion of M. sieversii populations in the Ili Botanical Garden.
... 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). ...
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.
... 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. ...
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.
... 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. ...
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.
... 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. ...
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 whether 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.
A free Plain Language Summary can be found within the Supporting Information of this article.
... While the quantitative component refers to the number of seeds removed and transported away from parental plants, the quality component is the probability of a given seed to produce a new plant (Schupp, 1993). From the animal perspective, most studies focus on the role of interspecific traits in determining quantitative contributions of different species of frugivores to seed dispersal (Campagnoli & Christianini, 2021;Godínez-Alvarez et al., 2020;González-Castro et al., 2015;Schupp et al., 2010). ...
... To estimate the contribution of a species to seed dispersal, most studies rely on average values of the quality component, extracted from different individuals, and treat all variation as random noise (Godínez-Alvarez et al., 2020;González-Castro et al., 2015;Jordano et al., 2007). However, grouping individuals of a species and relying on averages may be problematic, because there is often a large intraspecific variation in morphological, physiological, and behavioral traits among individuals (Ball & Balthazart, 2007;Møller & Garamszegi, 2012;Tobias et al., 2022). ...
Frugivorous animals play crucial roles dispersing seeds away from parental plants and influencing plant recruitment. Most studies focus on comparisons of seed dispersal services provided by distinct species of animals, but neglect how within-species variation may affect dispersal. Individual traits, such as body mass and sex, are related to metabolic rates, gut load capacity, and transit times that potentially influence dispersal quantity and quality. Here, we aim at answering if individual traits (body mass and sex) of Pale-breasted Thrushes (Turdus leucomelas) affect seed dispersal quality by testing the following hypotheses (a) individual traits influence seed retention time and germination, (b) seed retention time affects seed germination, and (c) seed passage through the gut enhances germination. We found that females retained seeds in the gut for longer periods than males. Gut passed and manually depulped seeds had similar germination success. However, heavier birds, irrespective of sex, had longer seed retention times and promoted higher germination. Our results indicate that intraspecific differences in morphological traits of frugivores are a source of variation in dispersal outputs and may help to explain complex patterns of seed dispersal. We highlight the importance of considering the quality of seed dispersal at an individuallevel, as well as at a species-level, and reinforce that some individuals may contribute more to seed germination, and potentially recruitment, than others. Finally, a decrease in body masses of tropical birds in response to global warming may cascade to a decrease in seed dispersal quality.
... While the quantitative component refers to the number of seeds removed and transported away from parental plants, the quality component is the probability of a given seed to produce a new plant (Schupp, 1993). From the animal perspective, most studies focus on the role of interspecific traits in determining quantitative contributions of different species of frugivores to seed dispersal (Campagnoli & Christianini, 2021;Godínez-Alvarez et al., 2020;González-Castro et al., 2015;Schupp et al., 2010). ...
... To estimate the contribution of a species to seed dispersal, most studies rely on average values of the quality component, extracted from different individuals, and treat all variation as random noise (Godínez-Alvarez et al., 2020;González-Castro et al., 2015;Jordano et al., 2007). However, grouping individuals of a species and relying on averages may be problematic, because there is often a large intraspecific variation in morphological, physiological, and behavioral traits among individuals (Ball & Balthazart, 2007;Møller & Garamszegi, 2012;Tobias et al., 2022). ...
Frugivorous animals play crucial roles dispersing seeds away from parental plants and influencing plant recruitment. Most studies focus on comparisons of seed dispersal services provided by distinct species of animals, but neglect how within‐species variation may affect dispersal. Individual traits, such as body mass and sex, are related to metabolic rates, gut load capacity, and transit times that potentially influence dispersal quantity and quality. Here, we aim at answering if individual traits (body mass and sex) of Pale‐breasted Thrushes ( Turdus leucomelas ) affect seed dispersal quality by testing the following hypotheses (a) individual traits influence seed retention time and germination, (b) seed retention time affects seed germination, and (c) seed passage through the gut enhances germination. We found that females retained seeds in the gut for longer periods than males. Gut passed and manually depulped seeds had similar germination success. However, heavier birds, irrespective of sex, had longer seed retention times and promoted higher germination. Our results indicate that intraspecific differences in morphological traits of frugivores are a source of variation in dispersal outputs and may help to explain complex patterns of seed dispersal. We highlight the importance of considering the quality of seed dispersal at an individual‐level, as well as at a species‐level, and reinforce that some individuals may contribute more to seed germination, and potentially recruitment, than others. Finally, a decrease in body masses of tropical birds in response to global warming may cascade to a decrease in seed dispersal quality.
Abstract in Portuguese is available with online material.
... Legitimate seed dispersers also exhibited limited variation in the quality component of seed dispersal effectiveness (Figure 3). The resulting probability of recruitment per consumed fruit was surprisingly similar between frugivore species, indicating a broad functional redundancy in their dispersal service (González-Castro et al., 2015). However, when considering the final seed dispersal effectiveness, two bird species (C. ...
... Such high reciprocity appears characteristic of many seed dispersal systems and other generalised, resource-based mutualisms (Ollerton, 2006;Wheelwright & Orians, 1982). However, reciprocity in a mutualistic system could be compromised whenever there are large differences between partners quality, as occurs for example in systems with highly heterogeneous frugivore assemblages (García-Rodríguez et al., 2021;González-Castro et 2015). Reciprocity can also be broken when antagonists disrupt, to a variable extent, mutualistic interactions of plants with legitimate seed dispersers (Jácome-Flores et al., 2020); however, mutualism breakdown scenarios have been largely examined for intimate interactions, not for free-living species (Chomicki & Renner, 2017;Sachs & Simms, 2006). ...
Mutualistic interactions among free‐living species generally involve low‐frequency interactions and highly asymmetric dependence among partners, yet our understanding of factors behind their emergence is still limited. Using individual‐based interactions of a super‐generalist fleshy‐fruited plant with its frugivore assemblage, we estimated 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 frugivore species, while frugivores interacted with most individual plants, resulting in strong asymmetries of mutual dependence. Interaction effectiveness was mainly driven by interaction frequency. Despite highly asymmetric dependences, the strong reliance on quantity of fruit consumed determined high reciprocity in rewards between partners (i.e. higher energy provided by the plant, more seedlings recruited), which was 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.
... 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. ...
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.
... 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. ...
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.
... Before multiplication in Equation (5), we transformed the degree of insectivory into a proportion. This approach combines a quality component (agronomic quality) with a quantity component (abundance weighted by degree of insectivory), and it is equivalent to the effectiveness framework used to assess species contributions in other animal-driven ecosystem services, such as seed dispersal and pollination (González-Castro et al. 2015, Gómez et al. 2022). ...
Insectivorous birds provide an essential ecosystem service in agriculture by feeding on arthropods considered pests but can also consume arthropods considered to be natural enemies of such pests. Therefore, depending on the dietary composition of the birds, intraguild predation could outweigh pest control services. This study addressed the agronomic quality, defined as the trade-off between ecosystem services (pest control) and disservices (intraguild predation), of 26 insectivorous bird species in culturally and economically important cider apple orchards in northern Spain. We used DNA-metabarcoding techniques to analyze bird’ diets. First, we examined whether the trophic position of bird species can be inferred from functional traits related to foraging and movement behavior and from the degree of insectivory in their diets. Then, we tested whether bird abundance and trophic position influenced agronomic quality, based on the proportion of arthropod crop pests and natural enemies in their diet. Finally, we combined bird abundance, insectivory and agronomic quality to infer the potential contribution of each bird species to pest control. Bird trophic position was positively related to the degree of insectivory, with this effect being modulated by traits related to body size. The trophic position of birds was inversely related to their agronomic quality. Nevertheless, the agronomic quality only slightly affected the differential contribution of bird species to the whole assemblage effect. Overall, we found the potential of insectivorous bird species to control pests can be estimated based on their trophic position. Yet, in agroecosystems with uneven avian species abundance, the potential contribution of bird species to pest-control services may be driven by their quantitative contribution rather than by the bird’s per capita, qualitative effects. Finally, our results suggest that rare insectivorous birds may have a redundant role in pest control, due to the overwhelming functional dominance of common species.
... Therefore, the outcomes of seed germination are species-specific and can hardly be transposed between different plant-frugivore interactions. Although key to SDE, frugivore gut treatment and its effect on seed germination are often neglected in communitylevel studies (but see Fricke et al., 2019;González-Castro, Calviño-Cancela, et al., 2015;Nogales et al., 2017 for examples in oceanic islands). ...
Seed dispersal by frugivores is a crucial step of the life cycle of most plants, influencing plant population and community dynamics. Although very important for most ecosystems, we are just beginning to understand which are the mechanisms driving frugivore‐mediated seed dispersal. Most studies identifying the drivers of seed dispersal use interaction frequency as a proxy for estimating seed dispersal success, rather than looking at the functional outcomes of those interactions (e.g., contributions to successful seed germination). A valuable tool to link plant–frugivore interactions to seed dispersal success is the seed dispersal effectiveness (SDE) framework, which accounts for the quantity and quality components of seed dispersal.
We evaluated which mechanisms, including morphological traits, trait matching and phenological overlap of interacting species, as well as degree of frugivory and feeding behaviour of frugivores, influenced the quantity (interaction frequency and number of seeds dispersed per visit) and quality (seed germination after gut passage) components of SDE. To this end, we combined three methods (focal observations, mist‐netting and camera traps) to sample interactions between plants, birds and mammals in a species‐rich community of Cerrado in southeastern Brazil.
We recorded 590 pairwise interactions between 34 plants and 49 frugivores. We found that phenological overlap among interacting species explained most of the variation in interaction frequencies. Trait matching affected the number of seeds dispersed per visit more for gulpers than mashers and peckers, and frugivore body mass and seed sizes positively affected seed germination. Finally, interaction frequencies had a stronger contribution to SDE, compared with the number of seeds dispersed per visit and seed germination, indicating an indirect effect of phenological overlap on SDE.
Synthesis. We found that highly abundant plant–frugivore species with the most overlap in their phenologies also yield the highest values of SDE, suggesting that phenological overlap was the most important driver of SDE in this hyperdiverse community. However, the number of seeds dispersed per visit also influenced SDE and seed germination was species‐specific, suggesting that estimating SDE at the community level is necessary to understand how communities work, and the current and future challenges they face.
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... La componente cualitativa refleja los efectos per cápita de las interacciones, es decir, aquellos asociados a la identidad de las especies participantes e independientes de su abundancia o frecuencia de interacción (Herrera, 1987;Schupp et al., 2010). Por ejemplo, distintos dispersores de semillas pueden provocar efectos diferentes en la capacidad de germinación de las semillas debido a distintos tiempos de retención en el tracto digestivo, así como distintas expectativas de supervivencia de las semillas frente a los depredadores en función de dónde las depositan (González-Castro et al., 2015). Desde la perspectiva animal, distintas plantas ofrecen recursos en su néctar, polen o frutos que son cualitativamente diferentes en términos de aprovechamiento y calidad nutricional. ...
Las interacciones mutualistas planta–animal (IMPA) incluyen aquellas
relaciones entre plantas y animales que, a través de efectos ecológicos
positivos y recíprocos, pueden llegar a operar como fuerzas de selección
natural. Aunque el papel demográfico y evolutivo de las IMPA es bien
conocido desde hace décadas, estas interacciones rara vez se analizan como
funciones y/o servicios de los ecosistemas. En este capítulo interpretamos la
polinización y la dispersión de semillas por animales como procesos ecosistémicos
cuya magnitud y estabilidad dependen de la propia biodiversidad
contenida en las interacciones ecológicas. Para ello consideramos los efectos
funcionales de las IMPA a la hora de regular la biomasa y la abundancia de
las especies en las redes tróficas, a través de componentes que representan
tanto la cantidad como la calidad de las interacciones. También resaltamos
que numerosos estudios muestran los efectos positivos de la abundancia y la
riqueza de especies de animales en la magnitud de las funciones de polinización
y dispersión de semillas. Estos vínculos positivos se explican a partir de
diferentes mecanismos como los efectos de muestreo, la complementariedad
de nicho y la facilitación interespecífica. Menos estudiado ha sido el papel
positivo de la biodiversidad en la estabilidad de la polinización y la dispersión
de semillas, que potencialmente surge de efectos portafolio, de compensación
de densidad o de diversidad de respuesta. Tener en cuenta los rasgos de las
especies que participan en las IMPA —interpretados como rasgos de efecto
funcional o de respuesta a las perturbaciones— ayuda a entender mejor la
resiliencia de la polinización y la dispersión de semillas frente a las perturbaciones
y los impactos antrópicos. En un mundo donde multitud de especies
vegetales y animales sufren declives poblacionales y extinciones locales de
manera generalizada, y donde el bienestar diario de millones de personas
se ve progresivamente afectado por la pérdida de servicios de los ecosistemas,
resulta prioritario estudiar los mecanismos que regulan el resultado
funcional de las interacciones ecológicas.
... The complementarity of the dispersal by the community of short-distance frugivore passerines and long-distance generalist mammals was shown by the model to be an important ecosystem service promoting colonization and expansion in fragmented landscapes. González-Castro et al. [18] resorted to StoX for the first ever SDE study at community level, encompassing the eleven plant species that account for the 99.9% of fleshy fruits produced in the most threatened habitat in the Macaronesian Islands, the thermophile belt. The study included six native dispersers (an endemic lizard and five passerines) to build the SDE landscapes [1] for two years. ...
Seed dispersal effectiveness measures the number of new plants effectively produced by the services of seed disperser agents. This depends on a complex process involving multiple stages and actors, and has profound implications for conservation. StoX is a distribution agnostic multistage stochastic model that differentiates among dispersers in their contribution to seed rain and recruitment. It can be parameterized with quantity and quality components of dispersal measured in the field. It preserves the inherent stochastic nature of the recruitment process and can be validated by statistical comparison between its predictions and recruitment patterns in the field. StoX has already been used in several successful studies, at both population and community levels.
... This adaptable marking behaviour of red fox translates into shifts in seed-arrival patterns (García-Cervigón et al., 2018), with proportionally fewer seeds being deposited in open environments. Habitat suitability is a qualitative component of seeddispersal effectiveness (Schupp, 2007) that impacts the probability of seedling recruitment and thereby influences the quality of dispersal services (Beckman & Rogers, 2013;González-Castro et al., 2015). In ...
Current global change scenarios demand knowledge on how anthropogenic impacts affect ecosystem functioning through changes in food web structure. Frugivorous mesocarnivores are a key link in trophic cascades because, while their abundance and behaviour are usually controlled by apex predators, they can provide high‐quality seed‐dispersal services to plant communities. Thus, the recent rewilding of large carnivores worldwide can trigger cascading effects for plants.
We investigated the top‐down effects of an apex predator (Iberian lynx Lynx pardinus) on seed‐dispersal services mediated by two mesocarnivore species (red fox Vulpes vulpes and stone marten Martes foina) at the plant community level by comparing areas with and without lynx in a Mediterranean mountain range in Southern Spain.
We collected scats of mesocarnivores (n = 1575) to assess frugivory and seed dispersal of 15 plant species over two consecutive fruiting seasons and two habitat types (open and forest). Specifically, we assessed the effect of lynx presence on (i) seed occurrence and fleshy‐fruit biomass per scat, (ii) number of scats containing seeds and (iii) diversity of dispersed seeds.
The quantity and diversity of dispersed seeds drastically decreased under predation risk for both mesocarnivore's species. Seed dispersal by stone martens was negatively affected by the presence of lynx, with a marked reduction in the number of scats with seeds (93%) and the diversity of dispersed seeds (46%). Foxes dispersed 68% fewer seeds in open habitats when coexisting with lynx, probably leading to differential contributions to seed‐dispersal effectiveness among habitats.
Our study reveals a novel trophic cascade from apex predators to plant communities. The behavioural responses of frugivorous mesocarnivores to predation risk and the reduction in the intensity of their faecal deposition pattern are probably related to their lower abundance when co‐occurring with apex predators. While rewilding apex predators is a successful conservation tool, attention should be paid to cascading effects across food webs, particularly where frugivore megafauna is missing and mesocarnivores provide unique services to plants.
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... For example, the length of time from seed consumption until digestive passage or regurgitation (seed retention time [SRT]) varies among species and is an important predictor of dispersal kernel properties [8,25,26]. The size, movement, and habitat preferences of animals have all been shown to contribute to SDE [25,27,28]. Disperser movement, behavior, and seed retention times provide necessary inputs to estimate seed dispersal kernels [29][30][31][32][33][34][35]. ...
The primacy of endozoochory for the maintenance and expansion of many woody plant populations is well known, but seed dispersal is not well understood for most species. This is especially true for rare species, where small population size and low fruit production can limit field- or observation-based experiments. Additionally, the effect of environmental heterogeneity on disperser movement is rarely investigated but has been shown to improve estimates of plant population spatial patterns and dynamics. We used simulation experiments to explore the effects of environmental heterogeneity and disperser movement on Lindera subcoriacea seed dispersal, a rare shrub from the southeastern United States with avian-dispersed seeds. Our experiments incorporated environmental heterogeneity and simulated disperser movement for five bird species, based on either landscape permeability or straight path rules. We anticipated that permeability-based movement would result in greater dispersal distances and seed dispersal effectiveness, which characterizes both quantity and quality. Generally, we did not find differences in seed dispersal between permeability and straight path experiments. However, we did find that permeability-based experiments had greater deposition into suitable habitat during flight (23 vs. 1%). These rare but longer distance depositions may be especially important for plants that are influenced by gap or interpopulation dynamics. We also found consistently greater dispersal into high quality habitats regardless of disperser species in permeability experiments, implying that incorporating species-specific assessments of landscape utilization (occupancy) could influence the effectiveness of seed dispersal. Our study suggests that including environmental heterogeneity in seed dispersal models can provide additional insights not provided by avian parameters (e.g., gut capacity, seed retention time, and flight speed) commonly used to inform dispersal models.
... Variation in disperser assemblage has functional consequences for an individual plant's reproductive success (Calviño-Cancela & Martín-Herrero, 2009). Frugivores differ in their habitat preferences and movement patterns, due to which the outcomes of seed dispersal by different frugivores will vary (González-Castro et al., 2015;Jordano et al., 2007;. It is likely that greater diversity of frugivores visiting fruiting plants may result in greater range of distances over which the seeds are dispersed (Bleher & Böhning-Gaese, 2001), and diversity of habitats and microhabitats where the seeds are dispersed. ...
Various factors may mediate the visitation of frugivores to fruiting plants, which can dictate the quantum of seeds removed (dispersed) away from the parent plant. Past studies have laid emphasis on species‐specific factors and environmental contexts that frugivores may use as cues to make foraging decisions and differentially visit various plant species. However, differences in plant traits (intrinsic factors) and local environmental contexts (extrinsic factors) can influence the diversity and abundance of frugivores that visit individual plants of the same species, resulting in intraspecific variation in seed dispersal. We observed individuals of two co‐fruiting plant species with morphologically similar fruits— Naringi crenulata and Ziziphus oenopolia— for 134 h and examined the influence of fruit crop size, plant height, and fruiting neighborhood on the diversity of visiting avian frugivores and quantum of fruit removal for individual plants. We found that despite their similarity in fruits and sharing of a similar set of frugivore species, the two plant species differed in how they attracted frugivores, with consequences for fruit removal rates. Fruit crop size was an important determinant of fruit removal for N. crenulata ¸ while plant height led to greater visitation and fruit removal for Z. oenopolia . We discuss potential reasons for the difference in frugivore visitation and fruit removal for the two plant species. Our results support a growing body of evidence that intraspecific variation in seed dispersal is pervasive and highly context‐dependent, and describe frugivore interactions of two plant species from an understudied tropical savanna.
... Shorth distance was identified in all species where barochory was the most common dispersal type, while seeds dispersed by birds were considered as longer distance (Nogales et al. 2013). Mean distance was identified for species with wind dispersal seeds, or even with zoochory by lizards, including not only fleshy fruits, but also dry fruits (González-Castro et al. 2015). The same three localities and individuals used to estimate herbivory damage (see above) were also used to evaluate seed productivity. ...
Climate change is modifying plant communities and ecosystems around the world. Alpine ecosystems are of special concern on oceanic islands, due to their characteristic higher endemicity percentage, small area and undergoing severe climate change impact in the last few decades. During recent decades there has been increasing interest in the effects of climate change on biodiversity and a range of methods have been developed to assess species vulnerability. However, some new insights are necessary to obtain useful information for species management on oceanic islands. Here in the alpine area of two oceanic islands (Tenerife and La Palma) we evaluate the drivers that best explain the vulnerability of 63 endemic species along three scenarios, covering recent past to present and two future projections (2041–2060 and 2061–2080). The selected drivers were: loss of potential area, mismatch index between potential and occupied areas in different scenarios, and adaptive capacity constraints. We assess the influence of potential area size and whether the drivers of risk and the vulnerability for common, restricted and rare species are significantly different. Our results indicate that management must be widely distributed over the species, and not only focus on restricted species. Evidence for this was that drivers directly deriving from climate change showed no significant differences in their impact on the rarity groups identified. Vulnerability depends partially on the potential area size, showing a more complex picture where constraints on the adaptive capacity of the species have a strong enough influence to modify the effects of the characteristic drivers of climate change.
... Lizards are important seed dispersers (Valido & Olesen, 2019). In fact, lizards have been shown to be even more effective than birds for dispersing seeds in some plant communities, especially on islands (e.g., Galápagos and Canary Islands) where other seed dispersers have disappeared or experienced significant population declines (González-Castro et al., 2015;Heleno et al., 2013). Lizards are the earliest mutualistic vertebrates with plants since the Paolozoic Era (541-251 million years ago) and play an important role in seed dispersal (Tiffney, 2004;Willson et al., 1996). ...
The Mesopotamian spiny‐tailed lizard, Saara loricata, is one of the largest lizard species in the Middle East. Here, we report on the diet of the lizard and their potential role in seed dispersal in Southwestern Iran. We analyzed lizard fecal pellet groups (n = 124) for their food item composition and seed content. We calculated the relative frequency of occurrence (FO%), relative volume (V%), and importance value (IV%) for each food item. Moreover, the number of seeds of each plant food item was counted. Our findings reveal the first solid evidence of omnivorous behavior in the lizard. In total, 16 plant food items and 14 animal food items were identified. Herbaceous plants (IV = 110.2%) and invertebrates (4.8%) were the most important food groups. The plant food items with the highest FO% were Poaceae (56.4%), Centaurea sp. (43.5%), and Medicago polymorpha (27.4%); and the V% for these items were 53.6%, 30.9%, and 13.1%, respectively. Most of the seeds that were consumed by lizards were from Poaceae (547 seeds; 47.81%) and Fabaceae (285 seeds; 24.91%). We also found that each individual lizard could play an equal role in the seed dispersal of all plant families identified. Previous studies show that plant species density and richness are important features for the burrow site selection of Mesopotamian spiny‐tailed lizard. This study highlights the potential role of lizards in influencing the vegetation communities around their burrows through seed dispersal. The Mesopotamian spiny‐tailed lizard, Saara loricata (Blanford, 1874), is a desert dweller, one of the largest lizard species in the Middle East and occurs in Southwestern Iran and Southeastern Iraq.
... Therefore, the loss of one tree or frugivore species inside a block may have its ecological role substituted by another species in the block. However, our analysis does not account for variation in dispersal effectiveness among frugivores, which would be necessary to understand whether redundancy of species within blocks is actually realistic (Calviño-Cancela & Mart ın-Herrero, 2009;Gonz alez-Castro et al., 2015. By contrast, blocks with few species and therefore low redundancy, or blocks grouping many globally threatened species might require particular conservation attention. ...
Frugivory in tropical forests is a major ecological process as most tree species rely on frugivores to disperse their seeds. However, the underlying mechanisms driving frugivore–plant networks remain understudied. Here, we evaluate the data available on the Afrotropical frugivory network to identify structural properties, as well as assess knowledge gaps.
We assembled a database of frugivory interactions from the literature with > 10 000 links, between 807 tree and 285 frugivore species. We analysed the network structure using a block model that groups species with similar interaction patterns and estimates interaction probabilities among them. We investigated the species traits related to this grouping structure.
This frugivory network was simplified into 14 tree and 14 frugivore blocks. The block structure depended on the sampling effort among species: Large mammals were better‐studied, while smaller frugivores were the least studied. Species traits related to frugivory were strong predictors of the species composition of blocks and interactions among them. Fruits from larger trees were consumed by most frugivores, and large frugivores had higher probabilities to consume larger fruits.
To conclude, this large‐scale frugivory network was mainly structured by species traits involved in frugivory, and as expected by the distribution areas of species, while still being limited by sampling incompleteness.
... 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. ...
... 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. ...
... 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. ...
... 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]. ...
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.
... 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). ...
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.
... 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. ...
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.
... 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. ...
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.
... 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. ...
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.
... 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. ...
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.
... 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. ...
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, behaviour 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 behavioural 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 behaviours.
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 behavioural 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.
... 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. ...
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.
... 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). ...
... 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. ...
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.
... 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). ...
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.
Climate change is forcing species to shift their distribution ranges. Animal seed dispersers might be particularly important in assisting plants tracking suitable climates to higher elevations. However, this role is still poorly understood due to a lack of comprehensive multi‐guild datasets along elevational gradients.
We compiled seed dispersal networks for the five altitudinal vegetation belts of the Tenerife Island (0–3718 m above sea level) to explore how plant and animal species might facilitate the mutual colonisation of uphill habitats under climate change.
The overall network comprised 283 distinct interactions between 73 plant and 27 animal species, with seed dispersers offering viable pathways for plants to colonise upper vegetation belts. A pivotal role is played by a lizard as island‐level hub, while four birds and one introduced mammal (rabbit) are also important connectors between belts. Eleven plant species were empirically found to be actively dispersed to elevations beyond their current known range, with observed vertical dispersal distances largely surpassing those required to escape climate change. Furthermore, over half of the plants arriving at higher elevations were exotic.
Functionally diverse disperser communities are crucial for enabling plants tracking climate change on mountains, but exotic plants might particularly benefit from this upward lift.
The consequences of plant–animal interactions often transcend the mere encounter stage, as those encounters are followed by a chain of subsequent stages on the plant's reproductive cycle that ultimately determine fitness. Yet, the dissemination and recruitment stages of animal‐mediated seed dispersal are seldom analysed jointly, hindering a full understanding of the ecology of seed dispersal.
We analyse the dispersal and recruitment of a fleshy‐fruited plant (Pistacia lentiscus), from fruit production to seedling survival up to their second year. We link early reproductive investment of individual plants to seedling recruitment and explore the role played by seed viability, the coterie of frugivores and microhabitat seed deposition.
The proportion of viable seeds was generally low (mean = 34%) but highly variable among individual plants (range: 0%–95%). Seed viability did not seem to have a direct effect on individual plant's recruitment.
We recorded 28 bird species feeding on P. lentiscus fruits or seeds. Their contribution to plant recruitment was mainly determined by their intensity of fruit consumption and probability to disperse viable seeds. Most frugivores presented non‐random microhabitat preferences, delivering uneven seed contributions to different sites.
Post‐dispersal seed predation by rodents was the most limiting phase in P. lentiscus recruitment. Yet, microhabitats showing the lowest predation rates received the lowest seed rain. Hence, we found a decoupling of the dissemination and recruitment stages: most seeds do not arrive at the most suitable microhabitats.
We estimate P. lentiscus plants need to produce c. 5 × 10⁵ fruits to recruit a single seedling that survives to its second summer in our study site. Its success as a prevalent species in Mediterranean lowland landscapes relies on its high fecundity and thorough fruit removal and dispersal by a diversified frugivore assemblage, which compensates for the high seed unviability characteristic of this genus.
Synthesis: Measuring the delayed, post‐dispersal outcomes of animal frugivory interactions may overturn inferences based on consumption observations only. Seed rain patterns are often decoupled from microhabitats' suitability for seedling recruitment. Hence, more integrative studies that encompass the entire plant reproductive cycle (from fruit production to seedling recruitment) are needed to fully understand frugivores' lasting contribution to plant regeneration in natural populations.
Frugivorous birds are the primary seed dispersers for fleshy-fruited plants through defecation. In general, smallsized species disperse seeds across short distances from parental plants. However, multiple seeds or seeds of different plant species are frequently mixed in the fecal mass, because birds are prone to eat multiple fruits of a few plant species during foraging. This suggests birds deposit seeds as clumps in the field, causing inter- and intraspecific competition. However, the exact number of dispersed seeds for each defecation is very hard to estimate in field. It may also vary according to several variables, such as body size of birds and number of seeds per fruit. To clarify seed deposition patterns, we captured small frugivorous birds and collected the feces and regurgitations. The number of seeds excreted in fecal samples was investigated. From 2003 to 2019, a total number of 21518 seeds from 60 plant species were collected from 2214 birds of 17 species. Average number of seeds included in the fecal sample was 9.7 ± SD 18.4 (range: 1–340). The frequency of the number of excreted seeds was not normally distributed and the mode value was one in all cases and for five main dispersers. In most cases (64.8–74.5%), birds excreted a single seed. Furthermore, the effects of morphological traits of birds and plants on number of excreted seeds were analyzed using GLMM. The body mass of birds had a positive effect on the number of excreted seeds. However, fruit and seed weight exhibited negative effects, suggesting the number of excreted seeds is smaller when smaller birds eat larger fruits bearing larger seeds. The seed deposition pattern based on excretion of a single seed may avoid seed and seedling aggregation at local sites
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 eight 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 world‐wide, 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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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.
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.
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.
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.
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
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.
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 has 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 combination 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 above‐ground biodiversity effect into complementarity and selection effects.
We observed strong positive biodiversity effects on both above‐ground 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.
A free Plain Language Summary can be found within the Supporting Information of this article.
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.
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.
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.
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.
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 life span and senescence patterns, and the roles of viability selection and sexual selection in shaping senescence through trade‐offs and antagonistic pleiotropy.
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.
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.
A free Plain Language Summary can be found within the Supporting Information of this article.
We analyzed 621 lizard fecal pellets to assess the diet of the endemic lizard Gallotia galloti
(Lacertidae) throughout one year in the thermophilous scrubland, the most threatened habitat in the Canary
Islands. Indicating the importance of frugivory, 98.1% of pellets contained seeds from fleshy-fruited plant
species (8,028 seeds in total), and the fruit volume reached 47.5%. The Canarian endemic plants Rhamnus
crenulata and Canarina canariensis were most important in frequency of occurrence and number of seeds
found in pellets, respectively. Lizards were more frugivorous during the summer (63.0% of volume), and
seasonal variation was associated with temporal changes in availability of ripe fleshy fruits. We detected
microspatial differences in the consumption of fruits and plant material. Significant correlations were found
between plant cover of each species and their respective consumption by lizards. Lizards consumed
invertebrates throughout the year; Formicidae, Hemiptera, Coleoptera, and Hymenoptera were the most
frequently consumed prey (76.5% of the animal prey items). Our results indicate that G. galloti is one of the
most frugivorous lacertids studied. The high number of undamaged seeds removed by these lizards also
implies an important role in the seed dispersal processes of many fleshy-fruited plant species from this
threatened habitat.
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.
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.
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.
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.
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.
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.
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
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.
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.
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.
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.
The Canary Islands have become a model region for evolutionary studies. We obtained 1.8 Kbp of mtDNA sequence from all known island forms of the endemic lizard genus Gallotia and from its sister taxon Psammodromus in order to reanalyze phylogenetic relationships within the archipelago, estimate lineage divergence times, and reconstruct the colonization history of this group. Well-supported phylogenies were obtained using maximum parsimony and Bayesian inference. Previous studies have been unable to establish the branching pattern at the base of the tree. We found evidence that G. stehlini (Gran Canaria) originated from the most basal Gallotia node and G. atlantica from the subsequent node. Divergence times were estimated under a global clock using Bayesian Markov Chain Monte Carlo methods implemented by three different programs: BEAST, MCMCTREE, MULTIDIVTIME. Node constraints were derived from subaerial island appearance data and were incorporated into the analyses as soft or hard maximal bounds. Posterior node ages differed slightly between programs, possibly due to different priors on divergence times. The most eastern Canary Islands first emerged just over 20 mya and their colonization appears to have taken place relatively quickly, around 17-20 mya. The subsequent node is consistent with cladogenesis due to colonization of Gran Canaria from the eastern islands about 11-13 mya. The western islands appear to have been colonized by a dispersal event from Lanzarote/Fuerteventura in the east to either La Gomera or one of the ancient edifices that subsequently formed Tenerife in the west, about 9-10 mya. Within the western islands, the most recent node that is ancestral to both the G. intermedia/G. gomerana/G. simonyi and the G.galloti/G. caesaris clades is dated at about 5-6 mya. Subsequent dispersal events between ancient Tenerife islands and La Gomera are dated at around 3 mya in both clades, although the direction of dispersal cannot be determined. Finally, we show that G. galloti is likely to have colonized La Palma more than 0.5 Ma after emergence of the island 1.77 mya, while G. caesaris from the same clade may have colonized El Hierro very soon after it emerged 1.12 mya. There are tentative indications that the large-bodied endangered G. simonyi colonized El Hierro around the same time or even later than the smaller-bodied G. caesaris. This study demonstrates the effectiveness of Bayesian dating of a phylogeny in helping reconstruct the historical pattern of dispersal across an oceanic archipelago.
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.
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.
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.
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.
As the need increases for sound estimates of impending rates of animal and plant species extinction, scientists must have a firm grounding in the qualitative and quantitative methods required to make the best possible predictions. Extinction Rates offers the most wide-ranging and practical introduction to those methods available. With contributions from an international cast of leading experts, the book combines cutting-edge information on recent and past extinction rates with treatments of underlying ecological and evolutionary causes. Throughout, it highlights apparent differences in extinction rates among taxonomic groups and places, aiming to identify unresolved issues and important questions. Written with advanced undergraduate and graduate students in mind, Extinction Rates will also prove invaluable to researchers in ecology, conservation biology, and the earth and environmental sciences.
The chapters of this book on seed dispersal are divided into four parts: (1) frugivores and frugivory (8 chapters); (2) seed and seedling shadows (7 chapters); (3) seed fate and establishment (eight chapters); and (4) management implications and conservation (six chapters). The book presents both recent advances and reviews of current knowledge.
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.
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.
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.
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.
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.
General principles about the consequences of seed dispersal by animals for the structure and dynamics of plant populations and communities remain elusive. This is in part because seed deposition patterns emerge from interactions between frugivore behaviour and the distribution of food resources, both of which can vary over space and time. Here we advocate a frugivore-centred, process-based, synthetic approach to seed dispersal research that integrates seed dispersal ecology and animal movement across multiple spatio-temporal scales. To guide this synthesis, we survey existing literature using paradigms from seed dispersal and animal movement. Specifically, studies are discussed with respect to five criteria: selection of focal organisms (animal or plant); measurement of animal movement; characterization of seed shadow; animal, plant and environmental factors included in the study; and scales of the study. Most studies focused on either frugivores or plants and characterized seed shadows directly by combining gut retention time with animal movement data or indirectly by conducting maternity analysis of seeds. Although organismal traits and environmental factors were often measured, they were seldom used to characterize seed shadows. Multi-scale analyses were rare, with seed shadows mostly characterized at fine spatial scales, over single fruiting seasons, and for individual dispersers. Novel animal- and seed-tracking technologies, remote environmental monitoring tools, and advances in analytical methods can enable effective implementation of a hierarchical mechanistic approach to the study of seed dispersal. This kind of mechanistic approach will provide novel insights regarding the complex interplay between the factors that modulate animal behaviour and subsequently influence seed dispersal patterns across spatial and temporal scales.
Question: In semi-arid systems, rainfall gradients can cause plant-plant interactions to shift from negative to positive or vice versa. However, the importance of a second major abiotic factor, soil nutrients, has rarely been considered. We consider different combinations of both factors and ask: do net adult-seedling interactions become less competitive and more facilitative with increasing overall abiotic harshness?
Location: Succulent Karoo, Western Cape, South Africa.
Methods: We examined the interactions between seedlings and adult shrubs at two sites. Sites differ in rainfall, and each contain two habitats: Nutrient-rich mounds associated with underground termitaria and a relatively nutrient-poor matrix. We carried out a spatial pattern analysis of community-wide seedling-adult associations. We then conducted field and greenhouse experiments to test the effects of soil and the presence of neighbouring shrubs on the growth and survival of six seedling species.
Results: At the higher rainfall site, both competitive and facilitative effects of adults on seedlings were found but did not differ by habitat, despite the more benign conditions in the mound habitat. At the lower rainfall site, adult shrubs generally had neutral effects on seedlings in the matrix habitat. In the nutrient-rich mound habitat, however, adult shrubs had strong and consistently competitive effects on seedlings.
Conclusion: Seedling-adult interactions could not be predicted by a simple overall gradient of abiotic harshness, demonstrating the need for more complex, mechanistic models to predict plant-plant interactions. We suggest that rainfall and soil nutrients affect seedling-adult relations through their interactive effects on the life-history attributes of the species involved.
Few studies link seed dispersal with its demographic consequences, or provide reliable estimates of seed dispersal effectiveness.
One reason is the complexity of measuring the suitability for plant recruitment of seed arrival sites. In this study, I compare
three methods that differ in the effort required to measure site suitability for seedling recruitment. All are based on the
proportion of seeds that become seedlings (seedling-to-seed ratios). Method I is the most detailed and labour intensive. The
fate of seeds was followed throughout the different steps of the recruitment process, from fruit removal until seedling emergence,
including both seeds dispersed by different animals and undispersed seeds. Method II is based on seed addition experiments.
Seeds were sowed in plots, and seedlings emerging were counted in the following two seasons. In Method III, average seed input
during dispersal was measured with soil seed bank samples taken in pre- and post-dispersal periods, and seedling emergence
estimated with samples of three seasons. Method II provided results similar to those of Method I, which, conversely, provides
more insight in the actual processes driving recruitment. Method III, however, systematically underestimated site suitability
(seedling-to-seed ratios) by about 50% as compared to the other methods in all microhabitats studied. Relative instead of
absolute indices of site suitability were, however, reliable with this method. Method II and III are significantly less costly
and could be good alternatives to Method I for some purposes, simplifying future studies on the demographic consequences of
seed dispersal and the effectiveness of dispersers.
KeywordsSeed dispersal–Dispersal quality–Dispersal effectiveness–SDE–Seed additions
Question: Does the influence of plant canopy on seedling establishment interact with climate conditions, and particularly, do intensified drought conditions, enhance a positive effect of the vegetation canopy on seedlings in Mediterranean-type ecosystems.
Location: Mediterranean shrubland near Barcelona, Spain at 210 m a.s.l.
Methods: Over the course of four years we recorded seedling emergence and survival in open areas and below vegetation under control, drier and warmer experimental climatic conditions.
Results: Seedling emergence is more sensitive to climate conditions than later stages of growth. When considering the whole set of species, the total number of established seedlings at the end of the experiment was lower in the drought and warming stands than in control ones, and vegetation canopy increased the number of these seedlings in the drought stands. Drought reduced seedling emergence but not warming, while the interaction between climate treatments and vegetation canopy was not significant. Seedling survival was lower in the warming treatment than in the control. Under drought conditions, vegetation canopy increased seedling emergence of the dominant Globularia alypum. In control stands, vegetation canopy reduced their survival. Vegetation canopy increased the survival of the dominant Erica multiflora in warming stands, and it reduced the survival of G. alypum in drought stands. No significant effects of drought and warming were observed in the seed rain of these two species.
Conclusions: The balance of the facilitation-competition interactions between vegetation canopy and seedling establishment in Mediterranean-type ecosystems determined by water availability, and drought conditions enhance the positive effect of vegetation canopy. This interaction is species-specific and shows important between-year variability.
The spatial distribution of seeds can influence several parameters of the natural regeneration of plant populations. Factors shaping seedfall patterns have been typically explored from the tree perspective (seed shadow) or from the population perspective (seed rain). However, the seed rain is actually composed of multiple seed shadows. In this paper, we use this framework to explore the variables shaping the seedfall pattern of the wild olive tree (Olea europaea var. sylvestris), a fleshy-fruited tree of the Mediterranean scrublands. We monitored the movement patterns of avian seed dispersers and the seedfall around each fruit-bearing O. europaea tree in two contrasting sites, differing in the degree of human management and abundance of scrub cover. None of the seed dispersers moved between microhabitats (different shrub species and open interspaces) as a function of microhabitat relative abundance. All dispersers foraged preferentially at O. europaea; only the smaller species visited open interspaces, and these only sporadically. Avoidance of open sites by frugivores, especially larger species, and their attraction to source trees were the major determinants of the seedfall pattern. Regarding seed size distribution among microhabitats, we found that only small seeds were significantly overrepresented in open interspaces. From the seed shadow perspective, seed density under trees was similar in the: two study sites, but it decreased with distance at a higher rate in the disturbed scrubland. From the seed rain perspective, seed density was significantly different among microhabitats, with open interspaces collecting few, if any, seeds, and places under source trees receiving the highest densities. Results from seed shadow and seed rain analyses were integrated to construct a path model to explore the relative contribution of spatial, microhabitat, and individual tree features to the seedfall pattern. Factors related to microhabitat were identified as having a major role in shaping seedfall pattern. Open interspaces collected few seeds, points under shrub species with sparse foliage collected moderate seed densities, and points under shrubs with dense foliage collected the highest seed densities. The comparison between sites suggests that habitat alteration (a reduction of the scrub layer) can lead to contrasting seedfall patterns. The occurrence of an abundant scrub layer in the well-preserved scrubland allowed a complex pattern of seed rain. In contrast, the sparse scrub cover in the disturbed scrubland yielded a seedfall pattern composed of multiple seed shadows constrained to the vicinity of tree crowns. Thus, our sampling design and analytical approach have proved useful in describing the relative importance of the set of variables that shapes the complex seedfall pattern of a bird-dispersed plant. This seedfall pattern, in turn, is central to the understanding of the spatial patterns of plant recruitment and the efficiency of the dispersal mutualism.
Disperser effectiveness is the number of new plants resulting from the activity of one disperser relative to other dispersers or to nondispersed seeds. Effectiveness remains largely uninvestigated due to the complexity of its measurement. We measured the effectiveness of seed dispersers ( Larus michahellis , Turdus merula , and Oryctolagus cuniculus ) of the shrub Corema album (Empetraceae) using a simulation model of the recruitment process that was parameterized with field data of seed dispersal, predation, and seedling emergence and validated with independent data on seedling density. The model allows tracking the fate of seeds dispersed by each animal and estimating, for the first time, disperser effectiveness as seedlings per square meter contributed by each disperser. It also allows quantifying the relative importance of different recruitment processes in determining the quantity and spatial distribution of recruitment.
Larus michahellis was the most effective disperser in two of the three habitats studied, contributing 3–125 times more than the other two species, whose lower effectiveness depended mostly on deposition patterns ( T. merula ) or deleterious effects on seedling emergence ( O. cuniculus ). The dependence of the plant on each disperser differed between habitats and was the greatest in sparse scrub, where recruitment depended almost exclusively on gulls (90%). Quantity and quality of dispersal were not correlated; quality was a better predictor of disperser effectiveness. Seedling emergence was the most crucial process in determining both the spatial pattern of recruitment among microhabitats (99.8% of variance explained) and the quantity of recruitment within microhabitats (43–83%). A sensitivity analysis showed that increasing seed dispersal improved the recruitment for all dispersers when there was no competition for fruits. However, with limited fruits, increased dispersal of lower quality dispersers reduced overall recruitment.
Our results show important differences in effectiveness among dispersers and illustrate the different influences of the components of effectiveness, which varied depending not only on the disperser but also on the circumstances (e.g., type of habitat).
The mutualistic interactions between plants and the animals that pollinate them or disperse their fruits have molded the organization of Earths's biodiversity. These interactions create networks of interdependence often times involving dozens or hundreds of species. Recent research has used concepts from graph theory to characterize the architecture of these networks. Mutualistic networks are heterogeneous, nested and build upon weak and asymmetric links among species. This network architecture highly affects its robustness to perturbations such as the extinction of a species.
The main drivers of global environmental change (CO2 enrichment, nitrogen deposition, climate, biotic invasions and land use) cause extinctions and alter species distributions, and recent evidence shows that they exert pervasive impacts on various antagonistic and mutualistic interactions among species. In this review, we synthesize data from 688 published studies to show that these drivers often alter competitive interactions among plants and animals, exert multitrophic effects on the decomposer food web, increase intensity of pathogen infection, weaken mutualisms involving plants, and enhance herbivory while having variable effects on predation. A recurrent finding is that there is substantial variability among studies in both the magnitude and direction of effects of any given GEC driver on any given type of biotic interaction. Further, we show that higher order effects among multiple drivers acting simultaneously create challenges in predicting future responses to global environmental change, and that extrapolating these complex impacts across entire networks of species interactions yields unanticipated effects on ecosystems. Finally, we conclude that in order to reliably predict the effects of GEC on community and ecosystem processes, the greatest single challenge will be to determine how biotic and abiotic context alters the direction and magnitude of GEC effects on biotic interactions.
The relative effects of resource availability and partitioning on animal population density are unresolved yet central to ecology and conservation. Species-depauperate islands offer an intriguing test case. Across 643 lizard populations from around the world, local abundances are one order of magnitude higher on islands than on mainlands, even when controlled for resource availability. On mainlands, predator and competitor richness only weakly correlate with lizard densities. On islands, sharp reductions in predator and competitor richness are the dominant drivers of lizard abundance. Our results demonstrate the dramatic effect insularity has on the interplay between biotic and abiotic control of animal abundances and the heightened sensitivity of island communities to species' losses and gains.
- R R Sokal
- F J Rohlf
Sokal R. R., and F. J. Rohlf. 1995. Biometry, 3rd edn. New York: Freeman
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Seed dispersal by birds, effect of vegetation structure and influence on succession in a Mediterranean Region
- M J Debussche
- J Lepart
- Molina
Debussche, M., J. Lepart, and J. Molina. 1985. Seed dispersal by birds, effect of vegetation
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structure and influence on succession in a Mediterranean Region. Acta Oecologica-487
Elsa Bonnaud and Concepción Nieves, who 451 helped at different stages of the study Javier Rodríguez-Pérez, Alfredo Valido, the handling 452 editor and four anonymous referees made useful comments to a previous version of the 453 manuscript
- Benito Pérez
- Yurena Gavilán
- Patricia Marrero
Benito Pérez, Yurena Gavilán, Patricia Marrero, Elsa Bonnaud and Concepción Nieves, who
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helped at different stages of the study. Javier Rodríguez-Pérez, Alfredo Valido, the handling
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editor and four anonymous referees made useful comments to a previous version of the
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manuscript. A.G.-C. benefited from a JAE-PRE fellowship from the Spanish National Research
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This work was financed by the Spanish Ministry of Science and Education project 456 (CGL2007-61165/BOS), supported by FEDER funds from the European Union
- Galicia
Galicia). This work was financed by the Spanish Ministry of Science and Education project
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(CGL2007-61165/BOS), supported by FEDER funds from the European Union. The Cabildo of
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-C. was supported by an Isidro Parga Pondal contract
- M C Council
Council (CSIC), and M.C.-C. was supported by an Isidro Parga Pondal contract (Xunta de
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Seeds: the ecology 509 of regeneration in plant communities
- P Jordano
Jordano, P. 2000. Fruits and frugivores. Pages 125-165 in M. Fenner, editor. Seeds: the ecology
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of regeneration in plant communities, 2nd edn. CAB International, Oxford, UK.
who 451 helped at different stages of the study. Javier Rodríguez-Pérez, Alfredo Valido, the handling 452 editor and four anonymous referees made useful comments to a previous version of the 453 manuscript
- Benito Pérez
- Yurena Gavilán
- Patricia Marrero
- Elsa Bonnaud
- Concepción Nieves
Benito Pérez, Yurena Gavilán, Patricia Marrero, Elsa Bonnaud and Concepción Nieves, who
451
helped at different stages of the study. Javier Rodríguez-Pérez, Alfredo Valido, the handling
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editor and four anonymous referees made useful comments to a previous version of the
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manuscript. A.G.-C. benefited from a JAE-PRE fellowship from the Spanish National Research
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Los Bosques Termófilos de Canarias
- F Morici
- C Barone
F., Morici, C. & Barone, R. (2008) Los Bosques Termófilos de Canarias. Proyecto
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