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Recruitment of a Mast-Fruiting, Bird-Dispersed Tree: Bridging Frugivore Activity and Seedling Establishment
Ecological Monographs
Abstract
The recruitment of Phillyrea latifolia L. (Oleaceae), a bird-dispersed tree of Mediterranean forest, is described. Fruit removal by birds, seed rain, post-dispersal seed predation, seed germination, and seedling emergence, survival, and establishment were studied. The main objective was testing whether seed dispersal by birds produced a pre- dictable seedling shadow as a result of coupled patterns of seed rain, seedling emergence, and seedling establishment. P. latlfolia is a mast-fruiting species and large fruit crops were produced in only 2 (1 98 1 and 1989) out of 15 yr (1 978-1 992). We report here on the 1989 fruiting event at one scrubland and one forest site. Ripe fruits were available from mid-September to early June. Extensive removal by birds started after fruit crops of other species were depleted. Seed dispersers were more abundant, and fruit predators more scarce, in scrubland than in forest. P. latifolia fruits were a major component in the diet of principal seed dispersers (Sylvia atricapilla and Erithacus rubecula) that depended almost exclusively on them for food late in the season. Fruit removal levels were higher, crops were depleted earlier, and individual plants dis- persed more seeds in scrubland than in forest. Crop size was the best predictor of number of seeds dispersed by individual plants in scrubland, while fruit characteristics were more influential in forest. Seed dispersal was largely a within-population phenomenon, as no seed fall occurred in traps set beyond the distributional limits of P. latifolia in the study region. Frugivores produced a spatially predictable seed rain at the two sites. Seed rain was greatest beneath fleshy fruit-producing species (under female individuals in dioecious species) in scrubland and at forest-gap interfaces in forest. Post-dispersal seed predation was low at the two sites (39 and 54% after 1-yr exposure). In forest, seed survival was lower in gaps than in forest interior or forest edges. In scrubland, seed survival differed widely among microhabitats (defined by overlying plant species), ranging from 19% (open ground) to 6 1% (beneath Rosmarinus oficinalis). In forest, density of emerging seedlings was unrelated to location in the habitat mosaic (gap, forest edge, interior). Seedling density did differ among microhabitats in scrubland, where emergence was greatest under fleshy fruit-producing species. Seedling survival was higher in forest than in scrubland, where seedlings incurred greater mortality due to desiccation. In both sites, seedling survival depended significantly on microhabitat and was depressed under adult conspecifics. The activity of frugivores directly impacted seedling distribution in scrubland, as spatial patterns of seed deposition were not overshadowed by later-acting factors, such as rodent seed predation or variation in germination. In forest, there was spatial discordance between seed rain and seedling distribution, as a consequence of uncoupled seed rain and seedling emergence. Spatial patterns of seed deposition by birds may thus have a lasting impact on the population dynamics of P. latlfolia, but this will vary among populations depending on the extent of coupling of the different stages in the recruitment process (dispersal-seed rain-germination and seedling establishment).
... The net outcome of these opposing interactions on plant reproductive performance will depend on multiple factors such as plant reproductive investment, plant traits, the strength of antagonistic and mutualistic interactions, and the potential direct or indirect effects among interacting animal species [9][10][11][12][13]. Ultimately, plant-animal interactions could determine seed output, seedling recruitment, and plant population dynamics [3,[14][15][16] and can have important consequences for selection on plant reproductive traits [10,[17][18][19]. ...
... We observed temporal variation in seed dispersal within the same population, increasing during a year of large seed production, although the amount of frugivory did not differ from the other year with lower cone production. This suggests a potential satiation effect on local avian dispersers [9,15,79]. However, we quantified seed dispersal by birds during late autumn or early winter, which could have somewhat underestimated the cumulative cone removal by migratory thrushes. ...
... As in other woody perennials, junipers produce irregular and synchronous cone crops as an evolutionary mechanism to reduce seed predation by specialized predispersal seed predators through a satiation effect during large crops [9,55]. However, high supra-annual variations in cone production by junipers also leads to the satiation of local avian dispersers [9,15,73,79]. Despite the disadvantage of satiating bird frugivores, juniper species tend to favor the avoidance of specific seed predators [9,52]. ...
Simple Summary
Plants interact with various animals during reproduction, which influences their success and evolution. Predispersal seed predators reduce fruit crop, potentially decreasing seed dispersal success through a reduction in the quantity and quality of fruits available for dispersers. We explored this phenomenon in a gymnosperm producing fleshy cones, Spanish juniper (Juniperus thurifera). Spanish juniper cones are damaged by three predispersal arthropod taxa and dispersed by birds. We assessed how these interactions change over time and across different locations. Cone production was the main factor affecting predispersal seed predation. High crops reduced relative seed predation rates due to a satiation effect, although seed dispersal did not increase significantly. Cone crop size had a strong effect on the relative abundance of each arthropod species, with higher competition among arthropods in years with low cone production. Crop size and cone traits at individual trees influenced which seed predators were attracted and the foraging activity of birds. Competition among arthropods increased during years with fewer cones, and seed predators sometimes deterred birds from eating the cones. Overall, large year to year fluctuations in cone production appear to favor Spanish juniper by reducing the impact of seed predators.
Abstract
Plants interact with both antagonistic and mutualistic animals during reproduction, with the outcomes of these interactions significantly influencing plant reproductive success, population dynamics, and the evolution of plant traits. Here, we investigated the spatial and temporal variations in the interactions between Juniperus thurifera, its seed-dispersing birds, and three specific arthropod species that attack the fleshy cones during the predispersal period. We assessed how plant traits affect levels of cone damage by arthropods and seed dispersal by birds, the occurrence of competition among arthropod species, and the impact of seed predators on the activity of frugivores. Plant traits, cone damage by arthropods, and seed dispersal by birds showed spatiotemporal variability. Fluctuation in cone abundance was the leading factor determining damage by arthropods and bird dispersal with a secondary role of cone traits. Large crops satiated predispersal seed predators, although the amount of frugivory did not increase significantly, suggesting a potential satiation of bird dispersers. Crop size and cone traits at individual trees determined preferences by seed predator species and the foraging activity of bird dispersers. Competition among arthropods increased during years of low cone production, and seed predators sometimes negatively affected bird frugivory. High supra-annual variations in cone production appear to be a key evolutionary mechanism enhancing J. thurifera reproductive success. This strategy reduces the impact of specialized seed predators during years of high seed production, despite the potential drawback of satiating seed dispersers.
... Hence, seed dispersal represents the 'demographic bridge' between adults and recruits, shaping the initial spatial template where plant establishment takes place (Herrera et al., 1994;Nathan & Muller-Landau, 2000). After dispersal, establishment involves sequential life stages (dispersed seed, seedling, sapling and adult) connected by a series of demographic processes, namely post-dispersal seed survival, seed germination, seedling survival and sapling survival (Wang & Smith, 2002). ...
... After dispersal, establishment involves sequential life stages (dispersed seed, seedling, sapling and adult) connected by a series of demographic processes, namely post-dispersal seed survival, seed germination, seedling survival and sapling survival (Wang & Smith, 2002). These demographic processes can be quantified in the field (in situ) as the probabilities that an individual (seed, seedling or sapling) transitions from one stage to the next of its life cycle, thereby, they are known as transition probabilities (Figure 1) (Herrera et al., 1994). At the population level, the transition probability can be interpreted as the proportion of individuals that successfully move to the following stage. ...
... The establishment of woody plants in the Mediterranean has been extensively studied over the last three decades (Fedriani & Delibes, 2011;Herrera et al., 1994;Traveset et al., 2003). However, this information is non-standardized and scattered on the literature, which hinders access and precludes an overview of potential knowledge gaps, such as those resulting from taxonomic, geographic and demographic research biases. ...
Motivation
Plant establishment is the result of sequential demographic processes, namely post‐dispersal seed survival, seed germination, seedling survival and sapling survival. These processes can be quantified as transition probabilities between life stages through field experiments, and their product provides an overall establishment probability. This information is essential to understand demography within populations and plant colonization potential under global change scenarios. The Mediterranean Region constitutes a biodiversity hotspot characterised by severe summer droughts, which suppose a critical demographic bottleneck for perennial plant establishment. Despite many studies have quantified transition probabilities of woody species in this region, information is scattered through the literature and has not yet been compiled. To fill this gap, we collated data from a systematic literature review and completed them with new unpublished data to create the EstablishMed dataset.
Main types of variables contained
EstablishMed is a compilation of 4728 records of transition probabilities that quantify demographic processes operating during plant establishment. All records belong to native species and were obtained in situ under field conditions. Each record includes information about the specific spatiotemporal context of the study (i.e., year, site, population, habitat and microhabitat) and the experimental procedures employed (e.g., degree of protection against natural enemies). In addition, we included taxonomic and trait information of the study species (i.e., seed mass, dispersal syndrome and life form), and the bioclimate of the study sites.
Spatial location and grain
The dataset covers the whole Mediterranean Region. The finest spatial resolution corresponds to microhabitat types within populations.
Time period and grain
Data were extracted from 271 studies originated between 1991 and 2024.
Major taxa and level of measurement
134 woody species from 80 genera and 39 families.
Software format
EstablishMed is available in .csv format in Dryad repository.
... Thus, the impact of frugivores on plant recruitment is not solely determined by the quantity of seeds 24│| General Introduction they disperse, but also by the long-term consequences of their dispersal. Pre-and post-dispersal processes of plants are often studied in isolation and few studies have successfully managed to connect frugivore consumption with seedling recruitment as this requires abundant data gathering (e.g., Herrera et al. 1994, Jordano & Herrera 1995, Schupp 1995, Jordano & Schupp 2000, Rey & Alcántara 2000, Côrtes et al. 2009, Rother et al. 2013, Donoso et al. 2016. Treating jointly dissemination and establishment processes can enhance our understanding of the role of frugivores along demographic transitions from fruit production to seedling establishment, and can become useful to predict the consequences of environmental changes and animal fluctuations for plant regeneration. ...
... Our results are consistent with previous reports showing that extremely high seed production and consumption are required to ensure recruitment, given sharp decreases in survival probability as seeds move along dissemination and establishment stages (Herrera et al. 1994, García-Fayos & Verdú 1998, Gómez-Aparicio 2008. ...
... Integrative studies that connect frugivore consumption with seedling recruitment are much less frequent (e.g., Herrera et al. 1994, Jordano & Herrera 1995, Schupp & Fuentes 1995, Jordano & Schupp 2000, Rey & Alcántara 2000, Côrtes et al. 2009, Donoso et al. 2016). Here we managed to estimate the recruitment success of individual plants from seed production to seedling survival, assessing the delayed consequences of pre-dispersal (e.g., seed viability, frugivore predation) and post-dispersal stages (frugivore-mediated seed rain, microhabitat-associated rates of seed predation or seedling survival) on plant overall recruitment success. ...
Studying interactions among species and their multiple forms and outcomes has become a central question of ecological research. Mutualisms have changed the way ecologists understand the functioning of ecosystems. Generalised mutualistic networks, especially among free-living species, have been observed to include highly heterogeneous assemblages, in which most species establish few interactions while a minority of species establish a wide range of interactions. These highly connected species are referred to as super-generalists. They are characterised for connecting otherwise isolated groups of interacting species or modules and for providing stronger cohesion to ecological networks. Their characteristics make them fundamental for local biodiversity and the structure and stability of interactions. In this PhD thesis we aim to better comprehend the super-generalist strategy and the mutualistic interactions at the individual level. For this purpose, we use as a model organism Pistacia lentiscus L. (Anacardiaceae), a woody shrub species abundant in the Mediterranean Basin, together with the coterie of frugivorous birds that consume its fruits and disperse its seeds. In Chapter 1 we review sampling methods used to record frugivory interactions, assessing their strengths, caveats, and convenience in different contexts. We highlight the significant advancements brought by emerging methods like camera traps and molecular tools, which allow recording interactions across large spatiotemporal scales and even tracking the movement of individual seeds by animals. We also show how data integration improves network completeness and representativity, and compare different data merging approaches for adjacency matrices. In Chapter 2, we explore the effectiveness of the frugivory/seed-dispersal mutualism between individual plants of P. lentiscus and its avian frugivore assemblage, assessing the level of reciprocity in reward exchange and dependence asymmetry among partners. We document how effectiveness of the the mutualistic service is mainly determined by fruit consumption frequency (the component with highest variation), leading to highly reciprocal exchange of services but still highly asymmetric dependence among partners. In Chapter 3 we investigate the delayed outcomes of animals’ fruit consumption in early seedling recruitment of P. lentiscus plants. Despite being mostly determined by the number of fruits consumed, the dispersal service provided by birds is decoupled from microhabitat suitability: frugivores deposit a smaller number of seeds in the most suitable microhabitats. These results underscore the role of different frugivores in spatial recruitment of heterogeneous landscapes. Lastly, in Chapter 4 we analyse individual-based networks of different plant species and regions of the world, we compare their topology and structure with that of species-based networks, and explore the specialisation and interaction profile of individual plants within populations. We demonstrate that the structure of individual based networks is very similar to that of species-based networks. Plant individuals presented similar interaction profiles irrespective of the species or regions their population belonged to. Within populations, plants present low to medium levels of specialisation, and few frugivore species contribute most interactions in all studied networks. Overall, these results suggest that super-generalist species may evolve when they combine sets of traits that make them accessible and attractive to a diversified assemblage of frugivores. Numerical effects, such as abundant fruit crops, facilitate plenty of frugivory interactions, characterised in most cases by high reciprocity. In exchange for a fair nutritious reward, plants secure their recruitment thanks to a vast amount of seeds dispersed. Finally, our results indicate that the variation encountered in the way plant individuals structure their interactions is highly consistent across populations of generalised mutualisms worldwide. Collectively, the four chapters in this thesis contribute to better understanding the origin and maintenance of super-generalist species within complex ecological networks, by focusing on the biological scale at which interactions actually occur in nature, that is, the individual scale.
... Un primer paso para entender la importancia de la escala espacial en las interacciones planta-animal es considerar dichas interacciones como filtros demográficos que actúan de forma secuencial a lo largo del ciclo de regeneración de la planta (Herrera et al., 1994;Rey y Alcántara, 2000;García, 2001). Las interacciones con animales determinan distintas probabilidades de transición (entendidas como probabilidad de supervivencia o mortalidad) entre fases consecutivas del ciclo de vida, que se inicia con la etapa de óvulo en la planta madre y acaba con la de adulto reproductor (Figura 7.1). ...
... Cada una de las probabilidades de transición determinadas por las interacciones planta-animal, como ocurre con las determinadas por factores abióticos (e.g., la probabilidad de supervivencia de las plántulas frente a la sequía) varían en el espacio de forma particular. Por ejemplo, en muchos sistemas forestales o arbustivos mediterráneos, la probabilidad de sobrevivir a los depredadores postdispersivos suele ser menor bajo la cobertura de arbustos, mientras que la supervivencia de las plántulas frente a los herbívoros ramoneadores y la sequía es mayor en estos puntos (Herrera et al., 1994;Schupp, 1995;Rey y Alcántara, 2000;Rey et al., 2002). Cuando, como en el anterior ejemplo, las distintas probabilidades de transición muestran patrones espaciales diferentes o incluso contrarios, hablamos de que existe desacoplamiento espacial (Schupp y Fuentes, 1995;Jordano y Herrera, 1995) a lo largo del ciclo de regeneración. ...
... The material in the collectors were retrieved monthly, following the methodology of Herrera et al. (1994); Grambone-Guaratini and Rodrigues (2002) The collected material was stored in plastic bags, labeled with collector and plot numbers and then taken to the Silviculture, Forest Management and Forest Technology Lab at the Federal University of Rondônia, where viable seeds were sorted, separated, quantified, and identified according to bibliographies (Lorenzi 2002;CRIA 2005) at the lowest possible taxonomic level. The common names of the identified species were given with the aid of a local parataxonomist, and the scientific names were determined with specific literature. ...
The aim of the study was to assess seed rain in a stretch of conserved forest, addressing seasonality and the potential of seed production for natural forest regeneration. Thirty five 1m2 collectors were randomly distributed between seven 50x50m plots. Material was collected monthly for a period of one year. Data analysis was carried out using species richness, density, frequency, period of production and type of seed dispersal. A total of 2,391 seeds (corresponding to 68 seeds.m-2) were sampled from 50 different species. 19 were classified as morphospecies and the remaining 31 were distributed in 18 families, 25 genera and 17 species. The family with the highest number of seeds was Annonaceae (15.65 seeds.m-2). The species with the highest seed densities were Bocageopsis multiflora (12.97 seeds.m-2) and Ilex affinis (10.49 seeds.m-2). In relation to frequency, Bocageopsis multiflora occurred in 97.1% of the points, followed by the Morphospecies 19 with 68.5%. The dry season (May to October) showed higher seed production at 47.4 seeds.m-2, as well as the highest number of species dispersing seeds at 27. Finally, the wind dispersion (anemochory) predominated, characterized by the occurrence of 20 species. Overall, it was observed that the production of seeds in the study area followed a seasonal pattern in response to varying precipitation, with higher seed production and the end of the dry season correlated as a possible species survival strategy.
... Vtáky tvoria jednu z kľúčových zložiek ekosystémov (Sekercioglu 2006), podieľajú sa napríklad na šírení semien (Herrera et al. 1994), či regulácii populácií bezstavovcov (Fowler, Knight & McEwen 1991;Holmes, Schultz & Nothnagle 1979). V tomto kontexte je úbytok hmyzu ako hlavnej zložky potravy v čase hniezdenia insektivorných poľných vtákov častokrát automaticky dávaný ako faktor negatívne ovplyvňujúci populácie týchto druhov (Newton 2004). ...
Populations of insectivorous farmland birds recently underwent dramatic declines. Agricultural intensification is the main cause of these population changes, but involves numerous different mechanisms. Changes in food supply are thought to be one of the key factors. Homogenization of diet supplied to insectivorous chicks reduces their growth rate resulting in their smaller size as adults; decreased abundance of prey affects both survival and fitness of chicks and the overall breeding success. The accessibility of food is one of the most important factors limiting the use of food-rich habitats. However, the impact of all these factors on population trends has been shown in a single species – grey partridge. While the effect of changes in food supply on the breeding success has been confirmed in many other species, there is a lack of information on subsequent links to the survival of fledglings and the major causes of mortality outside the breeding period remain unclear. In general, there is insufficient information on population consequences of the changes in food supply for farmland birds, particularly in Central and Eastern Europe – the region with different characteristics from those we find in regions in which most of the findings were collected. Without this information, it is difficult to assess the specific causes of decline of individual species and then propose measures to eliminate the negative impacts of agriculture.
... salzmannii de la sierra de Cazorla depende más de los agentes abióticos que de los bióticos. Concretamente, la sequía estival aparece como el factor más importante de cuantos determinan el éxito de la regeneración, circunstancia ésta que, por otro lado, es normal en el área mediterránea (Pigott y Pigott, 1993;García et al., 2000a;Herrera et al., 1994;Alcántara et al., 2000). Donde la viabilidad de las masas forestales está muy dificultada por las condiciones climáticas, el efecto adicional de los factores bióticos puede limitar severamente las oportunidades de regeneración (Zackrisson et al., 1995), acrecentando, en nuestro caso, los efectos negativos de la sequía. ...
This paper analyses the influence of different factors in the regeneration process of a natural Salzmann pine (Pinus nigra) forest in the Cazorla mountain range (south-east Spain). The factors analysed were related to stand structure, soil conditions, climate records, shrub competition and, finally, to the presence of seed predators. In particular, the forage pattern of seed predators in relation to the spatial distribution of shrubs was investigated, and, at the same time, whether shrubs do not compete with Salzmann pine seedlings for resources, but facilitate their establishment and growth. Results suggest that pine regeneration is facilitated by the presence of Juniper bushes (Juniperus communis), and that seed predators can not consume the whole harvest of a mast year. Of the other factors considered, only the long summer drought has a definitive influence on the population dynamics of Salzmann pine stands. For this reason, the use of selection felling methods is recommended, in order to maintain soil moisture, as is the maintenance of all the shrub species within the stand, and, finally, to be patient until achieved enough quantity of regeneration.
... Specifically, older forest stands may offer a more hospitable environment for oak seedling establishment, including factors such as increased organic matter, age-dependent changes in the forest understory and soil-microbiota-fungi-tree interactions, thereby promoting natural regeneration processes (Davis et al., 1999;Petritan et al., 2007). The relationship between regeneration and average stand age might also be driven by age-dependent changes in tree fecundity, with older trees being more fecund (Herrera et al., 1994). Interestingly, two recent studies from Central Poland have elucidated external factors' influence on acorn production, particularly for Q. rubra. ...
Oak species worldwide face substantial challenges in natural recruitment, significantly affecting biodiversity and ecosystem services. Oaks are a keystone species in northern temperate zones, influencing ecosystem dynamics. This study analysed oak regeneration patterns from 29 oak stands (Quercus spp.) across southern Sweden up to the species' northern range limit. The study focused on two native species, Q. robur and Q. petraea, and one introduced species, Q. rubra, used in Swedish forestry. We aimed to evaluate whether and how oak regeneration was i) associated with latitude, ii) influenced by ground moisture and nitrogen levels, and iii) correlated with stand age, as well as to iv) compare regeneration rates among the species. Contrary to the hypothesis that oak regeneration should decline towards the range margin, our results did not indicate any latitudinal association. This finding raises the possibility of a future northward range expansion for oaks. We also observed that oak regeneration was positively correlated with stand age, while increasing nitrogen and ground moisture levels were inversely related to regeneration. The positive age-dependent effect on recruitment also indicates that species recruitment dynamics within forests may be modified via age-dependent effects within the tree community, with implications for forestry and conservation management. Notably, the natural regeneration of the introduced Q. rubra indicates its successful adaptation to Swedish climate and forests. This study represents Sweden's first large-scale analysis of oak regeneration across multiple oak species. Future research should prioritise longitudinal monitoring, particularly at the northern range limits, and further investigate the expansion of the potentially invasive Q. rubra.
Most Psittacanthus (Loranthaceae) mistletoes depend on frugivorous birds for seed dispersal, and the behaviour of seed dispersers strongly influences their spatial distribution. However, the timing of seed germination stages remains poorly studied. In this study, ripe fruits from nine Psittacanthus species, inhabiting contrasting habitats and host tree species, were collected for seed germination experiments, in which ripe fruits had their exocarp manually removed, and squashed seeds were placed and glued with their viscin on wooden rectangle sticks and daily monitored for 150 d under common environmental conditions. The germination process from seed attachment involved stages such as drying of the viscin, seed coat breaking, cotyledon expansion, and production of sticky latex-like exudates. Notably, the breakdown of the seed coat and cotyledon number varied among species. Breakdown of the seed coat did not occur in some species at least until the day the experiment ended (P. sonorae and P. auriculatus) and cotyledon number ranged from two to eight, with highest cotyledon count to date recorded for P. schiedeanus. Germination indices differed among species, with P. schiedeanus exhibiting higher values for germination rate and synchrony. A strong phylogenetic signal was found in fruit length, fruit width and cotyledon number. After accounting for phylogeny, cotyledon number was negatively associated with mean germination time and germination uncertainty, and positively associated with mean germination rate and germination speed coefficient. The other germination indices were not significantly associated with fruit or seed morphological traits or altitude. Interspecific variation in cotyledon number, seed coat characteristics, and in the timing and duration of seed germination stages highlights distinct processes, likely influenced by environmental differences. These findings highlight species-specific germination processes, the impact of cotyledon number on germination speed, and the potential evolutionary significance of specific morphological traits among Psittacanthus species.
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