Tolerance to seed predation mediated by seed size increases at lower latitudes in a Mediterranean oak

Bogdziewicz M., Espelta J.M., Bonal R. (2019) Tolerance to seed predation mediated by seed size increases at lower latitudes in a Mediterranean oak. Annals of Botany. 123: 707-714.
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Doi: 10.1093/aob/mcy203

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Background and Aims: The ability of plants to allocate energy to resistance against herbivores changes with abiotic conditions and thus may vary along geographical clines, with important consequences for plant communities. Seed size is a plant trait potentially influencing plant tolerance to endoparasites, and seed size often varies across latitude. Consequently, plant tolerance to endoparasites may change across geographical clines. Methods: The interaction between Quercus ilex (holm oak) and seed-predating Curculio spp. (weevils) was explored along most of the latitudinal range of Q. ilex. This included quantification of variation in seed size, survival likelihood of infested seeds, multi-infestation of acorns and community composition of Curculio weevils in acorns. Key Results: Larger seeds had a higher probability of surviving weevil attack (i.e. embryo not predated). Southern populations of oak produced on average four times larger seeds than those of northern populations. Consequently, the probability of survival of infested acorns decreased with latitude. The community composition of Curculio varied, with large weevils (C. elephas) dominating in southern populations and small weevils (C. glandium) dominating in northern populations. However, damage tolerance was robust against this turnover in predator functional traits. Furthermore, we did not detect any change in multi-infestation of acorns along the geographical gradient. Conclusions: Quercus ilex tolerance to seed predation by Curculio weevils increases toward the southern end of its distribution. Generally, studies on geographical variation in plant defence against enemies largely ignore seed attributes or they focus on seed physical barriers. Thus, this research suggests another dimension in which geographical trends in plant defences should be considered, i.e. geographical variation in tolerance to seed predators mediated by seed size. © 2018 The Author(s).

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The effects of local climate on the correlation between weather and seed production differ in two species with contrasting masting habit

Bogdziewicz M., Szymkowiak J., Fernández-Martínez M., Peñuelas J., Espelta J.M. (2019) The effects of local climate on the correlation between weather and seed production differ in two species with contrasting masting habit. Agricultural and Forest Meteorology. 268: 109-115.
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Doi: 10.1016/j.agrformet.2019.01.016

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Many plant species present inter-annual cycles of seed production (mast seeding), with synchronized high seed production across populations in some years. Weather is believed to be centrally involved in triggering masting. The links between meteorological conditions and seeding are well-recognized for some species, but in others consistent correlates have not been found. We used a spatially extensive data set of fruit production to test the hypothesis that the influence of weather on seed production is conditioned by local climate and that this influence varies between species with different life history traits. We used two model species. European beech (Fagus sylvatica) that is a flowering masting species, i.e. seed production is determined by variable flower production, and sessile oak (Quercus petraea) that is a fruit-maturation masting species, i.e. seed production is determined by variable ripening of more constant flower production. We predicted that climate should strongly modulate the relationship between meteorological cue and fruit production in Q. petraea, while the relationship should be uniform in F. sylvatica. The influence of meteorological cue on reproduction in fruiting masting species should be strongly conditioned by local climate because the strength of environmental constraint that modulates the success of flower-to-fruit transition is likely to vary with local climatic conditions. In accordance, the meteorological cuing was consistent in F. sylvatica. In contrast, in Q. petraea the relationship between spring temperature and seed production varied among sites and was stronger in populations at colder sites. The clear difference in meteorological conditioning of seed production between the two studied species suggests the responses of masting plants to weather can be potentially systematized according to their masting habit: i.e. fruiting or flowering. © 2019 Elsevier B.V.

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Evidence of high individual variability in seed management by scatter-hoarding rodents: does ‘personality’ matter?

Feldman M., Ferrandiz-Rovira M., Espelta J.M., Muñoz A. (2019) Evidence of high individual variability in seed management by scatter-hoarding rodents: does ‘personality’ matter?. Animal Behaviour. 150: 167-174.
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Doi: 10.1016/j.anbehav.2019.02.009

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The predation and dispersal of seeds by scatter-hoarding animals is one of the most studied processes in the context of animal–plant interactions. Seed management by these animals has been traditionally approached at the population level: the patterns documented in the field are assumed to be similar for all individuals of the population and the variability within the population is considered to be random noise. However, little is known about to what extent this variability responds to different and consistent behaviours between individuals. The aim of this study was to analyse the individual variation and consistency in behaviour of scatter-hoarding rodents within a population. As our model we used the wood mouse, Apodemus sylvaticus, a key disperser of holm oak acorns, Quercus ilex, which, in turn, suffers high predation pressure by the common genet, Genetta genetta. In two sets of laboratory experiments, we compared the variance and consistency in behaviours and acorn management due to individual differences with that due to manipulation, using genet scents, of the perceived predation risk. Genet scents reduced the activity (i.e. time out of the refuge) in all wood mice, but the differences and consistency in activity between individuals accounted for most of the variance. Also, mice showed different and consistent stress or relaxed behaviours. Most of the variance in seed management variables, such as dispersal distance and seed size selection, was explained by consistent differences between individuals across scent treatments. The increase in stress behaviours and decrease in relaxed behaviours were positively related to dispersal ability (i.e. longer distances and larger acorns). Our study highlights the importance of considering the individual component of behaviour in scatter-hoarding rodents. This fine-scale level, largely overlooked in the ecological framework, will help to increase our understanding of seed management by scatter-hoarding animals. © 2019 The Association for the Study of Animal Behaviour

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Role of seed size, phenology, oogenesis and host distribution in the specificity and genetic structure of seed weevils (Curculio spp.) in mixed forests

Arias-Leclaire H., Bonal R., GarcÍa-LÓpez D., Espelta J.M. (2018) Role of seed size, phenology, oogenesis and host distribution in the specificity and genetic structure of seed weevils (Curculio spp.) in mixed forests. Integrative Zoology. 13: 267-279.
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Doi: 10.1111/1749-4877.12293

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Synchrony between seed growth and oogenesis is suggested to largely shape trophic breadth of seed-feeding insects and ultimately to contribute to their co-existence by means of resource partitioning or in the time when infestation occurs. Here we investigated: (i) the role of seed phenology and sexual maturation of females in the host specificity of seed-feeding weevils (Curculio spp.) predating in hazel and oak mixed forests; and (ii) the consequences that trophic breadth and host distribution have in the genetic structure of the weevil populations. DNA analyses were used to establish unequivocally host specificity and to determine the population genetic structure. We identified 4 species with different specificity, namely Curculio nucum females matured earlier and infested a unique host (hazelnuts, Corylus avellana) while 3 species (Curculio venosus, Curculio glandium and Curculio elephas) predated upon the acorns of the 2 oaks (Quercus ilex and Quercus pubescens). The high specificity of C. nucum coupled with a more discontinuous distribution of hazel trees resulted in a significant genetic structure among sites. In addition, the presence of an excess of local rare haplotypes indicated that C. nucum populations went through genetic expansion after recent bottlenecks. Conversely, these effects were not observed in the more generalist Curculio glandium predating upon oaks. Ultimately, co-existence of weevil species in this multi-host-parasite system is influenced by both resource and time partitioning. To what extent the restriction in gene flow among C. nucum populations may have negative consequences for their persistence in a time of increasing disturbances (e.g. drought in Mediterranean areas) deserves further research. © 2017 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd

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Invasive oaks escape pre-dispersal insect seed predation and trap enemies in their seeds

Bogdziewicz M., Bonal R., Espelta J.M., Kalemba E.M., Steele M.A., Zwolak R. (2018) Invasive oaks escape pre-dispersal insect seed predation and trap enemies in their seeds. Integrative Zoology. 13: 228-237.
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Doi: 10.1111/1749-4877.12285

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Species introduced to habitats outside their native range often escape control by their natural enemies. Besides competing with native species, an alien species might also affect the native herbivores by introducing a new source of different quality food. Here, we describe the case of northern red oak (Quercus rubra) invasion in Europe. We collected data on insect (moth Cydia spp. and weevil Curculio spp.) seed predation of northern red oak in its native (USA, North America) and invasive (Poland, Europe) range, as well as for sessile oaks (Quercus petrea) in Europe. We also evaluated the quality of acorns as hosts for weevil larvae by collecting infested acorns and measuring weevil developmental success, and quantifying acorn traits such as seed mass, tannins, lipids and protein concentration. We used DNA barcoding to identify insects to the species level. The predation by moths was similar and very low in both species and in both ranges. However, red oaks escape pre-dispersal seed predation by weevils in Europe. Weevil infestation rates of northern red oak acorns in their invasive range were 10 times lower than that of sessile oaks, and also 10 times lower than that of red oaks in North America. Furthermore, even when weevils oviposited into northern red oaks, the larvae failed to develop, suggesting that the exotic host created a trap for the insect. This phenomenon might gradually decrease the local abundance of the seed predator, and further aid the invasion. © 2017 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd

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Effectiveness of predator satiation in masting oaks is negatively affected by conspecific density

Bogdziewicz M., Espelta J.M., Muñoz A., Aparicio J.M., Bonal R. (2018) Effectiveness of predator satiation in masting oaks is negatively affected by conspecific density. Oecologia. 186: 983-993.
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Doi: 10.1007/s00442-018-4069-7

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Variation in seed availability shapes plant communities, and is strongly affected by seed predation. In some plant species, temporal variation in seed production is especially high and synchronized over large areas, which is called ‘mast seeding’. One selective advantage of this phenomenon is predator satiation which posits that masting helps plants escape seed predation through starvation of predators in lean years, and satiation in mast years. However, even though seed predation can be predicted to have a strong spatial component and depend on plant densities, whether the effectiveness of predator satiation in masting plants changes according to the Janzen-Connell effect has been barely investigated. We studied, over an 8-year period, the seed production, the spatiotemporal patters of weevil seed predation, and the abundance of adult weevils in a holm oak (Quercus ilex) population that consists of trees interspersed at patches covering a continuum of conspecific density. Isolated oaks effectively satiate predators, but this is trumped by increasing conspecific plant density. Lack of predator satiation in trees growing in dense patches was caused by re-distribution of insects among plants that likely attenuated them against food shortage in lean years, and changed the type of weevil functional response from type II in isolated trees to type III in trees growing in dense patches. This study provides the first empirical evaluation of the notion that masting and predator satiation should be more important in populations that start to dominate their communities, and is consistent with the observation that masting is less frequent and less intense in diverse forests. © 2018, The Author(s).

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Influence of clay licks on the diversity and structure of an Amazonian forest

Molina E., Espelta J.M., Pino J., Bagaria G., Armenteras D. (2018) Influence of clay licks on the diversity and structure of an Amazonian forest. Biotropica. 50: 740-749.
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Doi: 10.1111/btp.12568

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The spatial heterogeneity of resource availability is a major driver of biodiversity patterns. Some environmental conditions and resources are characterized by large-scale patterns of variation within the landscape. Clumped local discontinuities or discrete elements also increase spatial heterogeneity, promoting local ‘biodiversity hot spots’ by modifying habitat characteristics and promoting plant–animal interactions. Clay licks are faunal attractors owing to their role in the nutritional ecology of the user species; nevertheless, the effect of their presence on the surrounding vegetation has been poorly quantified. Here, we use data from 100 × 10 m transects and evaluate the effects of the presence of clay licks on forest diversity and structure at local and landscape scales. In clay lick areas, there was a higher abundance of certain species, which helps to homogenize species composition between localities counteracting the natural distance-decay of compositional similarity between transects without clay lick influence (controls). Compared to control sites, clay lick′s forests had higher palm densities, shorter but more variable individuals in the canopy and understory, a thinner canopy layer, and denser herbaceous and ground level covers. These differences were found along the whole length of transects in both sampled areas types. These results reveal that the presence of discrete elements (i.e., clay licks) may help to explain the compositional and structural heterogeneity of Amazonian forests influencing ecological processes such as seed dispersal and trampling. These considerations may be relevant for other biomes where clay licks are present and give weight to their inclusion in conservation initiatives in tropical forests. © 2018 The Association for Tropical Biology and Conservation

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Severe wildfire in a mediterranean forest

Molowny-Horas R., Borrego A., Riera P., Espelta J.M. (2018) Severe wildfire in a mediterranean forest. Equivalency Methods for Environmental Liability: Assessing Damage and Compensation Under the European Environmental Liability Directive. : 203-234.
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Doi: 10.1007/978-90-481-9812-2_11

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This case study illustrates the equivalency analysis for estimating ex post environmental damage and appropriate compensatory remediation following a severe wildfire caused by a power line in a forest protected under the European Union Habitats Directive (HD). The study addresses long-term environmental damage (e.g., over several decades) by a large-scale disturbance in a terrestrial ecosystem, and includes an analysis of uncertainty associated with the potential occurrence of natural future fire events in the area. Accounting for the probability of natural future forest fires directly affects both baseline and compensatory remediation options by reducing the habitat area compared to an assumption of no future forest fires. Only natural forest fires, i.e., 10% of all forest fires, have been included in the calculations of both the baseline and the compensatory remediation, since the operator may not be made liable for accidental or provoked forest fires. The impact of this hypothesis is tested by means of a sensitivity analysis. The case study illustrates: • Considerations in selecting a metric from various potential ones (hectares, trees, biomass, habitat quality) for terrestrial habitats included in the HD; • Application of a value equivalency approach (specifically, value-to-value); • Analysis of key variables (e.g., differences in metrics, single/multiple metrics, on-site/off-site implementation); and • Sensitivity of the results to changes in four key model parameters (i.e. area of future forest fires, tree mortality, percentage of natural forest fires and tree minimum diameter at breast height). © Springer Science+Business Media B.V. 2018.

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Zero-sum landscape effects on acorn predation associated with shifts in granivore insect community in new holm oak (Quercus ilex) forests

Ruiz-Carbayo, H., Bonal, R., Pino, J., Espelta, J.M. (2018) Zero-sum landscape effects on acorn predation associated with shifts in granivore insect community in new holm oak (Quercus ilex) forests. Diversity and Distributions. : 0-0.
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Doi: 10.1111/ddi.12701

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Distribution and space use of seed-dispersing rodents in central Pyrenees: implications for genetic diversity, conservation and plant recruitment

Urgoiti J., MuÑoz A., Espelta J.M., Bonal R. (2018) Distribution and space use of seed-dispersing rodents in central Pyrenees: implications for genetic diversity, conservation and plant recruitment. Integrative Zoology. 13: 307-318.
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Doi: 10.1111/1749-4877.12301

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The function and conservation of many forest ecosystems depend on the distribution and diversity of the community of rodents that consume and disperse seeds. The habitat preferences and interactions are especially relevant in alpine systems where such granivorous rodents reach the southernmost limit of their distribution and are especially sensitive to global warming. We analyzed the community of granivorous rodents in the Pyrenees, one of the southernmost mountain ranges of Europe. Rodent species were identified by DNA with particular attention to the Apodemus species, which are prominent seed-dispersing rodents in Europe. We confirmed for the first time the presence of the yellow-necked mouse, Apodemus flavicollis, in central Pyrenees, a typical Eurosiberian species that reaches its southernmost distribution limit in this area. We also found the wood mouse, Apodemus sylvaticus, a related species more tolerant to Mediterranean environments. Both rodents were spatially segregated by altitude. A. sylvaticus was rare at high altitudes, which might cause the genetic differentiation between populations of the different valleys reported here. We also found other seed consumers like dormice, Elyomis quercinus, and voles, Myodes glareolus, with marked habitat preferences. We suggest that population isolation among valleys may increase the genetic diversity of rodents, like A. sylvaticus. We also highlight the potential threat that global warming may represent for species linked to high-altitude refuges at the southern edge of its distribution, like Apodemus flavicollis. Finally, we discuss how this threat may have a dimension in the conservation of alpine forests dispersed by these rodent populations. © 2018 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd

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