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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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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Diversity in insect seed parasite guilds at large geographical scale: The roles of host specificity and spatial distance

Bonal R., Espelta J.M., Muñoz A., Ortego J., Aparicio J.M., Gaddis K., Sork V.L. (2016) Diversity in insect seed parasite guilds at large geographical scale: The roles of host specificity and spatial distance. Journal of Biogeography. : 0-0.
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Doi: 10.1111/jbi.12733

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Aim: Host specificity within plant-feeding insects constitutes a fascinating example of natural selection that promotes inter-specific niche segregation. If specificity is strong, composition of local plant parasitic insect guilds is largely dependent on the presence and prevalence of the preferred hosts. Alternatively, if it is weak or absent, historic and stochastic demographic processes may drive the structuring of insect communities. We assessed whether the species composition of acorn feeding insects (Curculio spp. guilds) and their genetic variation change geographically according to the local host community. Location: An 800 km transect across California, USA. Methods: We used DNA taxonomy to detect potential Curculio cryptic speciation and assessed intra-specific genetic structure among sampling sites. We monitored larval performance on different hosts, by measuring the weight of each larva upon emerging from the acorn. Our phylogenetic and spatial analyses disentangled host specificity and geographical effects on Curculio community composition and genetic structure. Results: DNA taxonomy revealed no specialized cryptic species. Californian Curculio spp. were sister taxa that did not segregate among Quercus species or, at a deeper taxonomic level, between red and white oaks. Curculio species turnover and intra-specific genetic differentiation increased with geographical distance among localities irrespective of local oak species composition. Moreover, larval performance did not differ among oak species or acorn sizes when controlling for the effect of the locality. Main conclusions: Historical processes have contributed to the structuring of acorn weevil communities across California. Trophic niche overlapped among species, indicating that ecologically similar species can co-exist. Acorn crop inter-annual variability and unpredictability in mixed oak forests may have selected against narrow specialization, and facilitated co-existence by means of an inter-specific time partitioning of the resources. Wide-scale geographical records of parasitic insects and their host plants are necessary to understand the processes underlying species diversity. © 2016 John Wiley & Sons Ltd.

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Wood mouse population dynamics: Interplay among seed abundance seasonality, shrub cover and wild boar interference

Sunyer P., Muñoz A., Mazerolle M.J., Bonal R., Espelta J.M. (2016) Wood mouse population dynamics: Interplay among seed abundance seasonality, shrub cover and wild boar interference. Mammalian Biology. 81: 372-379.
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Doi: 10.1016/j.mambio.2016.03.001

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Small rodents play a key role in forest ecosystems as common prey, but also as prevalent seed consumers and dispersers. Hence, there is a great interest in disentangling the factors involved in their population dynamics. We conducted an intensive 2-year field study to test the relative role of seasonality in seed abundance, shrub cover and wild boar interference on the population dynamics of wood mice, Apodemus sylvaticus, in a Mediterranean oak forest. Wood mice demographic parameters varied strongly with the seasonal variations in acorn availability on the ground. Mice survival and abundance dropped drastically during summer, the period of acorn scarcity, but rose again in autumn when acorn-fall began. Specifically, female abundance was associated with the temporal changes in acorn availability on the ground, but were randomly distributed in space whereas males showed a spatially aggregated pattern during the acorn-abundant seasons (autumn-winter). In contrast to studies conducted in sparse oak forests in drier environments, spatial variability in shrub cover and wild boar foraging activity did not affect directly the population dynamics of wood mice. This could be due to the presence of an abundant shrub layer and a closed canopy in our forest that enhance environmental conditions and provides shelter against predators and ungulates. Our study highlights that the relative importance of environmental factors and intraguild competition on rodent dynamics may be highly context-dependent, varying greatly among different sites. We suggest that the relationships between acorn dispersers and oaks are more reciprocal than previously considered. © 2016 Published by Elsevier GmbH.

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Unexpected consequences of a drier world: Evidence that delay in late summer rains biases the population sex ratio of an insect

Bonal R., Hernández M., Espelta J.M., Muñoz A., Aparicio J.M. (2015) Unexpected consequences of a drier world: Evidence that delay in late summer rains biases the population sex ratio of an insect. Royal Society Open Science. 2: 0-0.
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Doi: 10.1098/rsos.150198

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The complexity of animal life histories makes it difficult to predict the consequences of climate change on their populations. In this paper, we show, for the first time, that longer summer drought episodes, such as those predicted for the dry Mediterranean region under climate change, may bias insect population sex ratio. Many Mediterranean organisms, like the weevil Curculio elephas, become active again after summer drought. This insect depends on late summer rainfall to soften the soil and allow adult emergence from their underground refuges. We found that, as in many protandric species, more C. elephas females emerged later in the season. Male emergence timing was on average earlier and also more dependent on the beginning of late summer rainfall. When these rains were delayed, the observed weevil sex ratio was biased towards females. So far, the effects of global warming on animal sex ratios has been reported for temperature-dependent sex determination in reptiles. Our results show that rainfall timing can also bias the sex ratio in an insect, and highlight the need for keeping a phenological perspective to predict the consequences of climate change. We must consider not just the magnitude of the predicted changes in temperature and rainfall but also the effects of their timing. © 2015 The Authors.

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The interplay among acorn abundance and rodent behavior drives the spatial pattern of seedling recruitment in mature Mediterranean oak forests

Sunyer P., Boixadera E., Munoz A., Bonal R., Espelta J.M. (2015) The interplay among acorn abundance and rodent behavior drives the spatial pattern of seedling recruitment in mature Mediterranean oak forests. PLoS ONE. 10: 0-0.
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Doi: 10.1371/journal.pone.0129844

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The patterns of seedling recruitment in animal-dispersed plants result from the interactions among environmental and behavioral variables. However, we know little on the contribution and combined effect of both kinds of variables. We designed a field study to assess the interplay between environment (vegetation structure, seed abundance, rodent abundance) and behavior (seed dispersal and predation by rodents, and rooting by wild boars), and their contribution to the spatial patterns of seedling recruitment in a Mediterranean mixed-oak forest. In a spatially explicit design, we monitored intensively all environmental and behavioral variables in fixed points at a small spatial scale from autumn to spring, as well as seedling emergence and survival. Our results revealed that the spatial patterns of seedling emergence were strongly related to acorn availability on the ground, but not by a facilitationeffect of vegetation cover. Rodents changed seed shadows generated by mother trees by dispersing most seeds from shrubby to open areas, but the spatial patterns of acorn dispersal/predation had no direct effect on recruitment. By contrast, rodents had a strong impact on recruitment as pilferers of cached seeds. Rooting by wild boars also reduced recruitment by reducing seed abundance, but also by changing rodent's behavior towards higher consumption of acorns in situ. Hence, seed abundance and the foraging behavior of scatter-hoarding rodents and wild boars are driving the spatial patterns of seedling recruitment in this mature oak forest, rather than vegetation features. The contribution of vegetation to seedling recruitment (e.g. facilitation by shrubs) may be context dependent, having a little role in closed forests, or being overridden by directed seed dispersal from shrubby to open areas. We warn about the need of using broad approaches that consider the combined action of environment and behavior to improve our knowledge on the dynamics of natural regeneration in forests. © 2015 Sunyer et al.

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Acorn - weevil interactions in a mixed-oak forest: Outcomes for larval growth and plant recruitment

Munoz A., Bonal R., Espelta J.M. (2014) Acorn - weevil interactions in a mixed-oak forest: Outcomes for larval growth and plant recruitment. Forest Ecology and Management. 322: 98-105.
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Doi: 10.1016/j.foreco.2014.02.039

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Weevils are the most important pre-dispersal acorn predators in the Mediterranean region, where oaks often form mixed forests and different weevil species can coexist. The performance of weevil larvae depends in great extent on their feeding activities inside the infested acorns that, in turn, are known to reduce the viability of acorns. In this paper, we have analysed the interactions among the weevil community and four oak species (Quercus pyrenaica, Quercus suber, Quercus faginea and Quercus ilex) coexisting in a Mediterranean mixed-oak forest. DNA sequencing of weevil larvae revealed four different weevil species (Curculio elephas, Curculio glandium, Curculio pellitus and Curculio venosus) infesting the acorns of the four oak species. Oak species differed in acorn size, and weevil species also differed in body size. Weevil species showed some degree of specificity among the four oak species, but specificity was not related to variations in acorn size. By contrast, larval development and seedling recruitment were mostly driven by inter-specific differences in larval and acorn size. Larger seeded species suffered less seed damages by weevils (i.e. embryo predation and cotyledon consumption), thus reducing the impacts of acorn infestation in seedling emergence and seedling size. Larval development for the largest weevil species C. elephas was constrained by cotyledon depletion in all acorn species. Yet, this pattern was not observed for other weevil species. Larval size of the same weevil species also varied among different oak species after controlling for the amount of cotyledon eaten by larvae, thus, variation of other acorn traits among acorn species (e.g. chemical composition) may also have consequences for the performance of weevil larvae. It is likely that other variables operating at population level, such as temporal and spatial changes in acorn production or phenological variations of weevils and oaks, are also implicated in the complex functioning of these outstanding mixed-oak forests where natural regeneration seems to be threatened. © 2014 Elsevier B.V.

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Extensive pollen immigration and no evidence of disrupted mating patterns or reproduction in a highly fragmented holm oak stand

Ortego J., Bonal R., Munoz A., Aparicio J.M. (2014) Extensive pollen immigration and no evidence of disrupted mating patterns or reproduction in a highly fragmented holm oak stand. Journal of Plant Ecology. 7: 384-395.
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Doi: 10.1093/jpe/rtt049

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Aims Forest fragmentation and reduced tree population densities can potentially have negative impacts on mating patterns, offspring genetic diversity and reproductive performance. The aim of the present study is to test these hypotheses comparing an extremely fragmented, low tree density (~0.02 trees/ha) holm oak (Quercus ilex L.) stand from Central Spain with a nearby high tree density stand (~50 trees/ha). Methods We genotyped adult trees and seeds from the low-density stand (436 seeds from 15 families) and the high-density stand (404 seeds from 11 families) using nine microsatellite markers. With these data, we performed paternity analyses, determined pollen flow, mating patterns and pollen pool structure, and estimated progeny genetic diversity in both stands. We also studied seed set and production and performed a pollen supplementation experiment to determine whether reduced tree density has limited foreign pollen availability. Important Findings We have found extensive pollen immigration (>75%) into the low tree density stand and Monte Carlo simulations revealed that pollen moves larger distances than expected from null models of random dispersal. Mating patterns and differentiation of pollen pools were similar in the high-density stand and the low-density stand but we found higher inter-annual differentiation of pollen pools in the former. Progeny genetic diversity and self-fertilization rates did not differ between the low-density stand and the high-density stand. Seed set rates were significantly lower in the low-density stand than in the high-density stand and experimental cross-pollen supplementation evidenced that foreign pollen availability is indeed a limiting factor in the former. However, seed crops did not differ between the low-density stand and the high-density stand, indicating that limitation of foreign pollen is not likely to be of great concern in terms of reduced seed production and potential recruitment. Poor forest regeneration due to other ecological and human factors is probably a more important threat for the persistence of fragmented and low tree density stands than reduced pollen flow and only extremely small and isolated tree populations would be expected to suffer severe loss of genetic diversity in the long term. © 2013 The Author.

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Seeding phenology influences wood mouse seed choices: The overlooked role of timing in the foraging decisions by seed-dispersing rodents

Sunyer P., Espelta J.M., Bonal R., Munoz A. (2014) Seeding phenology influences wood mouse seed choices: The overlooked role of timing in the foraging decisions by seed-dispersing rodents. Behavioral Ecology and Sociobiology. 68: 1205-1213.
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Doi: 10.1007/s00265-014-1731-x

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Scatter-hoarding rodents influence the population dynamics of plants by acting as seed predators and dispersers. Therefore, rodent foraging preferences for certain seed traits (species, size, condition) have been extensively studied. However, to what extent these preferences are fixed or they track the temporal changes on seed characteristics due to phenological differences has been seldom explored. We studied the temporal variability in seed preferences by wood mouse (Apodemus sylvaticus), according to phenological changes in seed characteristics of two co-occurring oaks (Quercus ilex and Quercus pubescens). The phenology of acorn abundance and the acorn predation/dispersal patterns by rodents were monitored over an entire seeding season. Results revealed temporal changes in rodent preferences for acorns of the two oaks, matching their different seeding phenology (earlier in Q. pubescens and later in Q. ilex). On the other hand, whatever the species considered, rodents preferred larger and sound acorns along the entire season, although the dispersal of infested ones increased slightly during the peaks of acorn drop. The observed influence of seeding phenology on seed choices by rodents warns about inferring definite conclusions regarding their foraging behavior when arising from short-term experiments. Indeed, this study reveals that foraging preferences may be highly dynamic and context-dependent for some seed traits (e.g., species and condition), rather than fixed behavioral patterns. Plasticity in rodent foraging choices may allow them to successfully exploit different oaks with uncoupled seeding phenologies, while potentially favoring their coexistence. © 2014 Springer-Verlag Berlin Heidelberg.

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The ecology of seed dispersal by small rodents: A role for predator and conspecific scents

Sunyer P., Muñoz A., Bonal R., Espelta J.M. (2013) The ecology of seed dispersal by small rodents: A role for predator and conspecific scents. Functional Ecology. 27: 1313-1321.
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Doi: 10.1111/1365-2435.12143

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Seed-caching rodents play a key role in the ecology of seed dispersal by not only consuming but also dispersing seeds. Rodent foraging behaviour is usually framed within optimal models, which predict that their decisions should maximize food intake and minimize foraging costs. Although predation risk and seed pilferage by conspecifics have been envisaged as two potential costs, their relevance for seed-caching behaviour and seed dispersal has barely been addressed. To test the effect of predation and pilferage risk on the patterns of seed predation/dispersal by rodents, we performed a field experiment using a tri-trophic-level model (plant-mice-carnivore; Quercus spp-Apodemus sylvaticus-Genetta genetta) and the scents of the predator and conspecifics as direct cues. The behaviour of mice was analysed with video cameras set for continuous recording on consecutive nights, and we used tagged acorns to assess the patterns of acorn predation and dispersal. Our results revealed that rodents were able to discriminate between the scents of genet and conspecifics and modified their seed dispersal behaviour accordingly. Mice spent more time 'sniffing' in rodent cages than in genet cages, where they displayed more 'vigilance and freezing' behaviours. In sites with mice scents, acorns were dispersed at shorter distances and were less predated. Conversely, in sites with genet scents acorn removal was delayed. These results show that chemosensory information on predators and conspecifics influences the foraging decisions of seed-caching rodents over short spatial and temporal scales. This might entail cascading effects on the regeneration of plants. In sites where rodents perceive the risk of predation, inefficient foraging behaviour may result in less successful seed dispersal. Conversely, the detection of conspecific scents may increase dispersal efficiency and seedling recruitment. Ultimately, the relationships between two distant levels in trophic webs (plants-carnivores) appear intricate, since carnivores may affect seed dispersal by changing the foraging behaviour of their prey (the seed disperser). This indirect relationship should be considered as a new dimension of the ecology of seed dispersal by small rodents. © 2013 British Ecological Society.

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