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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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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Looking for variable molecular markers in the chestnut gall wasp Dryocosmus kuriphilus: First comparison across genes

Bonal R., Vargas-Osuna E., Mena J.D., Aparicio J.M., Santoro M., Martín A. (2018) Looking for variable molecular markers in the chestnut gall wasp Dryocosmus kuriphilus: First comparison across genes. Scientific Reports. 8: 0-0.
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Doi: 10.1038/s41598-018-23754-z

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The quick spread of the chestnut gall wasp Dryocosmus kuriphilus in Europe constitutes an outstanding example of recent human-aided biological invasion with dramatic economic losses. We screened for the first time a set of five nuclear and mitochondrial genes from D. kuriphilus collected in the Iberian Peninsula, and compared the sequences with those available from the native and invasive range of the species. We found no genetic variability in Iberia in none of the five genes, moreover, the three genes compared with other European samples showed no variability either. We recorded four cytochrome b haplotypes in Europe; one was genuine mitochondrial DNA and the rest nuclear copies of mitDNA (numts), what stresses the need of careful in silico analyses. The numts formed a separate cluster in the gene tree and at least two of them might be orthologous, what suggests that the invasion might have started with more than one individual. Our results point at a low initial population size in Europe followed by a quick population growth. Future studies assessing the expansion of this pest should include a large number of sampling sites and use powerful nuclear markers (e. g. Single Nucleotide Polymorphisms) to detect genetic variability. © 2018 The Author(s).

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Seed loss before seed predation: experimental evidence of the negative effects of leaf feeding insects on acorn production

Canelo T., GaytÁn Á., GonzÁlez-Bornay G., Bonal R. (2018) Seed loss before seed predation: experimental evidence of the negative effects of leaf feeding insects on acorn production. Integrative Zoology. 13: 238-250.
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Doi: 10.1111/1749-4877.12292

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Insect herbivory decreases plant fitness by constraining plant growth, survival and reproductive output. Most studies on the effects of herbivory in trees rely on correlational inter-individual comparisons and could, thus, be affected by confounding factors linked to both herbivory and plant performance. Using the Mediterranean Holm oak (Quercus ilex) as a study model, we followed an experimental approach in which leaf-feeding insects (mainly Lepidoptera caterpillars) were excluded from some shoots in all study trees. Shoots subjected to herbivore exclusion exhibited lower defoliation rates and produced more acorns than control shoots. Defoliation constrained shoot growth throughout the study period, but had no effect on the number of female flowers produced per shoot. Acorn production was, however, lower in control shoots due to their higher abortion rates, and also to their greater mortality risk during summer drought, as shoots with fewer leaves were less likely to survive. Plant reaction to herbivory inhibits certain physiological pathways involved in plant growth, which, together with the effects of physical damage, reduces the amount and efficiency of the photosynthetic tissue. This increases their vulnerability to environmental stresses, such as water deficit, which limit resource assimilation. Defoliation is likely a key factor affecting oak regeneration, as it may be a significant source of seed loss prior to pre-dispersal acorn predation. Further experimental studies could help to elucidate its effects in contrasting environments. In Mediterranean regions, the harsher droughts predicted by climate change models could worsen the effects of insect herbivory on oak reproductive output. © 2017 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd

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Araneus bonali sp. N., a novel lichen-patterned species found on oak trunks (Araneae, Araneidae)

Morano E., Bonal R. (2018) Araneus bonali sp. N., a novel lichen-patterned species found on oak trunks (Araneae, Araneidae). ZooKeys. 2018: 119-145.
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Doi: 10.3897/zookeys.779.26944

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The new species Araneus bonali Morano, sp. n. (Araneae, Araneidae) collected in central and western Spain is described and illustrated. Its novel status is confirmed after a thorough revision of the literature and museum material from the Mediterranean Basin. The taxonomy of Araneus is complicated, but both morphological and molecular data supported the genus membership of Araneus bonali Morano, sp. n. Additionally, the species uniqueness was confirmed by sequencing the barcode gene cytochrome oxidase I from the new species and comparing it with the barcodes available for species of Araneus. A molecular phylogeny, based on nuclear and mitochondrial genes, retrieved a clade with a moderate support that grouped Araneus diadematus Clerck, 1757 with another eleven species, but neither included Araneus bonali sp. n. nor Araneus angulatus Clerck, 1757, although definitive conclusions about the relationships among Araneus species need more markers examined and a broader taxonomic coverage. The new species was collected on isolated holm oaks and forest patches within agricultural landscapes. Adults were mostly trapped on tree trunks, where their lichen-like colours favour mimicry, while juveniles were collected on tree branches. Specimens were never found either in ground traps or grass samples. This species overwinters as egg, juveniles appear in early spring, but reproduction does not take place until late summer-early autumn. Araneus bonali Morano, sp. n. was found in the same locality from where another new spider species was described. Nature management policies should thus preserve isolated trees as key refuges for forest arthropods in agricultural landscapes, as they may be hosting more unnoticed new species. After including Araneus bonali Morano, sp. n. and removing doubtful records and synonymies, the list of Araneus species in the Iberian Peninsula numbers eight. © Eduardo Morano, Raul Bonal.

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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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Cheiracanthium ilicis sp. n. (Araneae, Eutichuridae), a novel spider species associated with Holm Oaks (Quercus ilex)

Morano E., Bonal R. (2016) Cheiracanthium ilicis sp. n. (Araneae, Eutichuridae), a novel spider species associated with Holm Oaks (Quercus ilex). ZooKeys. 2016: 21-39.
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Doi: 10.3897/zookeys.601.8241

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We describe a novel species Cheiracanthium ilicis sp. n. (Araneae, Eutichuridae) collected in the province of Toledo (Central Spain). It was found during a systematic sampling campaign carried out in an agricultural landscape with isolated Holm oaks Quercus ilex and small forest patches. Its morphology and affinities with other species of the genus are discussed. Furthermore, one mitochondrial gene was sequenced to confirm species membership and its differentiation from other Cheiracanthium species. The molecular phylogenies based on mitochondrial and nuclear genes showed a close relationship of C. ilicis sp. n. with C. inclusum and C. mildei, with which it also shares morphological similarities. Nonetheless, the sparse sampling of the phylogeny, due to the low number of sequences available, impedes drawing any definitive conclusion about these relationships; it is first necessary to perform an extensive review of the genus worldwide and more thorough phylogenies. C. ilicis sp. n. also shares certain ecological and phenological characteristics with C. inclusum and C. mildei. Like them, C. ilicis sp. n. is an obligate tree dweller that prefers a tree canopy habitat and reproduces primarily in late spring and summer. From a conservation perspective, the present study suggests the need to preserve isolated trees in agricultural landscapes. They are not only the refuge of common forest organisms but also of novel species yet to be discovered. © Eduardo Morano, Raul Bonal.

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