Ramón Perea

Moonlight and shelter cause differential seed selection and removal by rodents

Various environmental factors may influence the foraging behaviour of seed dispersers which could ultimately affect the seed dispersal process. We examined whether moonlight levels and the presence or absence of rodent shelter affect rodent seed removal (rate, handling time and time of removal) and seed selection (size and species) among seven oak species. The presence or absence of safe microhabitats was found to be more important than moonlight levels in the removal of seeds. Bright moonlight caused a different temporal distribution of seed removal throughout the night but only affected the overall removal rates in open microhabitats. Seeds were removed more rapidly in open microhabitat (regardless of the moon phase), decreasing the time allocated to seed discrimination and translocation. Only in open microhabitats did increasing levels of moonlight decrease the time allocated to selection and removal of seeds. As a result, a more precise seed selection was made under shelter, owing to lower levels of predation risk. Rodent ranking preference for species was identical between full/new moon in shelter but not in open microhabitats. For all treatments, species selection by rodents was much stronger than size selection. Nevertheless, heavy seeds, which require more energy and time to be transported, were preferentially removed under shelter, where there is no time restriction to move the seeds. Our findings reveal that seed selection is safety dependent and, therefore, microhabitats in which seeds are located (sheltered versus exposed) and moonlight levels in open areas should be taken into account in rodent food selection studies.

Shrubs facilitating seedling performance in ungulate-dominated systems: biotic versus abiotic mechanisms of plant facilitation

Shrubs are important microsites that facilitate seedling performance in abiotically stressed environments. However, shrub facilitation might work differently in ecosystems with high biotic stress (e.g., ungulate-dominated environments). We wonder whether ungulates through their preferences for different shrubs affect the facilitation process of seedlings, and whether this process remains consistent across different levels of abiotic stress. We study seedling performance (survival and growth) of a Mediterranean oak (Quercus pyrenaica) in three microsites (open, preferred and non-preferred shrubs by ungulates) for two contrasting climatic environments and throughout a complete growing season (increasing abiotic stress). Overall, there was a positive effect of shrubs in seedling survival. We found a microsite effect on seedling growth but this effect differed depending on the abiotic environment, with seedlings growing better in open microsites in the less stressful site. The larger abiotic context (climate) played an important role in determining which microsite is the most favorable for seedling growth but not necessarily for the eventual survival of seedlings. Wild ungulates started to damage seedlings early in the growing season, whereas abiotic stress (desiccation) affected mostly those plants that were not previously attacked by animals, showing the hierarchical effect (earlier and longer effect) of the biotic over the abiotic mortality agents. Non-preferred shrubs worked better as nurse shrubs only under high ungulate pressure. From the abiotic perspective, preferred and non-preferred shrubs did not apparently differ in the facilitation effect. Importantly, we found a greater facilitative effect of shrubs on the survival than on the growth of seedlings.

Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.)

The effect of non-reproductive trees and saplings as a physical barrier to pollen dispersal in wind-pollinated species’ forests has not received enough attention in the literature so far. The neighborhood seedling model was used to fit pollen dispersal models for beech at different stages of gap recolonization and to elucidate the effect of saplings as a physical barrier on pollen dispersal at local scale. Phenological overlap of leaf emergence, and pollen release as well as wind directionality patterns were also examined. As a case study, we used a mixed beech-oak forest that was managed as open woodland until 1974. The ban on entry of cattle has led to the recolonization of empty spaces by seedlings and saplings of beech (Fagus sylvatica L.) and two oak species (Quercuspetraea (Matts.) Liebl. and Q. pyrenaica Willd.) and, at last, to canopy closure. The average pollen dispersal distance for the first plants that regenerated in the gaps was almost twice those found for recently installed seedlings and seeds collected in traps, supporting the hypothesis that the understory may act as a physical barrier to pollen dispersal. Although a substantial part of effective pollination directionality is at random, horizontal winds and vertical anabatic winds may explain some of this directionality. At the time of beech pollen release, leaves of beech and sessile oak are fully developed, enhancing pollen interception by the saplings. Explicit models of pollen dispersal for wind-pollinated trees should incorporate the effect of canopy closure caused by growth of saplings and account for leaf phenology of co-occurring species in the forest.

Empty Seeds Are Not Always Bad: Simultaneous Effect of Seed Emptiness and Masting on Animal Seed Predation

Seed masting and production of empty seeds have often been considered independently as different strategies to reduce seed predation by animals. Here, we integrate both phenomena within the whole assemblage of seed predators (both pre and post-dispersal) and in two contrasting microsites (open vs. sheltered) to improve our understanding of the factors controlling seed predation in a wind-dispersed tree (Ulmus laevis). In years with larger crop sizes more avian seed predators were attracted with an increase in the proportion of full seeds predated on the ground. However, for abundant crops, the presence of empty seeds decreased the proportion of full seeds predated. Empty seeds remained for a very long period in the tree, making location of full seeds more difficult for pre-dispersal predators and expanding the overall seed drop period at a very low cost (in dry biomass and allocation of C, N and P). Parthenocarpy (non-fertilized seeds) was the main cause of seed emptiness whereas seed abortion was produced in low quantity. These aborted seeds fell prematurely and, thus, could not work as deceptive seeds. A proportion of 50% empty seeds significantly reduced ground seed predation by 26%. However, a high rate of parthenocarpy (beyond 50% empty seeds) did not significantly reduce seed predation in comparison to 50% empty seeds. We also found a high variability and unpredictability in the production of empty seeds, both at tree and population level, making predator deception more effective. Open areas were especially important to facilitate seed survival since rodents (the main post-dispersal predators) consumed seeds mostly under shrub cover. In elm trees parthenocarpy is a common event that might work as an adaptive strategy to reduce seed predation. Masting per se did not apparently reduce the overall proportion of seeds predated in this wind-dispersed tree, but kept great numbers of seeds unconsumed.

Disentangling factors controlling fruit and seed removal by rodents in temperate forests

Fleshy fruits fall on to the ground together with cleaned seeds previously ingested by primary dispersers, offering a wide range of fruits and seeds to the ground foragers. Although nutritional properties strongly differ between fruits and seeds, this different seed presentation (cleaned seeds versus seeds within the pulp) has not been addressed in seed removal studies. This study reports on the removal of fruits versus their seeds in five fleshy-fruited species in a temperate forest. We found that rodents removed most of the seeds and partially consumed most of the fruits, preferring seeds to fruits. Rodents bit the fruits to extract the seeds, leaving most of the pulp. We found a preference ranking for the seeds (Sorbus aucuparia . Ilex aquifolium . Sorbus aria . Rosa canina . Crataegus monogyna) but no preferences were found for the fruits, probably due to their similarities in pulp constituents. Seed and fruit choice were affected by chemical and physical properties and not by their size. The presence of alternative and preferred seeds (nuts) delayed the encounter of the fruits and seeds and diminished their removal rates. We found that higher rodent abundance is not necessarily associated with higher removal rates of fleshy fruits. Rodent abundance, fruit size and seed size are minor factors in the removal of fleshy fruits and their seeds. This study underlines that scatter-hoarding rodents are important removers of fleshy fruits and their seeds, producing a differential seed removal depending on the seed presentation (with or without pulp), the nutritional properties of the seeds (but not of the fruits) and the presence of alternative food.

Threatened woody flora as an ecological indicator of large herbivore introductions

Rewilding and translocations of large herbivores for conservation purposes have increased in recent times, with numerous introductions inside and outside their native range. This study aims to analyze the use of threatened plant taxa as a possible ecological indicator of large herbivore introductions. We examined the effects of a threatened large ungulate, the Barbary sheep (Ammotragus lervia), on both endangered and vulnerable woody taxa after its introduction in 1970. Contrary to our hypothesis, the herbivore impact on threatened woody species was higher than that found on widespread woody plants. The results reveal that 35.7% of the threatened species showed the highest possible level of herbivore damage in contrast to 6.5% for the widespread species. Threatened species were preferred over common plants, probably due to their greater palatability. Overall plant cover, including neighboring species, was also an important factor determining browsing damage and, thus, habitats with low ground cover should be particularly considered in conservation plans. Herbivore damage on common taxa should be taken with caution since they could mask unsustainable herbivore densities for threatened woody taxa or protected habitats. The use of threatened woody taxa through the studied ecological indicators (herbivore damage, plant preferences, habitat use and regeneration success) represented a useful tool to assess the sustainability of large herbivores introductions and to establish a priority conservation ranking for threatened plant species. These findings highlight the deleterious effects of overabundant ungulate populations regardless its origin (exotic or native) and the need of monitoring threatened woody taxa to better estimate the suitability and sustainability of large herbivore introductions.

Seed Predation on the Ground or in the Tree? Size-Related Differences in Behavior and Ecology of Granivorous Birds

Abstract. Seed-eating birds may consume seeds in the tree (pre-dispersal predation) as well as on the ground (post-dispersal predation), usually at contrasting microhabitat conditions. We examined the foraging behaviour and contribution to seed predation of a whole assemblage of seed-eating birds (mostly Fringillidae) at both dispersal phases (pre- and post-dispersal) in a wind-dispersed tree, the European White Elm Ulmus laevis. We found that most seed predators were tree-feeding birds that prey upon seeds for longer periods in the tree and spend shorter periods in larger flocks foraging on the ground. We also obtained significant differences in predation speed among the seed predator species. The overall number of seeds consumed by birds, as well as the amount of time spent foraging in the tree, increased with increasing feeding heights. Seed availability increases with height, which seems to be the main reason why birds spend more time foraging on higher branches. Birds strongly differed in their perching coefficient (PC, ration of feeding height to distance from crown edge). Small finches such as Serins Serinus serinus and Goldfinches Carduelis carduelis had a very high value of PC in comparison to large finches such as Greenfinches Carduelis chloris, Chaffinches Fringilla coelebs, and Hawfinches Coccothraustes coccothraustes. In general, finches showed much higher values of PC than non-fringillid species, indicating a greater adaptation to perch and feed on more flexible stems. Birds increased their overall seed predation and the time allocated to foraging on the ground when they were in flocks. Small finches tended to follow larger finches and flock in multispecies groups when foraging on the ground. We suggest that this behaviour increases both feeding efficiency and safety. Further studies should take into account possible differences in behavior of seed-eating birds throughout the dispersal season since it may have important implications for their adaptive behavior to select new niches.

Climate, female traits and population features as drivers of breeding timing in Mediterranean red deer populations.

Understanding the factors that lead to variation in the timing of breeding in widespread species such as red deer (Cervus elaphus) is crucial to predict possible responses of wild populations to different climate scenarios. Here, we sought to further understand the causes of inter-annual variation in the reproduction timing of female deer in Mediterranean environments. An integrative approach was used to identify the relative importance of individual, population and climate traits in the date of conception of free-ranging deer, based on a dataset of 829 hinds culled during 12 years. We found that a population trait, density, was the most important factor explaining the variation in conception dates, with greater densities causing later conception dates. Body mass was the second in importance, with heavier females conceiving earlier than lighter ones. Almost equally important was the spring real bioclimatic index, a measure of plant productivity, causing later conception dates in the least productive springs (drier and hotter). Another climatic component, the end of summer drought, showed that the sooner the autumn arrives (greater rainfalls and cooler temperatures) the earlier the conception dates. Interestingly, age class was found to be a minor factor in determining conception date. Only older females (≥10 years old) conceived significantly later, suggesting reproductive senescence. This study highlights not only the importance of population and individual traits but also the influence of climatic parameters on the deer reproductive cycle in Mediterranean environments, giving valuable insight into how reproductive phenology may respond to seasonality and global climate changes.

Jeffrey Pine Seed Dispersal in the Sierra San Pedro Mártir, Baja California, Mexico

ABSTRACT. The Sierra San Pedro Mártir (SSPM) in northern Baja California, Mexico, is a remote mountain at the southern edge of the California Floristic Province, a vegetation type that includes the Sierra Nevada of California and western Nevada. Unlike most forests in the southwestern United States, the forests of the SSFM have never been logged and have experienced only light grazing in recent years, and wildfires have not been suppressed until recent decades. The SSFM represents one of the best examples of an intact presettlement forest in the California Floristic Province. We investigated the mode of seed dispersal of Jeffrey pine (Pinus jeffreyi) in the SSPM, and compared it to that from the eastern slope of the Sierra Nevada, to determine how this process might differ between nearly pristine and heavily altered forests. We found that seed dispersal appears to occur by the same means in both forests (i.e., scatter hoarding of seeds by rodents), but that seedling establishment is much less successful in the SSPM. We considered several hypotheses for why this difference might exist, including the size of seed crops, fire regimes, climate change, grazing by domestic ungulates, and lack of facilitation by shrubs (i.e., nurse plants), but none of these explanations appears adequate to account for the difference. Instead, we suggest that the slow rate of seedling establishment at the SSPM is due to a greater consumption of seeds cached by California chipmunks (Tamias obscurus), who experience a relatively long period of euthermic winter activity in the warm climate of the SSPM. This greater consumption leaves few seeds to germinate. Future studies should test the relative importance of these alternative causes for low seedling recruitment at the SSPM.