Biological integrity enhances the qualitative effectiveness of conditional mice-oak mutualisms

Scatter-hoarding decisions by rodents are key for the long-term maintenance of scattered tree populations. Decisions are determined by seed value, competition and predation risk, so that they can be influenced by the integrity of the biological system composed by trees, rodents, ungulate competitors, and rodent predators. We manipulate and model the oak-mice interaction in a Spanish dehesa, an anthropogenic savanna system suffering chronic tree regeneration failure, and quantify the joint effect of intrinsic and extrinsic factors on acorn dispersal effectiveness. First, we conducted a large-scale cafeteria field experiment, where we modified ungulate presence and predation risk, and followed mouse scatter-hoarding decisions under contrasting levels of moonlight and acorn availability. Then, we estimated the net effects of competition and risk by means of transition probability models that simulated mouse scatter-hoarding decisions according to the environmental context. Our results show that suboptimal conditions for mice balance the interaction towards the mutualism as they force mice to forage less efficiently. Under stressful conditions (predation risks and presence of ungulates), lack of antipredatory cover around dehesa trees limited transportation of acorns, but also precluded mice activities outside tree canopies. As a result, post-dispersal predation rates were reduced and large acorns had a higher probability to survive. Our work shows that inter-specific interactions preventing efficient foraging by scatter-hoarders benefitted seed dispersal. Therefore, the maintenance of the full set of producers, consumers, dispersers and predators in ecosystems is key for promoting seed dispersal effectiveness in conditional mutualisms.

Mast seeding promotes evolution of scatter-hoarding

Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of ‘shared’ seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech ( Fagus sylvatica ) and yellow-necked mice ( Apodemus flavicollis ). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Great tits who remember more accurately have difficulty forgetting, but variation is not driven by environmental harshness

The causes of individual variation in memory are poorly understood in wild animals. Harsh environments with sparse or rapidly changing food resources are hypothesized to favour more accurate spatial memory to allow animals to return to previously visited patches when current patches are depleted. A potential cost of more accurate spatial memory is proactive interference, where accurate memories block the formation of new memories. This relationship between spatial memory, proactive interference, and harsh environments has only been studied in scatter-hoarding animals. We compare spatial memory accuracy and proactive interference performance of non-scatter hoarding great tits (Parus major) from high and low elevations where harshness increases with elevation. In contrast to studies of scatter-hoarders, we did not find a significant difference between high and low elevation birds in their spatial memory accuracy or proactive interference performance. Using a variance partitioning approach, we report the first among-individual trade-off between spatial memory and proactive interference, uncovering variation in memory at the individual level where selection may act. Although we have no evidence of harsh habitats affecting spatial memory, our results suggest that if elevation produced differences in spatial memory between elevations, we could see concurrent changes in how quickly birds can forget.

Effects of season and food on the scatter-hoarding behavior of rodents in temperate forests of Northeast China

To explore the differences in hoarding strategies of rodents for different seeds in various seasons, we labeled and released the seeds of Pinus koraiensis, Corylus mandshurica, Quercus mongolica and Prunus sibirica in temperate forests of Northeast China and investigated the fate of the seeds in spring and autumn. The analysis showed that the hoarding strategies of the rodents varied substantially between seasons. The seeds were consumed faster in the spring than in the autumn. More than 50% of the seeds in the two seasons were consumed by the 16th day. It took 36 days to consume 75% of the seeds in the spring and 44 days in the autumn. The rate of consumption of the seeds in the spring was greater than in the autumn, and the rate of spread of the seeds was greater in the autumn. The distances of removal for the consumption and dispersal of seeds in the spring (3.26 ± 3.21 m and 4.15 ± 3.52 m, respectively) were both shorter than those in the autumn (3.74 ± 3.41 m and 4.87 ± 3.94 m, respectively). In addition, the fate of different seeds varied significantly owing to differences in hoarding strategies. The seeds of the three preferred species, P. koraiensis, C. mandshurica, and Q. mongolica, were quickly consumed. More than 90% of the seeds of these species were consumed. Only 21% of Pr. sibirica seeds were slowly consumed, and the two seasons had the same seed consumption rate patterns: the consumption rate of P. koraiensis seeds was the highest, followed by C. mandshurica, then Q. mongolica, and finally Pr. sibirica. The median removal times of the two seasons were different, but the rules were the same: P. koraiensis was the shortest, followed by C. mandshurica, and the third was Q. mongolica. In both seasons, the most predated in situ seeds were those of P. koraiensis; the most hoarded seeds were those of C. mandshurica, and the most unconsumed seeds were those of Pr. sibirica.