Jose M. Fedriani Laffitte - Academia.edu (original) (raw)

Papers by Jose M. Fedriani Laffitte

Fruit– frugivore interactions are crucial for the dynamics and regeneration of most forested ecos... more Fruit–
frugivore interactions are crucial for the dynamics and regeneration of most forested ecosystems. Still, we lack an
understanding of the potential variation in the sign and strength of such interactions in relation to variations in the spatial
and temporal ecological context. Here, we evaluated spatial (three sites) and temporal (two fruiting seasons) local variation
in the sign (seed predation versus dispersal) and strength (frequency and quantity) of the interactions among six frugivorous
mammals and a community of Mediterranean fleshy-fruited shrubs. We examined mammal faecal samples and quantified
frequency of seed occurrence, number of seeds per faecal sample, seed species diversity and quality of seed treatment
(i.e. percentage of undamaged seeds). The frequency of seed occurrence and number of seeds per faecal sample strongly
varied among dispersers, sites, seasons and fruit species. For instance, fox Vulpes vulpes faeces showed between 6 and
40 times more seeds than wild boar Sus scrofa faeces in seasons or sites in which Rubus and Juniperus seeds were dominant.
However, in seasons or sites dominated by Corema seeds, wild boar faeces contained up to seven times more seeds than fox
faeces. Mammalian carnivores (fox and badger, Meles meles) treated seeds gently, acting mostly as dispersers, whereas deer
(Cervus elaphus and Dama dama) acted mainly as seed predators. Interestingly, rabbit Oryctolagus cuniculus acted as either
mostly seed disperser or seed predator depending on the plant species. Our results indicated that the sign of fruit–frugivore
interactions depended mainly on the identity of the partners. For a particular fruit–frugivore pair, however, our surrogate
of interaction strength largely varied with the spatio-temporal context (year and habitat), leading to a low specificity across
the seed–frugivore network. The high spatio-temporal variability of seed dispersal (in quantity, quality and seed diversity)
by different frugivores would confer resilience against unpredictable environmental conditions, such as those typical of
Mediterranean ecosystems.

Debido a que la dispersión de semillas por animales vincula el final del ciclo reproductor de las... more Debido a que la dispersión de semillas por animales vincula el final del ciclo reproductor de las plantas con el establecimiento de su descendencia, se le atribuyen profundos efectos sobre la sucesión, regeneración y conservación de los hábitats. Mediante una serie de experimentos de campo estudiamos, durante tres años, el papel de los mamíferos en distintos estadios del ciclo reproductor de varios arbustos de frutos carnosos en el Parque Nacional de Doñana. Los principales resultados fueron: -El gremio de mamíferos semifrugívoros estudiado ingiere y libera semillas viables en gran número y de una alta diversidad de especies de plantas de frutos carnosos de Doñana.

Most studies on the causes of animal dispersal focus on species of birds or small mammals, but th... more Most studies on the causes of animal dispersal focus on species of birds or small mammals, but there are few such studies on solitary carnivores. A complete picture of the causes of animal dispersal is not possible without considering cases on a representative set of animals. The Iberian lynx is a medium-size, solitary carnivore that inhabits metapopulations, where dispersal plays a prominent role. Between 1983 and 1998 we studied the proximate and ultimate causes of dispersal in Iberian lynx in the Doñana metapopulation (southwestern Spain), based on radio-tracking of 49 individuals. Saturation of limited breeding areas in this small population leads to high dispersal rates in both sexes. Most lynxes dispersed from their natal area between 12 and 24 months of age. Males younger than 1 year old tended to disperse in a higher proportion than females of the same age. However, high dispersal rates for both sexes by the age of 2 years and the lack of differences in the dispersal distances do not support inbreeding avoidance as an ultimate cause of dispersal. Dispersal mainly started between January and June (24/29 cases), when most social interactions occur, which supports the social subordination hypothesis. Lynxes left the natal range at an earlier age from the local population with higher density, which supports intraspecific competition for resources as a cause for dispersal. However, prey seems not to be the limiting resource because dispersal mostly started during the season of increasing prey density, and individual probability of dispersal increases with prey density in the natal area. Dispersers suffered higher mortality than nondispersing lynxes of the same age, due mostly to anthropogenic causes. About half of the dispersers successfully settled in a territory at distances that differed between areas of origin, but not between sexes. Distances reached, shorter than those reported for other similar-size solitary felids, are limited by anthropogenic barriers that prevent connection with closer metapopulations.

Literature on seed dispersal mutualisms suggests that plant populations should hardly adapt to th... more Literature on seed dispersal mutualisms suggests that plant populations should hardly adapt to their current dispersers. We address the predictions that selection pressures exerted by ants on dispersal-related diaspore traits of the antdispersed Helleborus foetidus are highly variable in space, and that geographic (inter-population) variation in these traits is unrelated to selection by current dispersers. To test these predictions we use the concept of the quantitative adaptive landscape for seed size at dispersal. Such landscape depicts the relationship between the population's mean trait value (mean seed size in the present study) and the population's mean fitness (mean dispersal probability in the present study). Adaptive landscapes make it possible to assess whether the mean population's phenotype agrees with one favored by selection. We first analyse, in 12 populations of H. foetidus from southern Spain, the extent of divergence among populations in seed and elaiosome size, and the abundance, composition, and behavior of the ant communities. Seeds from a fixed set of five of these populations were offered to ants in all the study sites to fit the adaptive landscape for seed size. In addition, seeds from the local population were also offered in each site. Our results show that seed size has undergone a larger divergence among populations than elaiosome size. Despite geographic variation in ant assemblages, the adaptive landscapes for seed size at dispersal were remarkably similar among sites: ants create disruptive selection on seed size in 10 out of 12 study sites. As predicted, the basic features of these adaptive landscapes (curvature and location of the minimum) varied geographically in accordance with variation in the size of seed dispersers. Also as predicted, in most populations, the observed mean seed size does not agree with that expected from the adaptive landscapes at dispersal. However, the relevance of dispersers for seed size evolution should not be neglected since the agreement between observed and Ó Springer Science+Business Media B.V. 2006 optimum seed size was stronger where dispersers were more abundant. Thus, against the general view, our results evidence that, in H. foetidus, the observed geographic variation in dispersal-related plant traits is partly linked to selection exerted by current dispersers. Geographic variation in ant assemblages determines both the existence of a selection mosaic and the degree of adjustment of populations to the patterns of selection in the mosaic.

The seeds of many plant species present a food body that is consumed by animal dispersers. In the... more The seeds of many plant species present a food body that is consumed by animal dispersers. In theory, if the animals are polyphagous, the availability of alternative food resource other than the diaspore itself may influence its dispersal and survival. We used the myrmecochore Helleborus foetidus L. (Ranunculaceae), the seeds of which are attached to a lipid-rich elaiosome that is attractive to ants, as a model system to investigate (1) whether alternative foods that are present along with the plant affect ant foraging behavior and diaspore removal and (2) whether food availability in an ant nest affects seed predation and germination. In a field experiment, artificial diaspore depots were offered together with either sugar, insect corpses, seed, or no food (control). Contrary to the prediction that ants would rather concentrate their foraging effort on the highly rewarding alternative foods only, many workers, attracted by the sugar, switched to the hellebore diaspores, which significantly enhanced removal rate. Results obtained in the laboratory further indicated that the larvae of Aphaenogaster iberica (a major seed disperser) predated more on the H. foetidus embryos when no alternative food was available. This, in turn, slightly reduced seed germination. Overall, these results shed light, for the first time, on the potential indirect effects of alternative resources on the fate of diaspores adapted for ant dispersal.

X. 2004. Geographical variation in the potential of mice to constrain an ant-seed dispersal mutua... more X. 2004. Geographical variation in the potential of mice to constrain an ant-seed dispersal mutualism. Á/ Oikos 105: 181 Á/191.

2005. Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide g... more 2005. Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range. Á/ Ecography 28: 583 Á/592.

1. Plant defensive compounds and predation risk are main determinants of herbivore foraging, thou... more 1.
Plant defensive compounds and predation risk are main determinants of herbivore
foraging, though empirical studies have seldom measured the combined effects of these
two factors. By considering the interaction between the herb
Helleborus foetidus
and
its main fruit and seed predator, the Wood Mouse
Apodemus sylvaticus
, we evaluated
whether the defensive role against seed predators of compounds present in
H. foetidus
unripe fruits holds across a micro-landscape that differs in foraging costs (i.e. predation
risk).
2.
First, we used standardized food patches that simulated fruiting
H. foetidus
plants
to ascertain fruit preferences of captive mice. Then, by means of field experiments, we
assessed the combined effects of fruit ripening and predation risk on foraging by freeranging
mice.
3.
Captive mice avoided plants with unripe fruit and avoided consuming unripe fruits
within a particular plant. Free-ranging mice also avoided unripe fruits in safe microhabitats
(rocky substrate), but not in risky microhabitats (bare ground) where few fruits
were consumed. This unexpected result may be driven by predation risk experienced by
mice foraging on
H. foetidus
fruits, and/or plant defensive compounds acting in a dosedependent
manner.
4.
Frugivorous mice responded to both chemical defences present in unripe
H. foetidus
fruits as well as to predation cost though such response was sequential. Plant defence
compounds appeared to play a part in mouse foraging only after mice selected low
predation risk microhabitats.
5.
Our study indicates that both digestive and ecological factors influence foraging
decisions, which in turn affects pressures exerted by herbivores on plant populations.

Seed dispersal by animals is a key interaction, with effects on the population ecology and evolut... more Seed dispersal by animals is a key interaction, with effects on the population ecology and evolution of many plant lineages. Despite the fact that infrequent seed dispersers can potentially provide important services to plant populations, little attention has been paid so far to scarce mutualists. We assessed different aspects of quantity and quality of seed dispersal from fruit removal to seed germination in the Iberian pear, Pyrus bourgaeana, finding that fruit consumers markedly differed in the nature of their interaction with the tree. Whereas the abundant rodents, rabbits, and deer damaged all seeds eaten, the uncommon carnivores badger and fox and the abundant boars dispersed a large fraction of ingested seeds as viable propagules, acting as legitimate seed dispersers. Despite low rates of visitation by badgers to fruiting trees, they transported more viable seeds than the abundant boars, due to better seed treatment and a higher feeding rate on pears. Seed dispersal by all 3 legitimate dispersers, especially the badger, enhanced post-dispersal P. bourgaeana seed survival, supporting the "escape" predation hypothesis. Pyrus bourgaeana showed relatively high frequencies of visits by a myriad of frugivores; however, it relied on the dispersal service provided by an infrequent carnivore, the badger, rather than on those provided by the abundant mammalian herbivores. Therefore, under some circumstances, uncommon animal counterparts play major roles in their mutualistic interactions with flowering plants.

Using field seed sowings, we assessed how four mammal species (Meles meles, Vulpes vulpes, Sus sc... more Using field seed sowings, we assessed how four mammal species (Meles meles, Vulpes vulpes, Sus scrofa, and Oryctolagus
cuniculus) influenced seed germination in three fleshy-fruited Mediterranean shrubs (Corema album, Pyrus bourgaeana,
and Rubus ulmifolius). We predicted that gut passage and removal away from mother plants would enhance the quantity,
speed, and asynchrony of seed germination. Results showed that percent germination was altered by gut passage, but that
the magnitude and even the direction of such effects varied according to plant and disperser species. Likewise, dispersal
away from mother plants affected the percentage and germination speed in some species but not others. Gut passage
increased asynchrony of germination in Rubus and Pyrus, and removal from the mother plant increased asynchrony in
Rubus, which likely enhances plant fitness in unpredictable environments. Gut passage generally had a stronger effect on
germination than removal away from mother plants, but for some species both factors were similarly influential.
Therefore, the combined effects of both seed dispersal services varied individually among fruit and frugivore species,
leading to unusually high functional diversity in this seed dispersal mutualism.

The degree to which plant individuals are aggregated or dispersed co-determines how a species use... more The degree to which plant individuals are aggregated or dispersed co-determines how a species uses resources, how it is
used as a resource, and how it reproduces. Quantifying such spatial patterns, however, presents several methodological
issues that can be overcome by using spatial point pattern analyses (SPPA). We used SPPA to assess the distribution of
P. bourgaeana adult trees and their seeds (within fecal samples) dispersed by three mammals (badger, fox, and wild boar)
within a 72-ha plot across a range of spatial scales. Pyrus bourgaeana trees in our study plot (n75) were clearly
aggregated with a critical spatial scale of ca 25 m, and approximately nine randomly distributed tree clusters were
identified. As expected from their marking behaviors, the spatial patterns of fecal deposition varied widely among
mammal species. Whereas badger feces and dispersed seeds were clearly clustered at small spatial scales (B10 m), boar
and fox feces were relatively scattered across the plot. A toroidal shift null model testing for independence indicated that
boars tended to deliver seeds to the vicinity of adult trees and thus could contribute to the maintenance and enlargement
of existing tree clusters. Badgers delivered feces and seeds in a highly clumped pattern but unlike boars, away from
P. bourgaeana neighborhoods; thus, they are more likely to create new tree clusters than boars. The strong tree
aggregation is likely to be the result of one or several non-exclusive processes, such as the spatial patterning of seed
delivery by dispersers and seedling establishment beneath mother trees. In turn, the distinctive distribution of
P. bourgaeana in Don˜ana appeared to interact with the foraging behavior of its mammalian seed dispersers, leading to
neighbourhood-specific dispersal patterns and fruit-removal rates. Our study exemplifies how a detailed description of
patterns generates testable hypotheses concerning the ecology of zoochorous. Pyrus bourgaeana dispersers were unique and
complementary in their spatial patterning of seed delivery, which likely confers resilience to their overall service and
suggests lack of redundancy and expendability of any one species.

We chose the interaction between the Mediterranean dwarf palm (Chamaerops humilis) and its major ... more We chose the interaction between the Mediterranean dwarf palm (Chamaerops
humilis) and its major seed disperser, the Eurasian badger (Meles meles), to evaluate the
hypothesis that endozoochory is characterized by a mixture of conflicting and overlapping
interests, with the capacity of being positive or negative for plant fitness. For instance, because
of the potential protective role against invertebrate seed predators of C. humilis pulp, we
expected that badger-ingested diaspores (i.e., seeds without pulp) would show lower survival
than control seeds with the pulp attached. Conversely, due to the possible germination
inhibitory function of C. humilis fruit pulp, it was also likely that badger-ingested seeds
germinate in higher proportion than control seeds. We evaluated our predictions by carrying
out a field sowing and monitoring it over two years. We estimated several stage-specific
transition probabilities as well as the cumulative probability of seedling recruitment under
different treatments. Our experimental results revealed the multifunctionality of C. humilis
fruit pulp and that fruit ingestion by badgers had conflicting outcomes for the palm. As
predicted, seed survival was much lower and seed predation by invertebrates much higher for
badger-ingested than for control seeds, suggesting a defensive role of C. humilis ripe fruit pulp.
All early-emerged seedlings came from badger-ingested seeds, suggesting an inhibitory
function of fruit pulp. Though we did not find an effect of removal from the maternal
environment on most components of fitness, seedling survival for badger-ingested seeds was
higher away from than beneath conspecifics. Badgers imposed a sizeable short-term fitness
cost to C. humilis and therefore could be categorized as a ‘‘dangerous liaison.’’ Nonetheless,
because of the high mobility of the badger, its dispersal service appears paramount given the
severe fragmentation and isolation of most C. humilis populations across the highly
humanized Mediterranean basin. Our study thus illustrates the necessity of assessing
concurrently direct and indirect effects of plant–disperser interactions at different stages of
the plant life cycle and recruitment process.

The persistence of mutualisms despite the strong incidence of exploiters could be explained if ex... more The persistence of mutualisms despite the strong incidence of exploiters could
be explained if exploiters deny one or more services (i.e., cheat) while eventually supplying
some subtler but critical services. Pulp feeders usually ingest fruit reward without dispersing
seeds and thus are considered to be mainly cheaters or thieves of seed-disperser mutualisms.
By consuming the fruit pulp, however, they could release seeds from pulp inhibitory effect,
enhancing germination and, potentially, subsequent seedling emergence, growth, survival, and
thus local recruitment. We evaluated such a largely neglected hypothesis by considering the
interaction between Pyrus bourgaeana and its pulp feeders. We experimentally showed that
pericarp removal had a consistent strong positive effect on seed performance (e.g., lower
rotting and higher germination percentages) and seedling fate (greater emergence, growth, and
survival to two years old). Interestingly, these relatively large positive effects of depulpation on
plant fitness persisted for a surprisingly long time. Though seedlings experienced higher
mortality under fruiting conspecifics, the benefits of depulpation were not overridden by high
propagule mortality beneath fruiting trees or in adverse microhabitats after two years of
monitoring. Specifically, the cumulative probability of establishment for depulped seeds was
4–25 times higher than for seeds in whole ripe fruits. Thus, under some circumstances, pulp
feeders can provide essential services to endozoochorous plants. Our study contributes to
clarifying the apparent paradox of plant–frugivore mutualisms that persist in the face of
exploitation by pulp feeders. Because ‘‘thieves’’ and ‘‘mutualists’’ refer to the extremes of a
complex continuum, and because organisms displaying concurrent cheating and honest
behaviors during different host stages are likely prevalent, the persistent language of
mutualists vs. thieves, cheaters, or exploiters might be misleading.

Pulp feeders usually ingest fruit rewards without dispersing their seeds, and thus are considered... more Pulp feeders usually ingest fruit rewards without dispersing their seeds, and thus are considered to be mainly cheaters or thieves of seed-disperser mutualisms. By consuming the pulp, however, they could release seeds from its inhibitory effect, enhancing germination, and potentially, subsequent seedling emergence, growth, survival, and thus local recruitment. We experimentally showed that pericarp removal of Pyrus bourgaeana fruits by rabbits, Oryctolagus cuniculus, had a consistent strong positive effect on both seed performance and seedling fate. Specifically, the probability of recruitment for depulped seeds was from 4 to 25 times higher than for seeds in whole ripe fruits. Because "thieves" and "mutualists" merely refer to the extremes of a complex continuum, the persistent language of mutualist vs. thieves, cheaters, or exploiters, might be misleading.

We compared movement patterns and rhythms of activity of a top predator, the Iberian lynx Lynx pa... more We compared movement patterns and rhythms of activity of a top predator, the Iberian lynx Lynx pardinus, a mesopredator, the red fox Vulpes vulpes, and their shared principal prey, the rabbit Oryctolagus cuniculus, in relation to moon phases. Because the three species are mostly nocturnal and crepuscular, we hypothesized that the shared prey would reduce its activity at most risky moon phases (i.e. during the brightest nights), but that fox, an intraguild prey of lynx, would avoid lynx activity peaks at the same time. Rabbits generally moved further from their core areas on darkest nights (i.e. new moon), using direct movements which minimize predation risk. Though rabbits responded to the increased predation risk by reducing their activity during the full moon, this response may require several days, and the moon effect we observed on the rabbits had, therefore, a temporal gap. Lynx activity patterns may be at least partially mirroring rabbit activity: around new moons, when rabbits moved furthest and were more active, lynxes reduced their travelling distances and their movements were concentrated in the core areas of their home ranges, which generally correspond to areas of high density of rabbits. Red foxes were more active during the darkest nights, when both the conditions for rabbit hunting were the best and lynxes moved less. On the one hand, foxes increased their activity when rabbits were further from their core areas and moved with more discrete displacements; on the other hand, fox activity in relation to the moon seemed to reduce dangerous encounters with its intraguild predator.

Photo 1. In the Pistacia-dominated shrubland, dwarf palms Chamaerops humilis and corn oaks Quercu... more Photo 1. In the Pistacia-dominated shrubland, dwarf palms Chamaerops humilis and corn oaks Quercus suber are abundant. Note also the Pistacia lentiscus shrubs in the second line.

1. Community context can alter the likelihood of interactions among community members and thus ex... more 1. Community context can alter the likelihood of interactions among community members and thus
exert critical ecological effects with potential evolutionary implications. For instance, plant–animal
mutualisms can be exploited by third species that usurp the resources and/or service that the mutualists
offer, while delivering limited or no benefits in return.
2. We experimentally revealed for the first time how exploiters of plant–disperser mutualisms (i.e.
pulp feeders) alter the frequency of plant interactions with subsequent mutualistic (seed dispersers)
and antagonistic (seed predators) animal associates. In doing so, we chose to study the endozoochore
Pyrus bourgaeana, which interacts with a diverse assemblage of frugivores including exploiters
(pulp-feeding rabbits), legitimate seed dispersers (mammalian carnivores) and seed and fruit predators
(rodents and deer, respectively). We hypothesized that pulp feeders would render fruit barely
rewarding, affecting subsequent tree–animal interactions.
3. As predicted, pulp removal lessened tree dispersal success (i.e. lowered interaction frequency
with seed dispersers) causing an indirect negative effect on its fitness. Furthermore, pulp feeders
facilitated foraging by seed-eating rodents, leading to a negative indirect effect on seed survival.
Nonetheless, these negative effects of pulp removal on tree fitness were partly counterbalanced by a
noticeable decrease in fruit predation by deer. Because both seed dispersers and seed predators preferred
large fruits, they exerted selection pressures on fruit size in opposite directions; thus, the net
selection regime on fruit size experienced by the tree appeared largely contingent on community
composition.
4. Synthesis. Our results illustrate how interactions among functionally distinct frugivores can act
synergistically or antagonistically and thus alter their ecological outcomes in ways that differ from
those predicted by pairwise interactions. Further research on the relationships between fruiting plants
and their consumers will certainly further our understanding of how community context can modify
ecological and evolutionary outcomes of complex multispecies interactions.

Intra- and interspecific spatially contagious seed dispersal has far-reaching implications for pl... more Intra- and interspecific spatially contagious seed dispersal has far-reaching
implications for plant recruitment, distribution, and community assemblage. However,
logistical and analytical limitations have curtailed our understanding concerning the
mechanisms and resulting spatial patterns of contagious seed dispersal in most systems and,
especially, in complex seed-disperser networks. We investigated mechanisms of seed
aggregation using techniques of spatial point pattern analysis and extensive data sets on
mutispecific endozoochorous seed rain generated by five frugivorous mammals in three
Mediterranean shrublands over two seasons. Our novel analytical approach revealed three
hierarchical and complementary mechanisms of seed aggregation acting at different levels
(fecal samples, seeds, pairs of seed species) and spatial scales. First, the three local guilds of
frugivores tended to deliver their feces highly aggregated at small and intermediate spatial
scales, and the overall pattern of fecal delivery could be described well by a nested doublecluster
Thomas process. Second, once the strong observed fecal aggregation was accounted
for, the distribution of mammal feces containing seeds was clustered within the pattern of all
feces (i.e., with and without seeds), and the density of fecal samples containing seeds was
higher than expected around other feces containing seeds in two out of the three studied seeddisperser
networks. Finally, at a finer level, mark correlation analyses revealed that for some
plant species pairs, the number of dispersed seeds was positively associated either at small or
large spatial scales. Despite the relatively invariant patterning of nested double-clustering,
some attributes of endozoochorous seed rain (e.g., intensity, scales of aggregation) were
variable among study sites due to changes in the ecological context in which seeds and their
dispersers interact. Our investigation disentangles for the first time the hierarchy of synergic
mechanisms of spatially contagious seed dispersal at a range of spatial scales in complex seeddisperser
networks, thus providing a robust and widely applicable framework for future
studies.