Scientific
publicationsThese are the abstracts of my main publications. Please, e-mail
me
Scientific
publicationsKeywords: avian frugivores, genefic diversity, plant recruitment, RAPD, seed dispersal, spatial variation
Abstract.- This paper analyses relationships between relative growth rate
(RGR), seed mass, biomass allocation, photosynthetic rate and other plant
traits as well as habitat factors (rainfall and altitude) in 20 wild species
of Aegilops L. and one closely related species of Amblyopyrum
(Jaub. & Spach) Eig., which differ in ploidy level (diploid, tetraploid
and hexaploid). The plants were grown hydroponically for 20 d in a growth
chamber. The relationships between parameters were calculated either using
the phylogenetic information (phylogenetically independent contrasts, PlC)
or without using the phylogenetic information (trait values of taxa, TIP).
The results using the two approaches were very similar, but there were a
few exceptions in which the results were different (e.g. RGR vs. seed mass).
Specific leaf area (SLA) was positively correlated with leaf area ratio
(LAR) and negatively correlated with net assimilation rate (NAR), which
together resulted in the absence of a correlation between SLA and RGR. Leaf
photosynthetic rates (expressed on a mass or area basis) showed no correlation
with RGR. RGR was positively correlated with the stem mass ratio and negatively
with root mass ratio. Species with a lower d. wt percentage have a higher
ROR. Aegilops species from locations with higher annual rainfall
invested less biomass in roots and more in shoots (leaves and stems) and
had a higher RGR. Diploid species had a lower seed mass and initial mass
than the hybrids (tetraploid and hexaploid species), but there was no correlation
of ROR with ploidy level. Polyploid species, which have higher seed mass,
occur at a higher altitude than diploid species. Our results show that variation
in ROR in Aegilops and Amblyopyrum spp. is associated mainly
with variation in biomass allocation (proportion of biomass in stems and
roots) and d. wt percentage, and not with variation in SLA, leaf photosynthetic
rates or seed mass.
Key words: Aegilops L., biomass allocation, photosynthesis, phylogeny,
rainfall, relative growth rate, seed mass, wild wheat.
Abstract.- By analyzing 296 published and unpublished data sets describing
annual variation in seed output by 144 species of woody plants, this article
addresses the following questions. Do plant species naturally fall into
distinct groups corresponding to masting and nonmasting habits? Do plant
populations generally exhibit significant bimodality in annual seed output?
Are there significant relationships between annual variability in seed production
and pollination and seed dispersal modes, as predicted from economy of scale
considerations? We failed to identify distinct groups of species with contrasting
levels of annual variability in seed output but did find evidence that most
polycarpic woody plants seem to adhere to alternating supra-annual schedules
consisting of either high or low reproduction years. Seed production was
weakly more variable among wind-pollinated taxa than animal-pollinated ones.
Plants dispersed by mutualistic frugivores were less variable than those
dispersed by either inanimate means or animals that predominantly behave
as seed predators. We conclude that there are no objective reasons to perpetuate
the concept of mast fruiting in the ecological literature as a shorthand
to designate a distinct bio\-logical phenomenon. Associations between supra-annual
variability in seed output and pollination and seed dispersal methods suggest
the existence of important reproductive correlates that demand further investigation.
Keywords: crop size, mast fruiting, pollination, seed dispersal, seed production.
Abstract.- Frugivorous birds consumed >75% of the ripe fruits of a Prunus
mahaleb population in southeastern Spain, but only half of the seed
crop was successfully removed from parent plants by legitimate seed dispersers.
For two consecutive years, I studied the sign and magnitude of phenotypic
selection exerted by frugivorous birds on fruit size and seed mass, two
key traits in this mutualistic plant-seed disperser interaction. Individual
plants showed extensive phenotypic variation in these traits, but among-individual
variation accounted for <30% of total trait variance. Selection patterns
were assessed at two levels by separating the effects of selection acting
on the parent tree (among-crop selection; comparing fruit removal and seed
dispersal efficiency among individual plants) and selection acting at the
individual seed level (comparing seed mass variation before and after dispersal
by frugivorous birds). Dispersal efficiency (percentage of the seed crop
dispersed) correlated negatively with crop size, fruit size, and seed mass.
However, only crop size was signifi\-cantly, positively, correlated with
the absolute number of seeds dispersed relative to the population mean,
used as the estimator for relative fitness. Greater visitation by dispersers
to smaller plants compensated for their lower fecundity but, for plants
with larger crops, a greater number of seeds was dispersed despite lower
dispersal efficiency. Directional and stabilizing/disruptive selection gradients
on fruit traits were not significant or, at best, only marginally significant,
indicative of weak and inconsistent selection effects on maternal phenotypes.
In contrast, selection on individual seed phenotypes was significant. Seeds
on the ground, after successful dispersal by frugivorous birds, were significantly
smaller than seeds 'available' at the start of the fruiting season. Observed
selection differentials on individual seed mass were -0.12 (1992) and -0.13
(1993), suggesting that frugivores might exert strong selection on individual
seed phenotypes irrespective of the maternal phenotype. This selection regime,
with far-reaching demographic consequences but low potential for inducing
evolutionary change in fruit traits, is expected on the basis of known hierarchical
selection cues used by foraging frugivores. Fruit phenotypic variation might
be irrelevant as a cue used by birds for discrimination among fruit crops,
but, given extensive within-crop variation, frugivores might strongly select
among seed phenotypes in a process not related consistently to among-crop
selection on maternal phenotypes.
Key words: fruit size; frugivorous birds; mutualism; phenotypic selection;
Prunus; seed dispersal; seed mass.
Abstract.- Variation in phenotypic traits of angiosperm fleshy fruits has been explained as the result of adaptations to their mutualistic seed dispersers. By analyzing the information available on fleshy fruit characteristics of 910 angiosperm species, I assess the hypothesis of evolutionary association between fruit phenotypic traits and type of seed disperser (birds, mammals, and mixed dispersers) and address explicitly and quantitatively alternative null hypotheses about phylogenetic effects. Phylogenetic affinity among plant taxa is accounted for by comparative methods including nested ANOVA, phylogenetic autocorrelation, and independent contrasts. Averaging over the 16 fruit traits examined, phylogenetic effects down to genus level explain 61% of total variance Phylogenetic autocorrelations are strong among close relatives, reaching significance for 11 of the 16 fruit traits examined. When assessed by independent contrast methods, correlated evolution between type of disperser and fruit traits is confined to fruit diameter. Differences among dispersal syndromes in other traits vanish after accounting for phylogenetic effects. These analyses reveal that seed dispersal syndromes are not entirely inter\-pretable as current adaptations to seed dispersers. Their status as exaptations can be assessed by combining experimental studies of natural selection on fruit size and rigorous comparative and cladistic tests of adaptational hypotheses.
Abstract: Recruitment of vertebrate-dispersed plants may be divided into
a series of sequential stages including fruit removal by frugivores, seed
delivery to the ground, post-dispersal seed survival, seedling emergence,
and seedling establishment. The particular processes operating at different
stages may be independent of each other ("uncoupled"), and peculiarities
in the configuration of the interrelationships between stages (sign and
magnitude of uncoupling) may lead to high site-specificity of the eventual
outcome ("spatial discordance"). This conceptual framework is
illustrated in this paper using recruitment data for the bird-dispersed
tree Phillyrea latifolia (Oleaceae) from two southeastern Spanish
localities (forest and scrubland habitats). Between-habitat differences
in P. latifolia recruitment are best understood by considering that
patterns of uncoupling among recruitment stages depend strongly on local
conditions, particularly on the thoroughness of fruit crop removal by frugivorous
birds. The interaction of P. latifolia with frugivores has implications
at every subsequent stage in recruitment, and proper understanding of the
constraints operating on recruitment requires recognition of the multiplicity
of stages involved. Uncoupling of stages was found to originate fine-scale
discordances in patterns of regeneration in the two habitats studied. We
use a structural equation model to quantify the direct and indirect effects
of the various recruitment stages on spatial variation in number of 2nd-year
seedlings recruited. Variation among microhabitats in recruitment was due
to variation in seed rain intensity and seed survivorship in scrubland,
while post-germination events limiting seedling emergence played a major
role in forest recruitment. Results of this study highlight the need of
considering the multi-staged nature of recruitment in vertebrate-dispersed
plants.
Keywords: Mediterranean habitats, population recruitment, seed dispersal
by vertebrates, seed and seedling survival, seedling recruitment, spatial
variation.
Abstract.- Spatial and temporal predictability in the mutual selective pressures of plants and frugivorous birds is a prerequisite for coevolution to occur. I examine the interaction patterns of strongly frugivorous thrushes (Turdus spp.) and their major winter food plants (Juniperus spp., Cupressaceae) and how they vary in space and time. Spatial congruency, rarely considered in seed dispersal studies, is studied at three spatial scales: 1) the total species range; 2) regional distribution; and 3) local abundance and its variation between seasons. Southern Spanish frugivorous thrushes and junipers show very low congruence in distribution patterns at each of these scales. Most juniper species show geographic distributions that are nested within the geographic ranges of thrush species. Bird species showed greater habitat breadth values than plants and were found in a greater percentage of localities. The local bird abundance was strongly correlated across years and sites with the local availability of juniper cones. Cone production varied markedly between years, but the rankings for different species in different years were statistically concordant at mid-elevation and lowland sites. Both bird abundance and cone production showed greater temporal than spatial variability. Variation of cone productions at both temporal and spatial scales was greater than variability in bird abundance. Species with strong interactions of mutual dependence showed very low values of biogeographic congruence, caused by differences in geographic range and habitat specificity. This obviously limits the possibilities for pairwise, specific coevolution to occur. However, mutual effects of species groups are possible to the extent that the component species are ecologically "interchangeable" in their selective effects and other constraints on coevolution are not operating. The approach used here to examine the patterns of species interactions at different biogeographic scales might prove useful in comparative studies of plant-animal interactions.
Abstract.- This study describes the reproductive biology of Prunus
mahaleb, a rosaceous treelet, in a southeastern Spanish population.
The species is gynodioecious with 55.4% of the plants being male-fertile
and 44.6% presenting non-functional, shrunken anthers with no pollen, and
behaving as functional females. Individual trees produced the same flower
morph in four consecutive study years. Fruit set in bagged inflorescences
was absent in male-sterile trees and was very reduced in male-fertiles.
Open-pollinated flowers of male-fertiles showed greater fruit set (mean
= 29.1%) than male-steriles (mean = 25.3%). Average fruit set in three experimental
treatments (control, selfed, and crossed) were 29.05%, 41.9% and 38.6%,
respectively, for male-fertile trees; those for male-steriles were 25.3%,
0% and 39.2%, respectively. Seeds from male-sterile plants were heavier
(71.33 mg) than those of male-fertile plants (66.05 mg) but did not differ
in germination ability. Male-fertile and male-sterile trees differ significantly
in average nectar concentration (73.5% and 55.9%, respectively) and nectar
volume secreted/flower and day (0.142 microL and 0.171 microL, respectively).
A total of 41 species of insect flower visitors were recorded. Calliphorid
and tachinid flies (41.97% of total visits), and andrenid bees (30.30%),
were the most frequent visitors. The diversity of insect visitors was greater
in male-fertile trees. Bees and flies accounted for 50.5% and 49.5%, respectively
of total visits to male-fertile trees. Flies were far more frequent than
bees at male-sterile flowers (76.9% and 23.1%, respectively). Male-sterile
trees received higher average visitation (47 insects/census) than malefertile
trees (32 insects/census). Individual trees showed a relative constancy
of the fecundity rankings between years. Fruit production was significantly
higher in male-sterile trees, with a four-year average of 6558 fruits, in
contrast with male-fertile trees which yielded 4670 fruits. This 1.77-fold
difference in favour of male-sterile trees over male-fertiles was not compensated
by the greater fruit set of the latter. This is attributable to the lower
outcrossing rate of male-fertiles, estimated as 52.68% from seed mass data.
In addition, greater seed mass of female progeny, and higher visitation
rate by insects might explain the maintenance of this polymorphism. These
results have far-reaching implications for the demography and seed-dispersal
ecology of this endozoochorus species.
Keywords:- Cryptic breeding systems - fruit set - gynodioecy - Mediterranean
- pollination Rosaceae.
Abstract.- Variation of gender expression and cone production is described
quantitatively for Juniperus phoenicea L. populations in southern
Spain and Morocco. The species is monoecious, but most populations showed
a dichotomy of gender expression at flowering, with predominantly "male"
and predominantly "female" plants and few "monoecious"
individuals, a functionally subdioecious breeding system. The proportion
of female plants in the Spanish populations ranged from 31% (R. B. Doñana)
to 40% (Cda. Sabinas, 1988) and did not exceed 10% in Morocco. Most plants
with femaleness values < 0.40 failed to set full-sized seed cones or
produced very small crops. Individual plants showed a significant constancy
of gender expression in consecutive years. Most inconsistencies in sexual
behavior involved transitions between the male and female expressions and
their respective "inconstant" conditions. Between-year variations
in seed-bearing cone production largely reflected changes in female flowering
gender of the individual plants; years with large crop production were characterized
by increases in average female gender expression for a given gender category
and, as a result, a greater percentage of the population producing female
cones. Plants differing in gender expression showed no significant differences
in size. Male plants always produced fewer than 10 female cones per crop,
and inconstant males rarely exceeded 200 female cones; female plants usually
had crop sizes above 100 cones, except in the seasons of cone crop failure.
Individual plants also differed in annual shoot growth, but these differences
were unrelated to both gender expression and cone production in the previous
season. Differences among populations accounted for 52% of total variance
in female cone size, while the effect of the individual plant accounted
for 26%; only 22% was attributable to within-plant variation. A nested model
with gender category as the main effect and plant as a nested effect accounted
for 88% of total variation in five cone characteristics, but gender effect
accounted for <= 2%.
Abstract.- The first data on flower biology and breeding systems of three
species of honeysuckle (Lonicera arborea Boiss., L. etrusca
G. Santi and L. splendida Boiss.) are reported for populations in
the Sierra de Cazorla y Segura (Jaén province, Spain). L. arborea
is predominantly pollinated during the day by bumblebees (Bombus
spp., Xylocopa spp. and Psithyrus vestalis, 70.1 %
of visits) and honeybees (28.3 % of the visits recorded), while L. etrusca
and L. splendida are pollinated during the evening and night by spbingid
moths (76.7 and 60.4% of visits, respectively). Bees are nectar robbers
in these two species with long tubular corollas. Percentage of flowers damaged
by nectar thieves averaged, per plant, 34.2% [10.1-75.6] for L. etrusca
and 18.2% [3.6-48.8%] for L. splendida. Flowers of L. arborea
last 4 days, with the stigma being receptive during the first and second
day; anthers dehisce on the second day of anthesis. Nectar production in
this species peaks in the second and third days. Flowers of both L. etrusca
and L. splendida open approximately 1 h before dusk; the stigma is
receptive in the first and second nights and anther dehiscence occurs on
the second day. Maximum nectar secretion for both species was recorded during
the first night of anthesis. Nectar secretion by L. arborea amounts
to 1.7 microL per flower/day with 40.2% disaccharide sugar concentration
while the other two species secrete 2.8 and 4.6 microL with concentration
of 23.5 and 19.6%, respectively. Seed set increased significantly after
crossed (xenogamous) pollinations (57-95% of flowers) relative to geitonagamous
crossings (18-29%) or controls. L. arborea was the only species setting
fruits with pollinators excluded. Xenogamous pollinations resulted in greater
weights of fruits and seeds for L. etrusca and L. splendida
because of the increased number of seed set but not as a result of the treatment
itself. Xenogamaus crossings resulted in significant increases in number
of seeds per fruit for the three species. Results suggest a dichotomy of
pollination systems within the genus among the sections Caprifolium
(long-tubed corollas) and Lonicera (short-tubed corollas), strongly
associated with other differences in growth patterns, geographic distribution
and habitat occupancy.
Key words: Pollination, breeding system, seed size, Bombus, Sphingidae,
Caprifoliaceae, Lonicera, nectar robbing, nectar.
Abstract.- The incidence of parthenocarpy and seed abortion as causes of
blank seed production in the dioecious, wind-pollinated shrub Pistacia
lentiscus were examined in a natural population in the Doñana
area, Huelva province, Spain. Fruits with empty seeds resulted either from
parthenocarpy, in absenee of pollination, or from embryo abortion, and in
both cases the fruit with empty seed rarely matured but was retained on
the plant. Average % of viable seeds were 19.89 ±15.82% (N= 29 plants),
and 43.38 ± 11.90% (N= 32 plants) for 1981 and 1982, respectively.
During 1981, with a severe drought, most fruit abscission was caused by
embryo abortion, with a small incidence of parthenocarpy. Increased rainfall
during the flowering period of 1982 most likely impaired the conditions
for wind transport of the pollen, and parthenocarpy was the main cause of
fruit abscission. The highest rates of fruit shedding were recorded for
most plants just after fruit set, well before the fruits had attained their
full size. After adjusting for the effects of crop size variation, the number
of viable seeds produced was positively correlated with plant size. The
number of aborted seeds and parthenocarpic fruits was independent of plant
size, being correlated only with crop size. The phenological uncoupling
with the flowering of males and increased distance to males, caused by the
neighborhood of other females, also contributed to reduced seed set. The
role of parthenocarpy and seed abortion as regulators of fruit number is
discussed in connection with the constraints derived by the wind-pollination
syndrome; their implications for the endozoochorous dispersal of seeds by
birds are also considered.
Key words: Anacardiaceae, Pistacia, reproductive biology, flowering,
fruiting, wind-pollination, parthenocarpy, seed abortion, Doñana,
Spain.
Abstract.- The frugivorous diets of Blackcaps and Garden Warblers in Mediterranean shrubland, determined by faecal analysis, are described. Variation in fruit consumption is related to the fruit supply and the relation with body mass and fat accumulation is examined. The overall diet was highly similar in the two study years but the rankings of the fruit species consumed in the same month of different years differed, suggesting that birds were adjusting the diet to variations in phenology and fruiting intensity. Regression analysis showed that fruit availability was the main factor correlated with fruit consumption. Both warbler species selected fruits with high energy-value and showed negative responses to fruit size only in the year when fruit supply was exceptionally high. Both species selected a small subset of the possible combinations of fruits (meals), including a large fraction of one or two major fruit species and small amounts of several minor species or insects. Meals of several fruit species were consumed more frequently than expected under the hypothesis of random and independent assortment of component fruits. Minor fruit species were consumed more frequently than expected from their relative availability. Pulp of minor fruits was significantly higher in minerals than the pulp of majors, that characteristically showed a higher energy content. Alkaloids were more frequently present in minor species. Both the accumulation of fat and body mass gain between recaptures of ringed birds were negatively correlated with the amount of fruit in their diet. A simulation of the diet under the premise of a total reliance on fruit food showed that warblers eating only fruits should obtain significantly reduced amounts of protein and minerals but increased energy income. Inclusion of minor amounts of insect prey dramatically increased the protein yield of the meals and this may be necessary to increase body mass and fattening. The implications of these patterns of dietary variation and fruit choice on plant seed dispersal are discussed.
Abstract.- Fruit consumption was assessed in six species of Sylvia warbiers and compared to variation in external morphology and digestive system. Variation in the use of fruit was determined primarily by external morphology (body-size, gape-width and hindlimb characteristics). Variation in digestive traits (intestine length, gizzard and liver weight) did not account for a significant fraction of variation in frugivory across species. Relative to other non-frugivorous Muscicapidae, Sylvia app. exhibit digestive adaptations specific to fruit processing; however, variation in external morphology constrains the degree of dependence on fruit within the genus.
Abstract.- Avian dispersal of seeds of the wild olive tree (Olea europaea
var. sylvestris) was studied in Mediterranean shrubland, southern
Spain. Fourteen species of small frugivorous birds in the genera Sylvia,
Turdus, Sturnus, and Erithacus accounted for 97.4%
of the fruits consumed by birds. The significance of each bird species as
an Olea fruit consumer was closely related to its abundance in the
area and was not associated with its dependence on the fruit for food; this
resulted in a highly asymmetric interaction between the plant and its dispersers.
Fruit production differed greatly between two consecutive seasons. During
an extremely dry year most trees aborted their entire fruit crop just after
flowering. During the 2nd yr, both flower production and fruit set increased,
and this resulted in larger crops of ripe fruit. Most fruits that ripened
(96.2% of the final-sized fruits) during the year of low fruit production
were consumed by dispersers (mean = 93.9%), and incidence of fruit-damaging
agents was low (6.0%). During the 2nd yr, fruit loss to the two main fruit
predators, Dacus oleae (Tephritidae) and Prays oleae (Yponomeutidae),
increased (mean = 27.1%, range 1.1-52.3%). A satiation process took place
during this year since fruit production exceeded the energy demand of the
disperser assemblage, and this increased the potential for fruit loss to
insect frugivores. Fruit removal by dispersers decreased (mean = 52.4%),
but the increase in fecundity during the 2nd yr for most of the trees compensated
for this difference and resulted in a greater absolute number of seeds removed.
Most variation in ripe fruit removal by birds was attributed to the interaction
of dispersal-related plant traits with insect frugivores that determine
post-ripening fruit losses. The types of higher order interactions that
result from the action of birds, the pulp-damaging fly, and the seed-eating
moth larva may damp, or reverse, any selective effect of a single system
component on plant traits related to seed dispersal.
Key words: Dacus; fruiting patterns; higher-order interactions; Olea
europaea; Prays; seed dispersal; seed predation; Spain; Sylvia;
Turdus.
Abstract.- Patterns of connectance and strength of mutual dependence in mutualisms have been examined by comparing the fraction of possible pairwise interactions established in a series of plant-pollinator and plant-seed disperser systems. As the number of species in the mutualistic system increases, the absolute number of interactions established increases, but connectance decreases exponentially. A given increase in diversity adds twice the number of interactions to dispersal systems as to pollination systems, suggesting a higher global specificity of the latter. Connectance patterns in mutualisms are analogous to some of those observed in complex food webs, suggesting a somewhat invariant structure in the relations between sets of interacting species. For seed dispersal systems involving frugivorous birds, mutual dependence values are strongly skewed toward the low end and illustrate generally strong asymmetries in mutualistic interactions. These patterns may be expected by considering simple multiplicative effects within multispecies assemblages as a result of variations in the number of species and in the underlying abundance distributions of the species involved. Coadaptation may originate from a process of species sorting without the necessity of genetic (coevolved) changes. Asymmetrical interactions and the prevalence of weak relations can provide pathways for rare species to persist and alternative routes for system responses to perturbations. These findings emphasize the diffuse nature of coevolution in mutualistic webs and suggest a mode by which diffuse coevolution can proceed.
| About l Home Page l Projects l Publications l Estación Biológica de Doñana l CSIC |