Luis Navarro

Beyond species loss: the extinction of ecological interactions in a changing world

Summary 1. The effects of the present biodiversity crisis have been largely focused on the loss of species. However, a missed component of biodiversity loss that often accompanies or even precedes species disappearance is the extinction of ecological interactions. 2. Here, we propose a novel model that (i) relates the diversity of both species and interactions along a gradient of environmental deterioration and (ii) explores how the rate of loss of ecological functions, and consequently of ecosystem services, can be accelerated or restrained depending on how the rate of species loss covaries with the rate of interactions loss. 3. We find that the loss of species and interactions are decoupled, such that ecological interactions are often lost at a higher rate. This implies that the loss of ecological interactions may occur well before species disappearance, affecting species functionality and ecosystems services at a faster rate than species extinctions. We provide a number of empirical case studies illustrating these points. 4. Our approach emphasizes the importance of focusing on species interactions as the major biodiversity component from which the ‘health’ of ecosystems depends.

Seed germination and seedling survival of two threatened endemic species of the northwest Iberian peninsula

Abstract We examined germination and seedling survival of Petrocoptis grandiflora and Petrocoptis viscosa (Caryophyllaceae), two narrow endemic species from the northwest Iberian Peninsula. The experiments were carried out with seeds of three of eight populations of P. grandiflora and one of the three sole populations of P. viscosa. Under natural conditions, both P. grandiflora and P. viscosa produce very large numbers of seeds. However, the specific microhabitat of these species (cracks and crevices of limestone rockfaces) has very marked effects on seed germination, and subsequent seedling survival. In the present study, we examined the effects of light, cold treatment and seed weight on germination capacity. In the case of P. grandiflora, we also compared the germination of seeds of the different populations. In addition, we assessed seedling survival over a 1-year period. Seeds maintained in darkness showed higher germination percentages than seeds maintained with a 12:12 h photoperiod. The application of a short period of cold prior to germination had no significant effect in either species. In the case of P. grandiflora, population of origin had a significant effect on germination percentage. Of all the factors considered, seed weight was the most important source of variability, both in seed germination and subsequent seedling survival. In both species in the natural habitat, less than 10% of germinated seeds survived by the end of the year. Seedling survival was affected by microhabitat. Seedlings in non-rockface soil microhabitats were more likely to suffer herbivory or interspecific competition than seedlings in crevices in the rockface.

Reproductive biology and effect of nectar robbing on fruit production in Macleania bullata (Ericaceae)

Hummingbird-pollinated flowers are frequently subjected to nectar robbing. In this paper, I examine the impact of nectar robbing on plant reproductive success on a hummingbird-pollinated species. After studying the basic aspects of the floral morphology and reproduction of Macleania bullata (Ericaceae) in a tropical montane wet forest in southwest Colombia, I examined the percent of flowers robbed and the effect of nectar robbery on fruit set. The flowers of this species are typical for plants pollinated by long-bill hummingbirds. They are protandrous and open for four days. Fruit production requires a pollinator visit; fruit set following pollinator exclusion was zero. Fruit set following xenogamous pollen transfer (36.8%) differed significantly from that of population controls (11.9%) and of autogamous pollen transfer (6.3%). Nectar volume, sugar concentration and sugar production were measured at daily intervals from bud opening until the fading of flowers. Daily nectar production (both volume and amount of sugar) varied considerably with flower age. Sugar production peaked on the second day, coinciding with the male phase. The frequency of nectar robbing in the studied population was very high (75% of examined flowers) and was positively correlated with reduced fruit set. I discuss the probability of a relation between reduced fruit set on robbed flowers and an energetic investment. Robbing by non-pollinating visitors can suppose the plant to re-synthesize more nectar. The high incidence of nectar robbing impugns the advantage of specialization.

Effect of pollination on floral longevity and costs of delaying fertilization in the out-crossing Polygala vayredae Costa (Polygalaceae).

BACKGROUND AND AIMSnThe effect of pollination on flower life span has been widely studied, but so far little attention has been paid to the reproductive consequences of delayed pollination in plants with long floral life spans. In the present study, Polygala vayredae was used to answer the following questions. (1) How does male and female success affect the floral longevity of individual flowers? (2) How does delaying fertilization affect the female fitness of this species?nnnMETHODSnFloral longevity was studied after experimental pollinations involving male and/or female accomplishment, bagging and open pollination. The reproductive costs of a delay in the moment of fertilization were evaluated through fruit set, seed-ovule ratio and seed weight, after pollination of flowers that had been bagged for 2-18 d.nnnKEY RESULTSnSenescence of the flowers of P. vayredae was activated by pollen reception on the stigmatic papillae, while pollen removal had no effect on floral longevity. Nonetheless, a minimum longevity of 8 d was detected, even after successful pollination and pollen dissemination. This period may be involved with the enhancement of male accrual rates, as the female accomplishment is generally achieved after the first visit. Floral life span of open-pollinated flowers was variable and negatively correlated with pollinator visitation rates. Delayed pollination had a major impact on the reproductive success of the plant, with fruit set, seed-ovule ratio and seed weight being significantly diminished with the increase of flower age at the moment of fertilization.nnnCONCLUSIONSnA strong relationship between pollination and floral longevity was observed. Flowers revealed the ability to extend or reduce their longevity, within some limits, in response to the abundance of efficient pollinators (i.e. reproductive fulfilment rates). Furthermore, with scarce or unpredictable pollinators, a long floral life span could maintain the opportunity for fertilization but would also have reproductive costs on production of offspring. Reduced female fitness late in the flowers life could shift the cost-benefit balance towards a shorter life span, partially counteracting the selection for longer floral life span potentially mediated by scarce pollination services.

When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae

A great proportion of bats of the New World family Phyllostomidae feed on fruit, nectar and pollen, and many of them present adaptations to feed also on insects and small vertebrates. So far, attempts to examine the diversification of feeding specialization in this group, and particularly the evolution of nectarivory and frugivory, have provided contradictory results. Here we propose a molecular phylogenetic hypothesis for phyllostomids. On the basis of a matrix of feeding habits that takes into account geographical and seasonal variation, we tested different hypotheses of the evolution of feeding specializations in the group. We find strong support for the evolutionary model of a direct dietary diversification from insectivory. The estimates of divergence times of phyllostomid bats and the reconstruction of ancestral states with a Bayesian approach support the parallel evolution of frugivory in five lineages and of nectarivory in three lineages during the Miocene. On the basis of these findings, and recent dietary studies, we propose that during the evolution of phyllostomids switches to new feeding mechanisms to access to abundant and/or underexploited resources provided selective advantages that favoured the appearance of ecological innovations independently in different lineages of the family. We did not find evidences to support or reject the hypothesis that the insectivorous most recent common ancestor of all phyllostomids was also phytophagous.

A New Approach to the Quantification of Degree of Reciprocity in Distylous (sensu lato) Plant Populations

BACKGROUND AND AIMSnAlthough evolution of sexual polymorphism has been traditionally analysed using discrete characters, most of these polymorphisms are continuous. This is the case of heterostyly. Heterostyly is a floral polymorphism successfully used as a model to study the evolution of the sexual systems in plants. It involves the reciprocal positioning of anthers and stigmas in flowers of different plants within the same population. Studies of the functioning of heterostyly require the quantification of the degree of reciprocity between morphs of heterostylous species. Some reciprocity indices have been proposed previously, but they show significant limitations that need to be dealt with. This paper analyses these existing indices, and proposes a new index that aims to avoid their main problems (e.g. takes into account population variability and offers a single value per population).nnnMETHODSnThe new index is based on the comparison of the position of every single sexual organ in the population with each and every organ of the opposite sex. To carry out all the calculations, a macro was programmed with MS Visual Basic in MS Excel. The behaviour of the index is tested using hypothetical data to simulate different situations of dimorphic populations; the index is also tested with some actual populations of different species of the genus Lithodora.nnnRESULTS AND CONCLUSIONSnThe index of reciprocity proposed here is a sound alternative to previous indices: it compares stigma-stamen height gaps for all potential crosses in the population, it comprises stigma-stamen distance as well as dispersion, it is not skewed by the more frequent sex, and it can be meaningfully compared between populations and species. It has produced solid results for both hypothetical and natural populations.

Natural regeneration of subtropical montane forest after clearing fern thickets in the Dominican Republic

Tropical forests can recover after anthropogenic disturbances of light to moderate intensity (Aide et al . 1995, 1996, 2000; Uhl 1987, Uhl et al . 1988); however, severe disturbances (e.g. compaction or loss of soil) often result in conditions that prevent forest recovery. These degraded sites are often dominated by grasses (Aide & Cavelier 1994, Cabin et al . 2002, Cavelier et al . 1998, Uhl et al . 1988) and ferns (Cohen et al . 1995, Garcia et al . 1994, Slocum et al . 2000, Walker & Boneta 1995) that can impose barriers for tree regeneration and arrest the succession process. Important barriers for tree regeneration include: (1) competition with grasses and ferns for soil moisture, nutrients and light (Aide & Cavelier 1994, Guimaraes-Vieira et al . 1994, Holl et al . 2000, Nepstad et al . 1996, Russell et al . 1998, Walker 1994, Zimmerman et al . 2000), and (2) dispersal limitation given that grasses and fernlands offer few resources that attract seed dispersers (Guevara & Laborde 1993, Holl et al . 2000, McDonnell & Stiles 1983, Slocum & Horvitz 2000, Zimmerman et al . 2000).

The role of floral biology and breeding system on the reproductive success of the narrow endemic Petrocoptis viscosa rothm. (Caryophyllaceae)

Morphological and functional characteristics of flowers may have major effects on their reproductive success. Here, we report a study on the characteristics of flowers of Petrocoptis viscosa, a herb species endemic to the northwest Iberian Peninsula, restricted to crevices in limestone outcrops, and currently occurring in only three populations within an area of less than 30 km 2 . We also investigated the effects of pollen source on indicators of reproductive success. The results show that Petrocoptis viscosa flowers are well adapted to autogamy. Inbreeding depression (as determined by comparison of results obtained after selfing and outcrossing) was negligible for fruit production (d=� 0.05) and mean seed number (d=� 0.11), low for seed germination percentage (d=0.08), but relatively high for mean seed weight (d=0.23). The spatial structure and small size of population of Petrocoptis viscosa may mean that inbreeding is frequent in natural habitats. Adaptation of plants to autogamy may therefore be energetically beneficial (i.e. less wasted expenditure on rewards and flowers). # 2001 Elsevier Science Ltd. All rights reserved.

Consequences of nectar robbing for the fitness of a threatened plant species

The effect of nectar robbing on plant fitness is poorly understood and restricted to a few plant species. Furthermore, the available studies generally evaluate the effects of nectar robbing on female fitness, disregarding the male component. Here we measured the effects of the nectar-robbing bumblebees on male (measured as pollen analogue flow distance) and female (measured as seed production) reproductive success in the insect-dependent Polygala vayredae, a narrow endemic species from the pre-Pyrenees (Spain). Intense nectar robbing by bumblebees significantly reduced the nectar available to legitimate pollinators in the studied population, and this reduction affected both male and female fitness. Significant differences were observed in fluorescent dye dispersion between robbed and non-robbed flowers within the population. Fluorescent dyes from non-robbed flowers were dispersed to larger distances and over a larger number of flowers when compared with robbed ones. Moreover, significant differences were observed in both fruit set and seed ovule ratios between the two groups, with non-robbed flowers presenting higher reproductive outcomes. However, no effect on seed weight was detected among treatments. The data obtained suggest that in this species, nectar robbing has important indirect and negative effects on plant fecundity, through both male and female functions, due to a modification in the foraging behaviour of legitimate visitors.

Reciprocal style polymorphisms are not easily categorised: the case of heterostyly in Lithodora and Glandora (Boraginaceae)

Interest in reciprocal floral polymorphisms, such as heterostyly, has increased in recent decades because they can be used as suitable model systems to study mechanisms of outbreeding and disassortative mating in plants. Heterostylous plants are characterised by the presence of discrete morphs that differ in sex organ position and in some other ancillary traits. As regards sex organ deployment, different types of polymorphisms have been described, depending on number and type of discrete classes present in populations and degree of reciprocity between them. However, a clear-cut characterisation of stylar polymorphisms does not appear to be the best approach when there is great variability among populations because of continuous variation of some of traits examined. A recent study in Lithodora sensu lato (recently split into two separate genera, Lithodora and Glandora) showed a wide variation in sex organ position across species in the genus, which warrants precise population analysis of stylar polymorphism and its reciprocity. We provide a detailed morphometric analysis of flower sexual traits and include those considered to be ancillary characters. We report a wide variation in these traits in populations of Lithodora s.l. and highlight the subjectivity of the former characterisation of style polymorphism based on visual inspection. Ancillary traits appear repeatedly in Lithodora and Glandora, particularly in the latter. The appearance of these traits seems to be related to greater reciprocity between sexual whorls in Glandora, with the exception of G.xa0prostrata. These results agree with evolutionary steps proposed in the build-up of heterostyly according to some evolutionary models. We also examined variation in polymorphisms in light of current models for evolution of heterostyly, and, more specifically, we sought to verify the prediction that flower traits as a whole (i.e., flower integration) respond to selective pressure to assure the exact location of pollen on the pollinator body. Most reciprocal populations and species, where between-morph pollen transfer is expected to be higher, would show greater integration. Our results confirm this hypothesis.