Temporal and spatial patterns of seed dispersal in two Cistus species (Cistaceae)

Cistus species are obligate seeding, early colonizers that follow disturbance, particularly fire, in Mediterranean ecosystems. We studied seed release, seed dispersal and soil seed populations in stands of Cistus ladanifer and C. libanotis. Seed release started in mid- to late summer (C. ladanifer) or in early autumn (C libanotis), and continued for a very extended period: 8-10 months in C. ladanifer, and for a mean of 16 months in C. libanotis. The xerochastic capsules of both species released seeds by successive dehiscence of the locules. All capsules begin to dehisce simultaneously at the start of the seed release period, but in C. libanotis capsule fragmentation replaced dehiscence early in the seed release period. In plants of both species, seed shadows were characterized by a peak of density beneath the plant canopy and a very short tail of much lower densities, indicating that seeds are concentrated beneath mother plants when dispersed. Nevertheless, in late May, at the onset of the fire season, soil seed densities beneath plant canopies were low compared with densities expected from seed shadows, but were apparently high enough to allow recovery of the stands if a disturbance, such as fire, had taken place. Seed-eating Bruchidae in summer and granivorous ants during the seed release period were apparently the main causes of seed losses. Results suggest that in both Cistus species, the staggered seed release could constitute an efficient risk-reducing trait. The plant pool of seeds existing throughout most of the year could be a relevant component of Cistus seed banks.     

Intra- and interspecific variation in DNA content in Cistus (Cistaceae)

Flow cytometry, using propidium iodide and 4',6-diamidano-2-phenylindole staining, was used to estimate the nuclear DNA content (2C) and the proportion of A-T base pairs in 16 species of the Mediterranean genus Cistus. Genome sizes were shown to be constant within species, since no significant intraspecific variation in 2C DNA content was detected. At the genus level, up to about 1.5-fold differences in absolute DNA amounts were observed, ranging from 3.92 pg in C. crispus to 5.88 pg in C. monspeliensis. The (AT) : (GC) ratio was close to 1, and was similar for all species examined, ranging from 47.87% A-T content in C clusii, to 50.67% in C. populifolius. Pink-flowered species (subgenus Cistus) had lower DNA amounts than white-flowered species (subgenera Leucocistus and Halimioides). However, the distribution of DNA amounts in Cistus appeared to be continuous and did not permit a clear separation of infra-generic ranks in the genus.     

Phylogeny,biogeography, and morphological ancestral character reconstruction in the Mediterranean genus Fumana (Cistaceae)

Fumana is a diverse genus of the Cistaceae family, consisting of 21 currently accepted species. In this study, nuclear (ITS) and plastid (matK, trnT‐L) molecular markers were used to reconstruct the phylogeny and to estimate divergence times, including 19 species of Fumana. Phylogenetic analyses (Bayesian Inference, Maximum Parsimony and Maximum Likelihood) confirmed the monophyly of Fumana and did not support the infrageneric divisions previously established. The results support four main clades that group species that differ in vegetative and reproductive characters. Given the impossibility to define morphological characters common to all species within the clades, our proposal is to reject infrageneric divisions. Molecular dating and ancestral area analyses provide evidence for a Miocene diversification of the genus in the north‐western Mediterranean. Ancestral state reconstructions revealed ancestral character states for some traits related to xeric and arid habitats, suggesting a preadaptation to the Mediterranean climate.     

Time of germination and establishment success after fire of three obligate seeders in a Mediterranean shrubland of central Spain

Aim Determining how differences in time of germination can affect plant establishment in plant communities that, after a disturbance, must reestablish from seeds under climatic conditions subject to extremes, such as the Mediterranean. Although early germination may be beneficial for survival in summer, when drought is severe, this may expose the seedlings to winter extremes, thus to higher mortality. Understanding how sensitive is the establishment of different species to temporal patterns of germination will help to understand the factors that control species distribution and community stability in disturbance‐prone environments, as well as its sensitivity to changes in weather patterns as climate changes. Methods An experimental fire was made in early fall in an old Cistus–Erica shrubland in Toledo (central Spain). After fire, germination, survival and growth of the three dominant seeder species (Cistus ladanifer, Erica umbellata and Rosmarinus officinalis) were monitored during the first 3 years after fire. Seedlings were tagged to identify their time of emergence, and divided into cohorts according to their month of germination. Differences in survival of the various cohorts were evaluated by means of a Wilcoxon (Gehan) statistic. Height of surviving, tagged plants was compared among cohorts by means of a Kolmogorov–Smirnov test. Results The year following fire was one of the driest on record, while the next one was one of the wettest. Germination was more abundant during the first than during the second year. Establishment was mainly from first‐year germination, as the majority of second‐year germinated seedlings died. Temporal patterns of germination within a year and between years varied between species. Seedling mortality was highest immediately following germination, not in summer. Mortality was related to time of germination: during a given period of time, the mortality of younger seedlings was higher than that of older ones. However, survival was not highest for the first cohorts. In general, the earlier the seedlings germinated the more vigourous they became, more clearly so for Cistus than for Rosmarinus, but differences tended to disappear with time. Overall, time of germination varied between species and affected differently seedling survival and vigour of the various species. Rosmarinus and Cistus had sufficient survivors to reestablish the initial population. Erica, despite abundant germination, suffered a strong population reduction. Main conclusions Mediterranean shrub species differ in their temporal patterns of germination and survival after fire. The effect of time of germination is complex: germinating early is advantageous since old seedlings fared better than younger ones when confronted with the same rigours. However, germinating early might expose the seedlings to greater hazards and the first cohort might not survive best. The temporal window for establishment is narrow and mainly restricted to the first year after fire. Second year seedlings, irrespective of most favourable conditions, survived very little. Missing the window of establishment might virtually lead to a population collapse, despite having very high germination, as found for Erica.     

Hierarchical pre-dispersal fitness assessment in a Mediterranean shrub plant

Under the concept of modularity, it is possible to recognise how seed production, as well as any other process affecting it, are hierarchically structured within fruits, within individual plants and within populations. In this work, we analysed the effects of pre-dispersal seed predation by insects upon a set of hierarchical levels in a population of the Mediterranean shrub plant Cistus ladanifer (“rock rose”) throughout a complete fruit-producing season (which takes place during the summer months). Almost all individual plants were predated, which implies that the effects of predation at the population level (regardless of the extent of predation within each individual) were virtually uniform. Within the individuals, however, the predation rate was close to a proportion of 0.5 (half of the fruits of each individual were predated), which indicates that this hierarchical level is likely to be subjected to a differential action of selection. Predation rates within the fruits showed an intermediate value (lower than that observed at the population level but higher than that at the individual level). According to these results, the pressure of phenotypic selection may therefore give rise to greater variation among fruits of the same individual than among seeds of the same fruit. In terms of the temporal patterns observed there was a large variation in the increments of predation along the fruiting season, which implies a high degree of heterogeneity in the temporal distribution of the effects of predation pressure on fitness. Besides its use in the specific example of the plant species studied in this work, the methodological procedure presented in this paper (integration of the temporal changes of different hierarchical levels) might be foreseen, in fact, as a useful tool for analysing the hierarchical structuring of fitness in modular organisms in general. This procedure allows to discriminate and integrate selection pressures and their effects across different phenotypic levels, from the infra-individual ones up to the population level.     

Mating flight, metrosis, and semi-claustrality in the seed-harvester ant Pogonomyrmex salinus (Hymenoptera, Formicidae)

Here we examine dispersal, metrosis, and claustrality in the seed-harvester ant Pogonomyrmex salinus at an unusually large mating aggregation. We found that mode of queen dispersal from the mating aggregation is not a function of queen mass and that wing damage among queens was relatively rare. P. salinus is haplometrotic in the field and foundress queens placed together in forced associations eventually fight to the death. While queens of Pogonomyrmex salinus can survive claustrally, producing a single minim from their body reserves in the laboratory, fed queens produce up to four significantly larger minims along with concurrent larvae and pupae during the same period. Since queens forage in the field, we interpret claustrality as a secondary reserve strategy when foraging fails, and suggest that foraging is obligate for P. salinus queens in an overdispersed and temperate environment. Thus, nest founding strategies employed by P. salinus may be environmentally determined and represent a continuum between fully claustral and obligate foraging. We discuss our results with reference to theories of pleometrosis and claustral colony founding. Received 12 November 2004; revised 12 April 2004; accepted 29 July 2005.     

An experiment on ant predation in soil using a new bait trap method

To examine which species of ant are underground predators, we invented a simple bait trap using live mealworms as bait. A total of 75 bait traps were buried in soil at various depths (10, 20, 30 and 50 cm) to investigate the vertical distribution of predatory ants. The ants captured in approximately 50% of the traps were mostlyTetramorium caespitum andSolenopsis japonica. Solenopsis japonica was captured at greater depths (>30 m) thanT. caespitum. Eight kinds of soil invertebrate (the earthworm, wood louse, pill bug, millipede, adults of the dung beetle and carabid beetle, larvae of a cetoniine beetle and the earwig), placed in traps at a depth of 10 cm, varied greatly in attractiveness and vulnerability to ant predation. The earthworm and the wood louse were both attractive and vulnerable to ant predation, whereas the pill bug, the dung beetle and the millipede were attractive but not vulnerable. The larvae of a cetoniine beetle, the carabid beetle and the earwig were mostly unattractive.     

The role of seed traits as segregation factors of hybrids in wild populations of Cistus (Cistaceae)

Hybridization has been postulated as a main speciation mechanism in Cistus, a hard-seeded group of plants widely distributed in fire-prone Mediterranean shrublands. However, ecological evidence about how the segregation of hybrids from parents might occur is nonexistent. The presence of two hybrid populations in Morocco and Spain from Cistus albidus and Cistus heterophyllus led us to investigate their seed trait differences (seed size, mass and coat thickness) with the parentals and their seed germinability. A sowing experiment to compare the seedling emergence ability and seedling fitness of hybrids and their parentals was also carried out. Hybrid seeds germinated in a similar proportion to those of the parents. The hybrid seeds were significantly lighter, smaller and had thinner seed coats in both populations. However, these seed trait differences did not affect the seedling fitness of hybrids. These results were interpreted as a successful shift in the regeneration niche of the hybrids due to a greater proportion of soft-coated seeds, able to emerge from the soil seed bank in absence of fire. Smaller seeds also would favour further and deeper seed dispersal to escape from a fire. Monitoring of the seed yield of the Spanish population showed a competitive ability of hybrids.     

Substantial direct fitness gains of workers in a highly eusocial ant

Hamilton's theory of inclusive fitness suggests that helpers in animal societies gain fitness indirectly by increasing the reproductive performance of a related beneficiary. Helpers in cooperatively breeding birds, mammals and primitively eusocial wasps may additionally obtain direct fitness through inheriting the nest or mating partner of the former reproductive. Here, we show that also workers of a highly eusocial ant may achieve considerable direct fitness by producing males in both queenless and queenright colonies. We investigated the reproductive success of workers of the ant Temnothorax crassispinus in nature and the laboratory by dissecting workers and determining the origin of males by microsatellite analysis. We show that workers are capable of activating their ovaries and successfully producing their sons independently of the presence of a queen. Genotypes revealed that at least one fifth of the males in natural queenright colonies were not offspring of the queen. Most worker‐produced males could be assigned to workers that were unrelated to the queen, suggesting egg‐laying by drifting workers.     

Leaf-cutting ant nests support less dense and impoverished seed assemblages in a human-modified Caatinga dry forest

Regenerating forests make up an increasingly large portion of tropical landscapes worldwide and regeneration dynamics may be influenced by leaf-cutting ants (LCA), which proliferate in disturbed areas and collect seeds for fungus culturing. Here, we investigate how LCA influences seed fate in human-modified areas of Caatinga dry forest. We evaluate the seed deposition and predation on Atta opaciceps nests, foraging habitat surrounding nest and control habitat away of nest influence of 15 colonies located along a forest cover gradient during the rainy and dry seasons. For each habitat, four 50-cm² plots were established and all seeds on the soil surface were collected along 1 year. We recorded 13,628 seeds distributed among 47 species and 36.57% of the total seeds did not show any sign of predation. Nest mound habitats supported low-density and species-poor seed assemblages, which were taxonomically distinct from the control habitats. These effects only occurred in the rainy season. The proportion of undamaged seeds were similar across the habitats. While forest cover did not influence seed assemblage in terms of species richness or seed predation, it did interact with habitat type via increments in seed abundance as forest cover increased across the nests. Forest cover also affected seed composition, but only in the rainy season. These results indicate that LCA decrease seed deposition in areas under their influence, particularly on the nest mounds. As LCA profit from human disturbance in the Caatinga, their role as seed ‘sinks’ should be enhanced in disturbed Caatinga patches, particularly during the rainy season, when most of the plant recruitment occurs. Our findings reinforce the importance of LCA as drivers of forest dynamics and resilience in human-modified landscapes.     

Effects of season and population size on pollination and reproductive output in a Mediterranean shrub

• Pollinator guilds may change throughout extended flowering periods, affecting plant reproductive output, especially in seasonal climates. We hypothesised a seasonal shift in pollinator guild and an autumn reduction in pollinator abundance, especially in small and sparse populations.
• We recorded pollinator identity, abundance and behaviour in relation to flower density from plant to population throughout the extended flowering of Ononis tridentata. We evaluated female reproductive output by recording pollination success and pre‐dispersal seed predation in eight populations of contrasting size and density. Offspring quality was also characterised through seed weight and germination.
• A diverse guild of insects visited O. tridentata in spring, while only Apis mellifera was observed in autumn. Visitation frequency did not vary seasonally, but the number of flowers per foraging bout was lower, and seeds were heavier and had a higher germination rate in autumn. Plant and neighbourhood flowering display were not related to pollinator visitation frequency or behaviour. However, the rate of fertilised ovules, seed set and autumn flowering display size were positively related to population density.
• The maintenance of pollination in autumn enhances the reproductive performance of O. tridentata due to higher quality of autumn seed, and to a large reduction in seed predator pressure. We also suggest that observed changes in pollinator behaviour could be one of the processes behind seasonal variation in seed performance, since geitonogamous crosses were less likely to occur in autumn.

     

Ecophysiology of fire-stimulated seed germination in Cistus incanus ssp. creticus (L.) Hey wood and C. salvifolius L.

Abstract. Seed germination characteristics were investigated in the most common Cistus species in Greece, namely C. incanus ssp. creticus and C. salvifolius. In addition to the soft seed subpopulation, both species produce a large fraction of hardcoated, water-impermeable seeds which can be softened and, thus, promoted to germinate by mechanical scarification and thermal pretreatment. Temperature and light control of seed germination are unimportant. In the ecological context of the Mediterranean ecosystems, the eventually advantageous, opportunistic strategy of germination is based on: (a) seed heterospermy (which allows the smaller, softcoated fraction to germinate promptly each year while the majority of the seeds, the hard ones, accumulate in the soil); (b) the seed population heterogeneity in relation to coat hardness (so that any heat conditions produced by fire induce the softening and germination of a certain seed fraction); (c) the notably low germination rate (which suppresses premature germination); (d) the wide, Mediterranean-type (relatively cool), temperature range of germination (while higher temperatures simply inhibit but do not induce any dormancy); and (c) the apparent lack of photo-sensitivity (enabling germination under every light regime). In non-fire years, the temporal distribution of field germination and seedling appearance might be partly determined by the seed dispersal strategy of the individual Cistus species. Nevertheless, the post-fire regeneration response is manifested in the form of a huge wave of germination (of practically all seeds softened by the fire heat), shortly after the onset of the rainy season.     

The red imported fire ant,Solenopsis invicta,modifies predation at the soil surface and in cotton foliage

Red imported fire ants, Solenopsis invicta, are generalist predators that can have major impacts on foliar arthropod communities in agricultural systems; however, their effects as predators at the soil surface have not been adequately characterized. We examined the contribution of fire ants to predation at the soil surface and in cotton foliage at two sites and over the course of two field seasons in Georgia, using egg masses of the beet armyworm, Spodoptera exigua. To assess interactions between fire ants and other arthropod species, we also measured the densities of edaphic predators and honeydew‐producing hemipterans at both sites. The sites occurred in different growing regions (Piedmont and Coastal Plain), and allowed us to characterize the importance of fire ants as predators under different climatic and soil conditions. Fire ant suppression decreased egg predation at both field sites, and predation by fire ants at the soil surface was equal to if not greater than that in cotton foliage. However, the impact of fire ants on predation varied between sites, likely due to differences in climate and the composition and activity of the extant arthropod communities. Our study also indicates that fire ant suppression is associated with decreases in the density of honeydew‐producing insects, and increasing abundance of whiteflies on the plants coincided with a decrease in egg predation at the soil surface. This finding suggests the mutualism between ants and whiteflies may lead to a shift in predation intensity from edaphic towards plant‐based food webs.     

Female reproductive output in a Mediterranean shrub: effects from inflorescence to population

Inflorescence effects have been poorly studied, in spite of the functional relevance of the inflorescence in fruit and seed ecology. The present study focused on the effects of inflorescence size and phenology, and flower position within the inflorescence, in relation to fruit and seed production of the Mediterranean shrub Ononis fruticosa. Variability in fruit and seed production, seed weight and germination were estimated and modelled. Results confirmed that the most important predictors in seed production were inflorescence flowering time and flower position within the inflorescence. Thus, the number of mature seeds per fruit was higher in earlier inflorescences and in basal positions. On the other hand, predation was higher in fruits in basal positions. In fact, seed predation seemed to be the most important factor controlling final seed production. Models at the plant level suggested a negative incidence of geitonogamous pollination and resource limitation, which were also observed at the fruit level. This study confirmed the relevance of inflorescence effects on the reproductive output of O. fruticosa. Although the underlying processes could not be identified, our results provide several hypotheses for future experimental studies.     

Seed dispersal curve of a Mediterranean myrmecochore: Influence of ant size and the distance to nests

Euphorbia characias is a Mediterranean spurge with a diplochorous dispersal system: after a ballistic dispersal that scatters the seeds, some ant species find and retrieve the seeds to their nest (myrmecochorous dispersal). The seed dispersal curve generated by ants in an abandoned field was described and partitioned according to ant size and to the distance to nest entrance from where seeds fell after ballistic dispersal. Both variables (ant size, distance to nest) affected dispersal distance. The seed dispersal curve showed a peak at short distance (median=1m) and a tail extending to 9.4m. The peak and the tail are explained differently. Short distances are usually generated by small ants (Pheidole pallidula and Tapinoma nigerrimum; 0.56±0.41m [n=48]) both from the nearest or farther nest entrances. The tail of the curve is generated disproportionately by big ants (Aphaenogaster senilis and Messor barbarus; 2.09±1.71m [n=61]) from farther nests. Seeds have a much greater probability (P=0.734) of being transported to nests which are not the nearest. This effect is largely due to transportation by big ants.     

Species richness and composition assessment of spiders in a Mediterranean scrubland

Intensive fieldwork has been undertaken in Portugal in order to develop a standardized and optimized sampling protocol for Mediterranean spiders. The present study had the objectives of testing the use of semi-quantitative sampling for obtaining an exhaustive species richness assessment of spiders and testing the effects of day, time of day, collector and sampling method on the collected species richness and composition of a Mediterranean scrubland. The collecting summed 224 samples corresponding to one person-hour of effective fieldwork each. In total, 115 species were captured, of which 110 were recorded inside a delimited one-hectare plot, corresponding to more than 70% of the about 160 estimated species. Although no estimator reached the asymptote, the Michaelis-Menten curve behaviour indicates that the estimated richness should be accurate. Most different sampling approaches (day, time of day, collector and sampling method) were found to influence richness, abundance or composition of the samples to some extent, although sampling method had the strongest influence whereas “collector” showed no effect at all. The results support the idea that the only variables that need to be controlled in similar protocols are the sampling methods and the time of day when each method is executed. We conclude that populations in structurally simple habitats present narrower peaks of adult abundance, which implies higher percentages of juveniles in samples. Finally, results also indicate that habitats with a relatively simple structure like scrublands may require as much sampling effort, in order to reach similar proportions of captured species in relation to the estimated richness, as habitats that are much more complex.     

Effect of ant predation and abiotic factors on the mortality of medfly larvae,Ceratitis capitata,in the Argan forest of Western Morocco

The Argan Argania spinosa (L.) Skeels (Ericales: Sapotaceae) is an endemic and emblematic tree growing in the centre and the southwest of Morocco. Argan fruits are frequently infested by the Mediterranean fruit fly Ceratitis capitata Wied (Diptera: Tephritidae). To date, no control program has been undertaken in the Argan forest. This research is the first investigation of natural mortality factors of C. capitata larvae in the Argan forest. The study was conducted at two localities near the city of Essaouira with different climatic conditions. Observations were conducted using 260 late instar larvae which were individually deposited on the ground, under fruiting host trees, where they naturally fall to find a suitable pupation site. Overall, 42% of the larvae died before being able to burrow into the ground, irrespectively of the location. Larval survival and their likelihood of burrowing decreased with increasing ground temperature, as 53% of all the larvae deaths occurred at temperatures over 48°C. However, at lower ground temperature, predation by ants and spiders accounted for 47% of all mortality. Four species of ants carried out 94% of the captures. Monomorium subopacum Mayr (Hymenoptera: Formicidae), which frequently forages under Argan trees, was by far the most efficient predator, due to a powerful sting that rapidly immobilizes the prey. Our results suggest that the burrowing performance of larvae is constrained by high thermal conditions and the presence of ant predators at lower temperatures.     

Multiple Recruitment Limitation Causes Arrested Succession in Mediterranean Cork Oak Systems

Lack of tree regeneration and persistency of species-poor shrublands represent a growing problem across Mediterranean evergreen oak forests. What constrains forest regeneration is poorly understood, and restoration attempts have been largely unsuccessful. We assessed the contribution of four different mechanisms of tree recruitment limitation (that is, source, dispersal, germination, and establishment) in a cork oak (Quercus suber) system in southern Portugal. Using a combination of field studies and experiments, we quantified seed production, seed removal and dispersal, seed survival and germination, seedling establishment and survival, as well as cork oak natural regeneration for the three dominant vegetation types in this system (Cistus ladanifer shrubland, oak forest, and oak savanna). We found that all four forms of cork oak recruitment limitation were significantly more severe in shrublands than in oak forests and savannas, so that oak seedling recruitment in shrubland was impeded in multiple ways. Our results explain why transitions from shrublands to oak savannas and forests are extremely difficult, and that the release from arrested succession in this system requires the simultaneous relief of multiple constraints on recruitment limitation in the early life history of oaks. These results have important implications for the restoration and conservation of Mediterranean oak systems.