Carlos Lara

Specialization in Plant-Hummingbird Networks Is Associated with Species Richness, Contemporary Precipitation and Quaternary Climate-Change Velocity

Large-scale geographical patterns of biotic specialization and the underlying drivers are poorly understood, but it is widely believed that climate plays an important role in determining specialization. As climate-driven range dynamics should diminish local adaptations and favor generalization, one hypothesis is that contemporary biotic specialization is determined by the degree of past climatic instability, primarily Quaternary climate-change velocity. Other prominent hypotheses predict that either contemporary climate or species richness affect biotic specialization. To gain insight into geographical patterns of contemporary biotic specialization and its drivers, we use network analysis to determine the degree of specialization in plant-hummingbird mutualistic networks sampled at 31 localities, spanning a wide range of climate regimes across the Americas. We found greater biotic specialization at lower latitudes, with latitude explaining 20–22% of the spatial variation in plant-hummingbird specialization. Potential drivers of specialization - contemporary climate, Quaternary climate-change velocity, and species richness - had superior explanatory power, together explaining 53–64% of the variation in specialization. Notably, our data provides empirical evidence for the hypothesized roles of species richness, contemporary precipitation and Quaternary climate-change velocity as key predictors of biotic specialization, whereas contemporary temperature and seasonality seem unimportant in determining specialization. These results suggest that both ecological and evolutionary processes at Quaternary time scales can be important in driving large-scale geographical patterns of contemporary biotic specialization, at least for co-evolved systems such as plant-hummingbird networks.

Preferential nectar robbing of flowers with long corollas: experimental studies of two hummingbird species visiting three plant species

Long flower tubes have been traditionally viewed as the result of coevolution between plants and specialized, legitimate, long billed-pollinators. However, nectar robbers may have played a role in selection acting on corolla length. This study evaluated whether hummingbirds are more likely to rob flowers with longer corollas from which they cannot efficiently extract nectar with legitimate visits. We compared two hummingbird species with similar bill lengths (Lampornis amethystinus and Colibri thalassinus) visiting floral arrays of artificial flowers with exaggerated corolla lengths, and also evaluated how the birds extract nectar rewards from medium to long corollas of three hummingbird-pollinated plants (Salvia mexicana, S. iodantha and Ipomoea hederifolia). The consequences of foraging for plant fitness were evaluated in terms of seed production per flower. Variation in seed production after legitimate visits of hummingbird-pollinated plants was mostly explained by differences in pollinator effectiveness. Seed production did not increase with the number of legitimate visits to a flower, except in I. hederifolia. We found that birds were more likely to rob both artificial and natural flowers with long corolla tubes. Nectar robbing was not observed on short-corolla flowers of Salvia spp., but robbing negatively affected seed production of long-tubed flowers of I. hederifolia. Significant differences between hummingbird species in the use of this behavior were observed, but males and females behaved alike. We suggest that short-billed hummingbirds with enlarged bill serrations (the edge of both tomia finely toothed) may have an advantage in illegitimately feeding at long-corolla flowers. This raises the possibility of counter-selection on increasing corolla length by nectar robbers.

Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. II. Attracting and rewarding mutualistic and antagonistic visitors

By definition, the floral morphs of distylous plants differ in floral architecture. Yet, because cross-pollination is necessary for reproductive success in both morphs, they should not differ in attributes that contribute to attracting and rewarding floral visitors. Floral and vegetative attributes that function in distylous polymorphism in hummingbird-pollinated Palicourea padifolia (Rubiaceae) and the responses of pollinators and insect herbivores to the resources offered by both morphs were investigated. The performance of each morph along multiple stages of the reproductive cycle, from inflorescence and nectar production to fruit production, was surveyed, and pollinator behavior and nectar standing crops were then observed. Costs associated with such attractiveness were also evaluated in terms of herbivore attack and of plant reproductive fitness (female function) as a function of leaf herbivory. The number of inflorescences, floral buds, open flowers, and ripe fruits offered by either floral morph were similar, but short-styled plants almost doubled the number of developing fruits of long-styled plants. Long-styled flowers produced higher nectar volumes and accumulated more nectar over time than short-styled flowers. Measures of nectar standing crop and data on pollinator behavior suggest that hummingbirds respond to this morph-specific scheduling of nectar production. Lastly, long-styled plants suffered a higher herbivore attack and lost more leaf area over time than those with short-styled flowers. Herbivory was negatively correlated with fruit number and fruit mass, and long-styled plants set significantly less fruit mass than short-styled plants. The results suggest that pollinators and herbivores may exert selective pressures on floral and vegetative traits that could also influence gender function.

Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus

We investigated whether an immune response is associated with growth, female reproduction and survival costs in the house cricket. Using different intensities of challenge immune (implantation of one piece of nylon (1N) and two nylons (2N), with their respective sham-challenge and control groups) with body size and exoskeleton thickness as response variables, growth costs were determined for both sexes. A similar methodology was followed for reproduction costs, in which egg number and size, and female survival were measured as response variables. It was also determined whether mated and virgin females showed different immune responses. Body size decreased with immune challenge but only in the 2N treatment. Exoskeleton thickness increased in both sham-challenge groups and the 1N group but decreased in the 2N group. Egg number decreased more in the sham-challenge groups followed by the 1N and 2N groups. The 2N group showed the largest egg size at the end of the experiment. In these females, 2N group died first followed by the 1N, two nylon sham and one nylon sham groups. Finally, mated females showed a lower immune response than virgin females. These results are consistent with ecological immunity theory. The discovery of exoskeleton-related costs of immunity and injury may have important implications for experimental design in studies of the cost of immunity.

Hummingbirds as vectors of fungal spores in Moussonia deppeana (Gesneriaceae): taking advantage of a mutualism?

Hummingbirds act as vectors of Fusarium moniliforme spores on protandrous flowers of Moussonia deppeana. The resulting interactions between the pathogen and plant-pollinator interactions were investigated in a 4-yr study to determine the pathogens impact on host flowering phenology, flower longevity, nectar production, and fruit and seed production. We also evaluated hummingbird behavior on healthy and diseased plants and its effectiveness on spore transmission. Individual plants expressed the disease from year to year, and new infected individuals were detected every year. A fraction of the flowers in a plant expressed the disease, and this varied among and within years. Diseased plants produced more inflorescences, buds, and open healthy flowers than did healthy plants. Further, diseased plants bore proportionally fewer pistillate flowers than did healthy plants when considering only healthy flowers. Neither nectar nor fruit production differed between healthy and diseased plants, but healthy plants produced more seeds. Infected flowers were retained longer than uninfected ones, producing an additional 2 mg · μL(-1) · flower(-1) of nectar sugar. Hummingbirds visited more flowers on diseased plants than they did on healthy plants, regardless of number and sexual phase. Most pollen and spores were deposited within plants. These behavioral outcomes may promote geitonogamy and limit fungal spore mixing.

Nectar replenishment and pollen receipt interact in their effects on seed production of Penstemon roseus

Resource supply and pollen delivery are often thought to equally limit seed production in animal-pollinated plants. At equilibrium, plants should show no response to experimental pollen supplementation because resources limit seed set above the current level of pollen attraction, while experimental reduction in pollen deposition below the equilibrium level would reduce seed set. The predicted equilibrium may be disrupted, however, if plants expend additional energy to replenish removed nectar. We investigated the combined effects of nectar removal and pollen delivery on female reproductive success of Penstemon roseus (Plantaginaceae), a hummingbird-pollinated plant that replenishes removed nectar. We first documented that the frequency of experimental nectar removal was correlated with total nectar secretion; and increased frequency of nectar removal resulted in increased female reproductive costs to the plant. Trade-offs between investing resources in nectar and investing resources in seeds were then investigated in two contrasting natural populations by removing nectar from flowers at increasing frequencies while simultaneously hand-pollinating flowers with increasing amounts of pollen. Seed set was lowest at low levels of pollen deposition, highest at medium-sized pollen loads, and intermediate when pollen loads were highest. At both sites, the frequency of nectar removal and pollen deposition had an interactive effect on seed production, in that intermediate levels of nectar removal result in the absolute highest seed set, but only at intermediate pollen loads. At high pollen loads, seed set was higher following little to no nectar removal, and at low pollen loads, all rates of nectar removal affected fecundity equally. Seed mass responded to nectar removal and pollination differently than did seed set. High levels of nectar removal and pollen delivery both lowered seed mass, with little interaction between main effects. Our findings are among the first to demonstrate that nectar replenishment costs and pollination intensity jointly affect seed production. This conflict between nectar replenishment costs and pollen-limiting factors results in trade-offs between pollinator attraction and seed provisioning. Thus, resource allocation towards nectar production should more often be considered in future studies of pollen limitation.

Provenance, guts, and fate: field and experimental evidence in a host-mistletoe-bird system.

Abstract: Theory suggests that host—parasite interaction should lead to local adaptation of parasites to their host. In mistletoe— host tree interactions the foraging patterns of fruit-eating birds can play an important role in host local adaptation, depending on the tree species on which the mistletoe fruits were consumed (host provenance) and the tree species on which the mistletoe seeds were deposited (host fate). Yet this interaction has not been previously documented. To determine the effects of host provenance, bird gut processing, and host fate on mistletoe seed germination and seedling establishment of Psittacanthus calyculatus, we conducted a seed inoculation experiment in Tlaxcala, Mexico. Mistletoe fruits were collected from Crataegus pubescens (Cp), Prunus serotina (Ps), and Salix bonplandiana (Sb) and measured. We then manually removed the exocarp and pulp of half the fruits, and the other half were given to grey silky-flycatchers (Ptilogonys cinereus) for gut processing. Obtained seeds of both groups of fruits were measured and deposited on branches of other trees of the same 3 host species in a full factorial design. Mistletoe fruit size varied significantly among host tree species, but differences did not coincide with those in gut retention time. Bird gut processing and the host provenance × host fate interaction were the best predictors for the occurrence of germination and establishment of seedlings. Seed germination and seedling establishment were more likely when seeds were gut processed by birds, but gut retention time had no significant effects. The significant host provenance × host fate interaction was largely due to higher success of mistletoe seeds from Sb to Sb and lower success from Sb to Ps. Our results suggest that to understand the efficiency of infection of P. calyculatus and possibly other mistletoe species, the linked effects of the digestive processes undergone by mistletoe seeds and the species of host trees where the seeds were consumed and ultimately deposited should be considered. Nomenclature: Kuijt, 2009.

Pollination ecology of Penstemon roseus (Plantaginaceae), an endemic perennial shifted toward hummingbird specialization?

SummaryPink-flowered tubular Penstemon roseus (Plantaginaceae), which has shifted partially to hummingbird pollination, blooms on high-elevation slopes in the mountains in Tlaxcala, Mexico. We studied the interactions between pollinator visitation rates to flowers, pollen removal and deposition, flower size, and nectar removal frequency on seed production in P. roseus. We combine observational and experimental studies in two contrasting natural populations. Our manual pollinations revealed that P. roseus is fully self-compatible. Autonomous self- and manual self-pollinated flowers matured as many seeds as when outcrossed, but outcrossing seems to become better than selfing as the flowering season progressed. Early in the season flowers that were bagged and hand-selfed, hand-outcrossed, or autonomously selfed, or unbagged and naturally pollinated had equal seed set in all four treatments. But later in the season, outcross pollen gave approximately twice as much seed set as the two self-treatments. Low levels of pollen receipt and pollen removal were consistent with the long time elapsed for a given plant to be visited by hummingbirds, which suggests pollen shortage in both sites. Despite differences in pollinator visitation rates to flowers, probability of flower visitation, removal and deposition of pollen, and nectar production rates between populations, we found that total nectar production had no effect on seed production at either site. The daily nectar secretion rate of 0.3–0.65 mg sugar per flower per 1–3 days was low relative to other hummingbird-adapted Penstemon species (typical range: 1.5–5 mg sugar per flower), and it might be intermediate between hummingbird- and bee-adapted Penstemon flowers. Our results support the hypothesis about a shift toward hummingbird pollination, and provide an example of a ‘despecialized’ Penstemon species, which attracts high-energy pollinators (hummingbirds) and profits from outcrossing, but retains bee-syndrome floral traits and low sugar production rates.

Nectar removal effects on seed production in Moussonia deppeana (Gesneriaceae), a hummingbird-pollinated shrub 1

ABSTRACT Animal-pollinated angiosperm plants that respond positively to nectar removal by replenishment invest energy that can entail a reproductive cost. Here we use nectar removal manipulation to investigate whether nectar removal increases total nectar production in Moussonia deppeana (Gesneriaceae) and to see if this leads to lower seed production. We found that flowers strongly respond to increased nectar removal by producing 2–4 times as much additional nectar. Other nectar removal treatments had little effect on nectar production and rule out alternative explanations at the flower level. Compared with open-pollinated flowers, hand cross-pollination yielded similar seed production in flowers with experimentally increased nectar removal. Although flower-level effects of nectar replenishment on seed production were not detected in M. deppeana, costs of nectar replenishment need further study as tradeoffs between nectar production and seed production could be expressed at the plant level and/or as long-term effects. Nomenclature: Wiehler, 1975; 1982.

Reproductive ecology and isolation of Psittacanthus calyculatus and P. auriculatus mistletoes (Loranthaceae)

Background Relationships between floral biology and pollinator behavior are important to understanding species diversity of hemiparasitic Psittacanthus mistletoes (c. 120 species). We aimed to investigate trait divergence linked to pollinator attraction and reproductive isolation (RI) in two hummingbird-pollinated and bird-dispersed Psittacanthus species with range overlap. Methods We investigated the phylogenetic relationships, floral biology, pollinator assemblages, seed dispersers and host usage, and the breeding system and female reproductive success of two sympatric populations of P. calyculatus and P. auriculatus, and one allopatric population of P. calyculatus. Flowers in sympatry were also reciprocally pollinated to assess a post-mating component of RI. Results Hummingbird assemblages differed between calyculatus populations, while allopatric plants of calyculatus opened more but smaller flowers with longer lifespans and produced less nectar than those in sympatry. Bayesian-based phylogenetic analysis indicated monophyly for calyculatus populations (i.e. both populations belong to the same species). In sympatry, calyculatus plants opened more and larger flowers with longer lifespans and produced same nectar volume than those of auriculatus; populations shared pollinators but seed dispersers and host usage differed between species. Nectar standing crops differed between sympatric populations, with lower visitation in calyculatus. Hand pollination experiments indicated a predominant outcrossing breeding system, with fruit set after interspecific pollination two times higher from calyculatus to auriculatus than in the opposite direction. Conclusions Given the low genetic differentiation between calyculatus populations, observed trait divergence could have resulted from changes regarding the local communities of pollinators and, therefore, expected divergence for peripheral, allopatric populations. Using RI estimates, there were fewer heterospecific matings than expected by chance in P. calyculatus (RI4A = 0.629) as compared to P. auriculatus (RI4A = 0.20). When considering other factors of ecological isolation that affect co-occurrence, the RI4C values indicate that isolation by hummingbird pollinators was less effective (0.20) than isolation by host tree species and seed dispersers (0.80 and 0.60, respectively), suggesting that host usage is the most important ecological isolation factor between the two species. Accordingly, the absolute and relative cumulative strength values indicated that the host tree species’ barrier is currently contributing the most to maintaining these species in sympatry.