Rodrigo Medel

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.

POLLINATOR-MEDIATED SELECTION ON THE NECTAR GUIDE PHENOTYPE IN THE ANDEAN MONKEY FLOWER, MIMULUS LUTEUS

Mimulus luteus (Scrophulariaceae) is a perennial herb occurring in the South American Andes that shows a wide variation in the size and shape of a red spot on the lower lobe of the yellow flower. We describe the preference of four insects (three bees and one butterfly) and one hummingbird species for floral characters, and estimated the strength, direction, and form of pollinator-mediated selection through female fitness. We applied geometric morphometrics to describe the preference of pollinator species for different guide shapes. Our results revealed striking differences in the floral phenotypes preferred by insects and hummingbirds. Insects visited flowers with corollas 1.25-fold larger and guides 1.72-fold larger than the hummingbird species did. While insects preferred flowers with nectar guides pointing toward the corolla tube, the hummingbird preferred flowers with heart-shaped nectar guides. Most of the floral preferences shown by pollinators translated into significant linear and nonlinear selection coefficients. When selection was analyzed on a per-flower basis and for female fitness, corolla size was under positive directional selection, and nectar guide size and shape were under disruptive selection. Because the insect and hummingbird pollinators showed a strong segregation in their daily activity time, we suggest that current disruptive selection on the nectar guide phenotype can result from the differential availability of the rewarding floral variants over a day. Our findings suggest that pollinator-mediated selection favoring extreme phenotypes in M. luteus may not only contribute to high nectar guide variation found in this species, but also can promote divergence of corolla and nectar guide traits.

Ancestral reconstruction of flower morphology and pollination systems in Schizanthus (Solanaceae)

Concerted changes in flower morphology and pollinators provide strong evidence on adaptive evolution. Schizanthus (Solanaceae) has zygomorphic flowers and consists of 12 species of annual or biennial herbs that are distributed mainly in Chile and characterized by bee-, hummingbird-, and moth-pollination syndromes. To infer whether flowers diversified in relation to pollinator shifts, we traced the evolutionary trajectory of flower traits and visitors onto a phylogeny based on sequence data from ITS, waxy, and trnF/ndhJ DNA. Maximum-likelihood ancestral reconstruction of floral traits suggests that ancestral Schizanthus had a bee-pollination syndrome. The hummingbird syndrome evolved in S. grahamii, a high elevation species in the Andes. The moth syndrome evolved in the ancestor of three species that inhabit the Atacama Desert. Results of mapping flower visitors onto the phylogeny show that the shift from bee to hummingbird pollination concurred with a shift in pollinators as predicted by the syndromes. However, the same pattern was not found for the moth syndrome. Visits by moths were observed only in one of the three moth-syndrome species, and at a very low rate. This mismatch suggests either anachronic floral characters or maintenance of rare, imperceptible moth pollination backed up by capacity for autonomous selfing. Overall, results suggest that diversification of flower traits in Schizanthus has occurred in relation to pollinator shifts.

Phylogenetic analysis of floral integration in Schizanthus (Solanaceae): does pollination truly integrate corolla traits?

To assess whether floral integration patterns result from the action of pollinator selection on functionally related traits, we compared corolla integration patterns in eight Schizanthus species differing in pollination systems and in their degree of pollinator dependence across a molecular phylogeny. Integration patterns differed among species and these differences were not related to their phylogenetic relatedness. When the putative original function of some corolla traits was lost in pollinator‐dependent species, the integration among nonfunctional characters and the rest of the corolla traits was disrupted. This pattern was not presented in species adapted for late autonomous selfing, which exhibited higher corolla integration than their pollinator‐dependent relatives. These results suggest that corolla integration in pollinator‐dependent species was shaped by pollinator‐mediated selection. Decoupling of nonfunctional traits in these species may result from a relaxation of correlational selection or from selection acting against a default covariation provided by genetic and developmental connections.

Effects of vector behavior and host resistance on mistletoe aggregation

Understanding the factors affecting parasite aggregation in natural host pop- ulations is one of the central questions in parasite ecology. While different biological mechanisms giving rise to aggregation have been documented in the literature, the role of established parasites in vector attraction, and its importance in determining clumped parasite distributions has received less attention. In a two-year field study, we evaluated the im- portance of a bird vector, Mimus thenca (Mimidae), on the aggregation dynamics of the holoparasitic mistletoe, Tristerix aphyllus, on its cactus host, Echinopsis chilensis. Removal of T. aphyllus from cacti decreased the number of visits and the time spent by the bird vector, which resulted in a 3.5-fold lower seed deposition of the mistletoe on experimental hosts than on control hosts. Vector preference, however, was not the only factor affecting aggregation in this system. Spine length of the cactus acted as a first line of defense against parasitism, by discouraging bird perching on top of host columns. While heavily parasitized hosts received more seeds than unparasitized hosts, spines counteracted this effect. These results provide field evidence that parasite aggregation results from the balance between vector behavior and host resistance traits.

Effects of sampling completeness on the structure of plant—pollinator networks

Plant-animal interaction networks provide important information on community organization. One of the most critical assumptions of network analysis is that the observed interaction patterns constitute an adequate sample of the set of interactions present in plant-animal communities. In spite of its importance, few studies have evaluated this assumption, and in consequence, there is no consensus on the sensitivity of network metrics to sampling methodological shortcomings. In this study we examined how variation in sampling completeness influences the estimation of six network metrics frequently used in the literature (connectance, nestedness, modularity, robustness to species loss, path length, and centralization). We analyzed data of 186 flowering plants and 336 pollinator species in 10 networks from a forest-fragmented system in central Chile. Using species-based accumulation curves, we estimated the deviation of network metrics in undersampled communities with respect to exhaustively sampled communities and the effect of network size and sampling evenness on network metrics. Our results indicate that: (1) most metrics were affected by sampling completeness but differed in their sensitivity to sampling effort; (2) nestedness, modularity, and robustness to species loss were less influenced by insufficient sampling than connectance, path length, and centralization; (3) robustness was mildly influenced by sampling evenness. These results caution studies that summarize information from databases with high, or unknown, heterogeneity in sampling effort per species and should stimulate researchers to report sampling intensity to standardize its effects in the search for broad patterns in plant-pollinator networks.

Assessment of parasite-mediated selection in a host-parasite system in plants.

A two-year field study was conducted to evaluate the potential of two cactus species, Echinopsis chilensis and Eulychnia acida, to evolve defensive traits against the parasitic mistletoe Tristerix aphyllus (Loranthaceae). The adaptive value of host traits against parasitism was inferred through: (1) identification of the relevant characters of cacti to prevent infection, (2) evaluation of the fitness impact of parasitism on cacti, and (3) estimation of the linear and nonlinear selection coefficients on the relevant characters. Different lines of experimental and correlative evidence indicated that spine length was important in preventing individuals of the two cactus species from becoming parasitized. However, the impact of the mistletoe on cactus fecundity was contingent on the species involved. Even though parasitism decreased fruit production, seed number per fruit, and the total seed output in E. chilensis, low and nonsignificant linear and nonlinear gradients of selection were prevalent in this speci...

Pollinator‐mediated selection in a specialized pollination system: matches and mismatches across populations

Most studies on pollinator‐mediated selection have been performed in generalized rather than specialized pollination systems. This situation has impeded evaluation of the extent to which selection acts on attraction or specialized key floral traits involved in the plant‐pollinator phenotypic interphase. We studied pollinator‐mediated selection in four populations of Nierembergia linariifolia, a self‐incompatible and oil‐secreting plant pollinated exclusively by oil‐collecting bees. We evaluated whether floral traits experience variable selection among populations and whether attraction and fit traits are heterogeneously selected across populations. Populations differed in every flower trait and selection was consistently observed for corolla size and flower shape, two traits involved in the first steps of the pollination process. However, we found no selection acting on mechanical‐fit traits. The observation that selection occurred upon attraction rather than mechanical‐fit traits, suggests that plants are not currently evolving fine‐tuned morphological adaptations to local pollinators and that phenotypic matching is not necessarily an expected outcome in this specialized pollination system.

Floral Herbivory Affects Female Reproductive Success and Pollinator Visitation in the Perennial Herb Alstroemeria ligtu (Alstroemeriaceae)

Floral damage can reduce flower attractiveness for pollinator service. However, the reproductive impact of flower herbivory may be contingent on a petal that is damaged. Flowers having nectar guides are expected to suffer reduction in reproductive success when damage is concentrated on these structures compared to petals less involved in pollinator attraction. In this study, we recorded the reflectance pattern of distinctive yellow tepals of Alstroemeria ligtu and examined their functional role for pollinator attraction and reproductive success. We quantified the richness and abundance of pollinator species attracted to flowers and estimated fruit set and seed production in flowers subject to (1) nectar guide removal, (2) lateral red tepal removal, and (3) unmanipulated flowers. Results indicate that nectar guide removal reduced pollinator visitation rate but did not affect community-level descriptors such as pollinator species richness and flower diversity. The reduction in visitation rate translated into a reduced fruit set and seed production, hence confirming that nectar guides have a clear functional role in the pollination process. We conclude that the location where damage occurs is a relevant factor for pollinator attraction and subsequent reproductive success in this species, suggesting that nectar guide damage may disrupt fine-tuned plant-pollinator communication systems.

Factors affecting pollinator movement and plant fitness in a specialized pollination system

The rate of pollen exchange within and among flowers may depend on pollinator attraction traits such as floral display size and flowering plant density. Variations in these traits may influence pollinator movements, pollen receipt, and seed number. To assess how floral display size and flowering plant density affect parameters of pollinator visitation rate, pollen receipt per flower, seed number per fruit and the between-plant pollinator movements, we studied the self-incompatible plant, Nierembergia linariifolia. Per-flower pollinator visitation rate and bout length increased linearly with increasing floral display size. Pollen receipt per flower increased linearly with increasing flowering plant density. For seed number per fruit, a polynomial model describing an increased seed number per fruit at low density and a decreased seed number per fruit at high density provided a significant fit. Per-flower pollinator visitation rate was not associated with pollen receipt per flower and seed number per fruit. Bees visited plants located near to the center of the population more frequently than plants located at the periphery. Increases in both floral display size and flowering plant density led to an increased chance of a plant being chosen as the center of the pollinator foraging area. These results suggest that even though large floral displays and high flowering plant density are traits that attract more pollinators, they may also reduce potential mate diversity by restricting pollen movement to conspecific mates that are closely located.