Opportunistic pollination by birds and lizards in the Canary Islands

  1. María Candelaria Rodríguez Rodríguez
Supervised by:
  1. Alfredo Valido Amador Director
  2. Diego Jordano Director
  3. José María Fernández-Palacios Martínez Tutor

Defence university: Universidad de La Laguna

Year of defence: 2016

  1. Esperanza Beltrán-Tejera Chair
  2. José María Gómez Reyes Secretary
  3. Jens Olesen Committee member
  1. Botánica, Ecología y Fisiología Vegetal

Type: Thesis

Teseo: 402962 DIALNET


The consequences of mutualistic plant-animal interactions on plant reproductive success depend on the animal’s effectiveness and the context in which the mutualism occurs. The present thesis is about the interplay between these two aspects in the mutualism of pollination. We try to meet the challenge with a particular group of pollinators, opportunistic nectar-feeding vertebrates, in a particular context, oceanic islands. Due to their intrinsic ecological conditions, oceanic islands favour the appearance of depauperate and disharmonic assemblages of opportunistic pollinators, whose effectiveness and level of context dependence may differ significantly from those of continental systems. In the concrete case of the Canary Islands, passerine birds and lacertid lizards are frequent floral visitors of native flora, but their pollination ecology has remained almost unknown. For this reason, the present thesis follows a dual objective: first to experimentally demonstrate the effectiveness of birds and lizards as pollinators (chapters 2-3) and analyse the potential differences between both functional groups (chapter 4), to then understand how their benefits on plant fitness vary under the presence of antagonists (chapters 5-6). Concretely, we pose the following questions: Are opportunistic vertebrates effective pollinators of the Canarian flora despite of their generalized diet (chapters 2-3)? To answer it, we chose two of the most representative bird-flower elements from the archipelago, the endemic plant species Isoplexis canariensis (Scrophulariaceae, chapter 2) and Canarina canariensis (Campanulaceae, chapter 3). As a basic step to understand the role of vertebrates on their sexual reproduction, we studied the breeding system of both species using experimental hand pollinations. The identity of floral visitors and visitation frequency were estimated by focal censuses, and their effectiveness by selective exclosures. We found that both species are self-compatible, but floral visitation by vertebrates enhances the production of fruits and viable seeds, especially by birds. Invertebrates were also frequent visitors, at least in C. canariensis, but their visits produced levels of female fitness similar (C. canariensis) or lower (I. canariensis) to spontaneous autogamy, indicating that they predominantly act as detrimental agents. Our results demonstrate that studied species crucially depend on opportunistic vertebrates for sexual reproduction, being the first time that vertebrate pollination has been empirically demonstrated in the Canarian archipelago. Do members of opportunistic vertebrate assemblages differ in their effectiveness as pollinators (chapter 4)? For this question, we dissect pollination effectiveness for birds and lizards on I. canariensis into its quantitative and qualitative components. Quantity was defined as the product of visitation rate per 30 min per plant and the number of flowers probed per plant visit. Quality was estimated as the proportion of pollen grains removed per anther (male fitness), added to the product of fruit set and the proportion of viable seeds produced per fruit (female fitness) resulting from a single floral visit. We found that the taxonomical identity of pollinators drives differences in quantitative effectiveness, while intraspecific aspects such as pollinator’s age (lizards) drive differences in qualitative effectiveness. Most of variation in effectiveness was found in visitation frequency (both lizards and birds), number of flowers probed (lizards) and proportion of viable seeds (birds). The marked differences among and within pollinator species made the insular assemblage limited in functional equivalence, a potential signal of its fragility against disturbances. How variable are the effects of multispecific assemblages across space and, how do they contribute to the spatial structure of plant reproductive success within the plant population (chapter 5)? Once analysed the effects of the pollinator assemblage on plant fitness of I. canariensis, we evaluated how their reproductive benefits vary spatially under the presence of antagonists. For this, we characterize the spatial structure of mutualistic and antagonistic interaction strengths using spatially explicit models. We estimated interaction strength as the frequency with which the specific guild interacted with individual plants, multiplied by its intensity. We found that both interaction types are spatially structured, but negatively correlated with each other. Given that both functional groups have a significant impact on plant reproductive success, the reproductive landscape results from a compromise between the simultaneous influence by both mutualists and antagonists. In consequence, plant fitness emerges as a mosaic of reproductive coldspots and hotspots, which corresponds to plants severely damaged by antagonists but weakly benefited by pollinators (coldspots) and vice versa (hotspots). Our results suggest that the spatial dynamics of plant reproduction derives from sequential processes in which the first plant-animal interaction’s modification of the floral phenotype (i.e. florivores) has consequences for subsequent interactions of the plant with the animals (i.e. pollinators). And finally, how does spatial variation in plant reproductive success emerge from the overrepresentation of certain animal interacting assemblages across individual plants (chapter 6)? After analysing the spatial structure in plant reproductive success of I. canariensis, we tested if this structure emerged from any pattern in the distribution of mutualistic and antagonistic interactions among plants, or from a random distribution of these interactions in the population. With the help of complex network theory, we characterized the interacting animal assemblage of each plant, and classified all individuals along an interaction gradient that ranged from plants with fully mutualistic assemblages to plants that interacted exclusively with antagonists. We found that, from all possible combinations of mutualistic and antagonistic interactions, there were two types of assemblages that appeared more frequently than expected by chance. These overrepresented patterns of interaction are called interaction motifs. Most plants interacted strongly with mutualists and weakly with antagonists, or vice versa, being a coherent result with the spatial segregation found between mutualistic and antagonistic interaction strengths. Depending on the interaction motif, an individual plant may contribute differentially to the overall dynamics of pollen transfer and production of viable seeds. Thus, female plant fitness predictably decreases as we move from the mutualistic to the antagonistic extremes of the interaction gradient. However, plants damaged by antagonists, whenever these plants have strong interactions with mutualists, are not systematically decoupled from the mating network via pollen flow. Moreover, these plants are more integrated in the mating network than plants with fully mutualistic assemblages. Our results suggest that measuring only the effects of mutualists may misrepresent whole-plant reproduction depending on the context of pollination, and encourage further research to elucidate to what extent antagonists alter the patterns of pollen transfer (direct and indirectly) and the mechanisms behind their influence on total fitness (male plus female components). Taken together, our results demonstrate that opportunistic nectarivorous vertebrates are effective pollinators of Canarian flora despite of their generalized diet. Considering life-history traits of bird and lizard pollinators was key to understand their consequences on plant reproductive success. However, our predictability improved when taking into account also the different life histories of floral antagonists and the inherent spatio-temporal variability of mutualistic and antagonistic interactions. For this reason, maybe the most important contribution of the present thesis has been the introduction of a quantitative and dynamical framework that integrates multispecies interactions, explicitly considering their diversity in functional guilds, in order to understand the context dependence of opportunistic pollination. We believe that this integrative perspective could be generalized to specialist pollination systems and other types of plant-animal mutualisms (e.g. seed dispersal) to accurately predict plant reproduction and population dynamics. Prediction will be very useful in the case of insular mutualisms which, due to their simplicity and low functional equivalence, are more susceptible to disturbances compared to complex systems.