Gerardo Arceo-Gómez

Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities

UNLABELLED PREMISE OF THE STUDY While we have a good understanding of how co-flowering plants interact via pollinator foraging, we still know very little about how plants interact via heterospecific pollen (HP) receipt. To fill this gap, we sought to illuminate the extent of HP receipt and quantitatively evaluate the fitness consequences of HP receipt. We consider plant traits that could mediate the fitness costs of HP receipt in an effort to better understand the potential consequences of pollinator sharing in natural communities. • METHODS We survey the literature for occurrence of HP receipt and assess variation in the fitness effects of a standard HP treatment. We develop a conceptual framework for understanding variation in fitness consequences of HP receipt. • KEY RESULTS We find evidence for variation in HP receipt and its costs. Our framework predicts that certain traits (self-incompatibility, small, highly aperaturate or allelopathic pollen) will lead to detrimental HP donors, whereas others (self-compatibility, small or wet stigmas, short styles) will lead to vulnerable HP recipients. We also predict that detrimental effects of HP receipt will increase with decreasing phylogenetic distance between donor and recipient. • CONCLUSIONS Our framework can guide much needed additional work so that we can evaluate whether and which plant traits contribute to the variation in the effects of HP receipt. This will be a step toward predicting the consequences of HP receipt in natural communities, and ultimately transform our understanding of the role of postpollination interactions in floral trait evolution and pollinator sharing.

Heterospecific pollen deposition: does diversity alter the consequences?

• In natural communities, plants can receive pollen from multiple heterospecifics as well as conspecifics. However, studies on the effects of interspecific pollen transfer have focused on interactions between species pairs. The potential exists for diverse interactions among heterospecific pollen (HP) grains on the stigma, and for these to affect plant reproduction, alone or in combination with conspecific pollen (CP) loss, but these interactions have not yet been explored. • We used hand-pollinations to simulate increasing community diversity and CP loss on Mimulus guttatus stigmas. We used pollen mixes of one to three heterospecific donors to determine how species composition and CP load size affect seed production and to characterize the mechanisms underlying fertilization failure. • Heterospecific pollen deposition reduced M. guttatus seed production and while the effect increased with the number of heterospecific donors, the strength depended on species composition and was independent of conspecific load size. Different types of interactions (additive and synergistic) are hypothesized to underlie the diverse effects on M. guttatus reproductive success. • Our results suggest that an increase in the diversity of heterospecific donors will not always lead to a greater decrease in fitness because multispecies effects depend on the interacting species.

Among-species differences in pollen quality and quantity limitation: implications for endemics in biodiverse hotspots

BACKGROUND AND AIMS Insufficient pollination is a function of quantity and quality of pollen receipt, and the relative contribution of each to pollen limitation may vary with intrinsic plant traits and extrinsic ecological properties. Community-level studies are essential to evaluate variation across species in quality limitation under common ecological conditions. This study examined whether endemic species are more limited by pollen quantity or quality than non-endemic co-flowering species in three endemic-rich plant communities located in biodiversity hotspots of different continents (Andalusia, California and Yucatan). METHODS Natural variations in pollen receipt and pollen tube formation were analysed for 20 insect-pollinated plants. Endemic and non-endemic species that co-flowered were paired in order to estimate and compare the quantity and quality components of pre-zygotic pollination success, obtained through piecewise regression analysis of the relationship between pollen grains and pollen tubes of naturally pollinated wilted flowers. KEY RESULTS Pollen tubes did not frequently exceed the number of ovules per flower. Only the combination of abundant and good quality pollen and a low number of ovules per flower conferred relief from pre-zygotic pollen limitation in the three stochastic pollination environments studied. Quality of pollen receipt was found to be as variable as quantity among study species. The relative pollination success of endemic and non-endemic species, and its quantity and quality components, was community dependent. CONCLUSIONS Assessing both quality and quantity of pollen receipt is key to determining the ovule fertilization potential of both endemic and widespread plants in biodiverse hotspot regions. Large natural variation among flowers of the same species in the two components and pollen tube formation deserves further analysis in order to estimate the environmental, phenotypic and intraindividual sources of variation that may affect how plants evolve to overcome this limitation in different communities worldwide.

Coflowering Community Context Influences Female Fitness and Alters the Adaptive Value of Flower Longevity in Mimulus guttatus

A major goal in evolutionary biology is to incorporate the complexity of multispecies interactions into our understanding of microevolutionary processes within populations. Although considerable work has been done on antagonistic interactions (e.g., plant-herbivore), little attention has been paid to the evolutionary implications of context dependency in mutualistic interactions (e.g., plant-pollinator). In this study, we use seep communities to evaluate how coflowering species richness affects key aspects of pollination (visitation rate and conspecific and heterospecific pollen receipt) of Mimulus guttatus. We assessed the importance of coflowering diversity in mediating floral evolution by determining whether species richness was associated with variation in flower size, longevity, and stigma-anther distance and by conducting a reciprocal transplant experiment in two contrasting pollination environments. We found lower visitation rates and higher heterospecific pollen transfer to M. guttatus growing in high-diversity coflowering communities compared to low-diversity coflowering communities. We found a positive correlation between flower longevity and coflowering species richness. Furthermore, our reciprocal transplant experiment showed that extended flower longevity was advantageous only in high-diversity seeps and identified coflowering diversity as the most likely selective agent. Our results suggest that coflowering diversity can promote floral trait differentiation among populations, in this case, flower longevity.

Patterns of among- and within-species variation in heterospecific pollen receipt: The importance of ecological generalization

PREMISE OF THE STUDY Coflowering plants are at risk for receiving pollen from heterospecifics as well as conspecifics, yet evidence shows wide variation in the degree that heterospecific pollen transfer occurs. Evaluation of patterns and correlates of among- and within-species variation in heterospecific pollen (HP) receipt is key to understanding its importance for floral evolution and species coexistence; however, the rarity of deeply sampled multispecies comparisons has precluded such an evaluation. METHODS We evaluated patterns of among- and within-species variation in HP load size and diversity in 19 species across three distinct plant communities. We assessed the importance of phenotypic specialization (floral phenotype), ecological specialization (contemporary visitor assemblage), and conspecific flower density as determinants of among-species variation. We present hypotheses for different accrual patterns of HP within species based on the evenness and quality of floral visitors and evaluated these by characterizing the relationship between conspecific pollen (CP) and HP receipt. KEY RESULTS We found that within-species variation in HP receipt was greater than among-species and among-communities variation. Among species, ecological generalization emerged as the strongest driver of variation in HP receipt irrespective of phenotypic specialization. Within-species variation in HP load size and diversity was predicted most often from two CP-HP relationships (linear or exponentially decreasing), suggesting that two distinct types of plant-pollinator interactions prevail. CONCLUSIONS Our results give important insights into the potential drivers of among- and within-species variation in HP receipt. They also highlight the value of explorations of patterns at the intraspecific level, which can ultimately shed light on plant-pollinator-mediated selection in diverse plant communities.

Heterospecific pollen receipt affects self pollen more than outcross pollen: implications for mixed‐mating plants

Flowering plants often occur in mixed-species groups where interactions between them can occur both pre- and post-pollination. In post-pollination interactions, conspecific (CP) and heterospecific pollen (HP) interact on the style and previous work indicates that these interactions, often, but not always, lead to reduced fitness. However, over half of insect-pollinated species display a mixed mating system, where both self and outcross CP could interact with HP, yet no study has evaluated the effects on both types of CP. We present and test hypotheses for the differential effects of HP depending on CP source and timing of HP arrival with a mixed-mating plant, Mimulus guttatus, and one of its HP donors (Helianthus exilis). We found H. exilis pollen reduced tube growth and fertilization success of M. guttatus self pollen to a greater degree than outcross pollen, but only when CP and HP were applied simultaneously. Our results indicate that for mixed-mating plants the fitness consequences of HP receipt can b...

Plant–flower visitor networks in a serpentine metacommunity: assessing traits associated with keystone plant species

Consistent topology of plant–pollinator networks across space may be due to substitutability of the plant species most important for community function (keystone species). It is unclear, however, whether keystone species identity varies within a community type and what traits underlie this variation. Using a network biology approach, we assess whether keystone plant species vary across a metacommunity of five serpentine seeps in California and determine the features that predict their identity. We define keystone species as those with high strength, low node specialization index (NSI), and/or low d′ and determine whether these parameters are predicted by floral traits (flower biomass, number of open flowers per plant, symmetry, or stamen number) and/or ecological features (variation in local floral abundance, endemism) within seeps and across the metacommunity. Keystone species identity varied among seeps and was associated with local flower abundance: mean floral abundance correlated positively with strength but negatively with NSI within most seeps as well as across the metacommunity. For the metacommunity, flower biomass correlated negatively with NSI while variation in flower abundance correlated negatively with strength. Across the metacommunity, the d′ metric was associated with flower biomass, whereby plants with smaller flowers interacted with the most abundant pollinators across the metacommunity. Results suggest that connectance and interaction evenness may not be greatly influenced by community composition turnover due to substitution of keystone plant species across space. Keystone species can be predicted by functional traits but which trait (flower abundance or size) depended on the metric used and the level observed.

Floral and reproductive biology of the Mexican endemic Chamaecrista chamaecristoides (Fabaceae)1

Abstract Arceo-Gómez, G. (Department of Biological Sciences, University of Pittsburgh, 4249 Fifth Ave., Pittsburgh, PA, USA), M. L. Martínez (Red de Ecología Funcional, Instituto de Ecología A. C. carretera antigua a Coatepec N° 351 El Haya, Xalapa Veracruz, México C.P. 91070), V. Parra-Tabla (Departamento de Ecología Tropical, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Km. 15.5 carretera Mérida-Xmatkuil, Mérida, Yucatán, México), and J. G. García-Franco (Red de Ecología Funcional, Instituto de Ecología A. C. carretera antigua a Coatepec N° 351 El Haya, Xalapa Veracruz, México C.P. 91070). Floral and reproductive biology of the Mexican endemic Chamaecrista chamaecristoides (Fabaceae). J. Torrey Bot. Soc. 139: 260–269. 2012.—Chamaecrista chamaecristoides is an enantiostylous shrub endemic to the coast of Mexico that is being heavily impacted by human activities along the Gulf of Mexico. Chamaecrista chamaecristoides is considered a key species of the sand dune communities, particularly for its role as a nurse species and in dune stabilization. While certain aspects of its population biology have been well studied, others, such as its reproductive biology, have been overlooked. Understanding the factors that contribute to the successful reproduction of this species is crucial for its maintenance in natural populations. In this study, we examine the floral and reproductive biology of C. chamaecristoides. Specifically, we evaluate flower morphology and phenology, the breeding system and the identity and foraging patterns of floral visitors. Our results show that flower morphs are morphologically identical; however, position, size, and pollen production vary between stamens within each flower, suggesting functional differentiation. Furthermore, plants differ in their proportion of right- and left-styled flowers over the flowering season. While this could promote cross-fertilization by favoring pollen transfer among individuals with opposite floral-morph ratios, the presence of a stamen adjacent to the style, its self-compatibility and the absence of inbreeding depression all compromise the role of enantiostyly as an outcrossing strategy in this species. Finally, even though flowers are visited by at least ten different floral visitors, reproduction of C. chamaecristoides depends heavily on only three species that together account for more than 70% of the total number of visits. Overall, our results suggest that C. chamaecristoides is highly dependent on a small subset of the community of floral visitors and that it has evolved floral strategies to reduce pollen loss and enhance the efficiency of pollen transfer. For these reasons, future conservation strategies must also consider the preservation of suitable habitat for the somewhat limited pollinator community of this species.

Effects of heterospecific pollen from a wind-pollinated and pesticide-treated plant on reproductive success of an insect-pollinated species

PREMISE OF THE STUDY Studies on the effects of heterospecific pollen (HP) transfer have been focused mainly on insect-pollinated species, despite evidence of insect visitation to wind-pollinated species and transfer of their pollen onto stigmas of insect-pollinated plants. Thus, the potential consequences of HP transfer from wind-pollinated species remain largely unknown. Furthermore, accumulation of pesticide residues in pollen of wind-pollinated crops has been documented, but its potential effects on wild plant species via HP transfer have not been tested. METHODS We evaluated the effect of wind-dispersed Zea mays pollen on pollen tube growth of the insect-pollinated Mimulus nudatus via hand pollinations. We further evaluated whether pesticide-contaminated Z. mays pollen has larger effects on M. nudatus pollen success than non-contaminated Z. mays pollen. KEY RESULTS We found a significant negative effect of Z. mays pollen on M. nudatus pollen tube growth even when deposited in small amounts. However, we did not observe any difference in the magnitude of this effect between pesticide-laden Z. mays pollen and non-contaminated Z. mays pollen. CONCLUSIONS Our results suggest that wind-pollinated species can have negative effects as HP donors on insect-pollinated recipients. Thus, their role in shaping co-flowering interactions for wind- and insect-pollinated species deserves more attention. Although we did not find evidence that pesticide contamination increased HP effects, we cannot fully rule out the existence of such an effect, because pollen load and thus the pesticide dose applied to stigmas was low. This result should be confirmed using other HP donors and across a range of HP loads, pesticide types, and concentrations.

Negative effects of heterospecific pollen receipt vary with abiotic conditions: ecological and evolutionary implications

BACKGROUND AND AIMS Studies that have evaluated the effects of heterospecific pollen (HP) receipt on plant reproductive success have generally overlooked the variability of the natural abiotic environment in which plants grow. Variability in abiotic conditions, such as light and water availability, has the potential to affect pollen-stigma interactions (i.e. conspecific pollen germination and performance), which will probably influence the effects of HP receipt. Thus, a more complete understanding of the extent, strength and consequences of plant-plant interactions via HP transfer requires better consideration of the range of abiotic conditions in which these interactions occur. This study addresses this issue by evaluating the effects of two HP donors (Tamonea curassavica and Angelonia angustifolia) on the reproductive success of Cuphea gaumeri, an endemic species of the Yucatan Peninsula. METHODS Mixed (conspecific pollen and HP) and pure (conspecific pollen only) hand-pollinations were conducted under varying conditions of water and light availability in a full factorial design. Reproductive success was measured as the number of pollen tubes that reached the bottom of the style. KEY RESULTS Only one of the two HP donors had a significant effect on C. gaumeri reproductive success, but this effect was dependent on water and light availability. Specifically, HP receipt caused a decrease in pollen tube growth, but only when the availability of water, light or both was low, and not when the availability of both resources was high. CONCLUSIONS The results show that the outcome of interspecific post-pollination interactions via HP transfer can be context-dependent and vary with abiotic conditions, thus suggesting that abiotic effects in natural populations may be under-estimated. Such context-dependency could lead to spatial and temporal mosaics in the ecological and evolutionary consequences of post-pollination interactions.