Ecosphere 5(7): 1-8 (July 2014)
Pollen Quality for Pollinators Tracks Pollen Quality for Plants in Mimulus Guttatus
R. L. Yeamans, T. H. Roulston, D. E. Carr

Abstract: Pollen viability ranges substantially among and within plant species, and can be reduced by various factors, including pollution and inbreeding. While it is evident that a reduction in gamete quality reduces the male component of plant fitness, the implications of changes in pollen viability on the nutritional value of pollen for pollinators has not been studied. To test this, we created a greenhouse population of Mimulus guttatus plants that ranged in pollen viability from 17% to 98.5% and related both pollen quantity and pollen protein content to pollen viability. We found that crude protein concentration ranged from 15% to 45% and was positively associated with pollen viability. We also found that pollen mass per flower ranged 5-fold, also positively related to pollen viability. Across experimental plants, there was an 11-fold difference in protein mass per flower between plants of the lowest and highest pollen viabilities. We conclude that conditions that lead to reduced pollen viability, especially early in pollen development, may greatly reduce the awards available to plant pollinators.

Introduction

Wild pollinators play important and sometimes dominant roles in the production of insect pollinated crops, as well as provide key pollination services to wild plants and the food chains that depend on them (Ricketts et al. 2004, Kremen et al. 2007, Winfree et al. 2008, Julier and Roulston 2009). Recently, however, many concerns have arisen about how land management and other environmental impacts affect pollinator populations. Factors already identified include loss of habitat (Bates et al. 2011, Roulston and Goodell 2011), insecticide use (Brittain and Potts 2011), loss of preferred food plants (Biesmeijer et al. 2006) and the introduction of novel parasites (Cameron et al. 2011, Li et al. 2011). Little attention has thus far focused on the potential for environmental changes to alter the quality of host plants that pollinators use as food.

Pollen is the primary protein source for many pollinators, especially bees (Gilbert 1972, Howell 1974, Gilbert 1981, Erhardt and Baker 1990, Michener 2000, Roulston and Cane 2000). Larval bees of nearly all species acquire protein exclusively from pollen, and adult females require a protein diet to maintain egg production (Michener 2000). Pollen protein concentration ranges from 2.5% to 61.7% protein by dry weight, and increased protein has been associated with improved larval development in some pollinators (Roulston and Cane 2000, Roulston et al. 2000). Thus, ecological or environmental factors that influence pollen protein levels in plants have the potential to influence the development of pollinators that rely on pollen as their protein source.

Current knowledge of variation in pollen protein concentrations is limited mainly to the range of variation across plant taxa, where it is evolutionarily conserved (Roulston et al. 2000). Little is known about the amount of variation within plant taxa or what factors may increase or decrease protein content. While it is unclear if there is any simple functional relationship between the amount of crude protein in pollen grains and any single role in plant reproduction (Roulston et al. 2000), substantial protein content comprises enzymes known to be involved in pollen tube growth and subsequent fertilization (Paton 1921), and these enzymes accumulate in the pollen grain during development (Gorenstein et al. 1991). Any disruptions to pollen development, therefore, could result in reduced enzyme production and lower protein content.

Pollen viability, the ability of pollen to germinate and grow, varies greatly among and within plants. Reduced viability is often associated with processes such as hybridization and inbreeding (Carr and Dudash 1997, Golmirzaie et al. 1998, Melser et al. 1999, Busch 2005, Glaettli and Goudet 2006, Eppley and Pannell 2009, Bures et al. 2010), or environmental stress such as exposure to high temperature or pollutants (Handique and Baruah 1995, Tretyakova et al. 1996, Gottardini et al. 2008, Pasqualini et al. 2011).

Pollen can become inviable either during initial pollen formation in the flower, resulting in malformed grains lacking some or all contents (Wilcock and Neiland 2002, Pipino et al. 2011), or after relatively complete pollen formation (Comtois and Schemenauer 1991). While these mechanisms yield roughly equivalent outcomes for the plant (failed fertilization), the timing of developmental failure could have important implications for the quality of pollen as animal food. As pollen grains develop, they acquire nitrogen transported from other tissues (Yuan et al. 2009). This nitrogen fuels a burst of DNA transcription and protein translation prior to anthesis that readies the pollen grain for the task of growing through stylar tissue and fertilizing ovules (Bedinger 1992, Lalanne et al. 1997). Developmental failure during this time would likely lead to pollen grains of lower overall mass, reduced nitrogen, reduced protein, and diminished nutritional value.

Here we pose two questions regarding pollinator rewards in Mimulus guttatus DC., a bee-pollinated plant species with varying levels of pollen inviability: (1) Is pollen viability related to protein concentration? (2) Is pollen viability related to pollen mass per flower?