Breeding system and pollination of Gesneria pauciflora (Gesneriaceae), a threatened Caribbean species

Highlights

• Gesneria pauciflora was pollinated by hummingbirds but visitation rate was low.

• Fruit and seed production in natural condition was low, indicating pollen limitation.

• Autogamy is a form of reproductive assurance by the erratic pollinator services.

• Breeding and pollination systems fit the ancestral pattern for insular gesneriads.

• Florivory was noticed (by native plume-moth), but its incidence seems to be small.

Abstract

Knowledge of plant breeding systems may be critical to facilitate recovery of species considered at risk. Gesneria pauciflora is a threatened, rupiculous, and riverine species with floral-traits that suggest a hummingbird-pollination system. Because these habitat-pollinator conditions have been linked to pollinator-independent reproductive systems, we expected a breeding system that provides reproductive assurance. We assessed the breeding system and potential vulnerabilities during pollination phase using field observations and pollination experiments, to determine pollinator dependency and the existence of strategies for reproductive assurance. Gesneria pauciflora was pollinated by two hummingbird species but visitation rates were low, probably due to low nectar rewards. Fruit set and seed production were significantly higher in flowers when pollen was artificially delivered (self- and cross-pollination) compared to when it was not (control and autogamy), suggesting that reproduction is pollen-limited. Gesneria pauciflora is self-compatible, with some seeds produced via autonomous selfing without any effects of pollination mechanism on seed germination rates. Florivory by the native plume-moth Postplatyptilia caribica was observed, but its incidence was low (12%). Our findings are consistent with theory on the evolution of plant breeding systems on islands, and contribute to the understanding of the evolution of breeding systems in Caribbean gesneriads. Overall, data do not show immediate vulnerabilities to this listed species at the pollination phase, and autogamy may represent reproductive assurance counteracting unpredictable environmental factors that influence its reproduction. However, its capacity for selfing is small relative to other tubular Puerto Rican Gesneria which may explain its rare status.

Introduction

Information on breeding systems may be critical for the development of successful strategies to facilitate recovery in rare, endemic, threatened, or endangered plant species (Cao et al., 2006; Pino-Torres and Koptur, 2009; Robertson et al., 2004; Rodríguez-Pérez, 2005). Breeding systems may influence processes at the reproductive stage that in turn influence the type of mating (selfing vs. outcrossing), the likelihood of fruit and seed production, and plant fitness. For example, Astrophytum asterias (Zucc.) Lem., a self-incompatible endangered cactus with a restricted distribution range, has a reproductive system that is highly dependent on the availability and effectiveness of its pollinators (Strong and Williamson, 2007). The same phenomenon has been shown for the threatened shrub Tetratheca juncea Sm. (Gross et al., 2003) and the endemic perennial shrub Polygala vayredae Costa (Castro, 2009; Castro et al., 2008). All of which faced reproductive constraints due to low biotic visitation rates and high pollinator dependence, which led to recommendations for management of their habitat as well as their plant-pollinator interactions to improve fruit and seed production. However, not all endangered or threatened species have an obligate pollination interaction but instead exhibit mixed pollination systems that may reduce their vulnerability (Yates and Ladd, 2004). The endangered herbs Helianthemum marifolium Mill. and H. caput-felis Boiss. are both self-compatible species that produce fruit and seeds in self-pollinated and outcrossed flowers (Rodríguez-Pérez, 2005); the endemic herb Petrocoptis viscosa Rothm, has an autonomous facultative self-pollination system that has the potential for outcrossing (Navarro and Guitián, 2002); and the endangered climbing vine species Jacquemontia reclinata House ex Small, is predominantly outcrossing but is also capable of producing fruits and seeds via late autogamy (Pino-Torres and Koptur, 2009). Thus, the observed variability in breeding system mechanisms across rare and endemic species may also be accompanied by variation in their reproductive capacity and in their demographic vulnerability.

Plants may exhibit a reduction in fitness during the pollination phase due to variation in biotic and abiotic factors, or by human-disturbance impacts through a variety of mechanisms. Large-scale disturbance events such as selective logging, metal soil contamination, wetland creation, may reduce the availability of pollinators and increase pollen limitation, but also diminish pollen loads on stigmas and in the process reduce outcrossing (Eckert et al., 2009). Likewise, forest patch isolation (habitat fragmentation) can reduce pollinator network connectivity and increase vulnerability in outcrossing species by reducing plant fitness (Vanbergen et al., 2014). Changes in climate (i.e. temperature and precipitation) by inducing early or late flowering events (Hamann, 2004; Iler and Inouye, 2013; Menzel et al., 2006) can lead to mismatches in plant-pollinator interaction that in turn may decrease fruit production (Hegland et al., 2009). Other vulnerabilities during the pollination phase may result from antagonist processes such as flower herbivory, in which pollinator' visitation rates might decrease due to a reduction in flower attractiveness, nectar production and delayed flowering (McArt et al., 2014; Schiestl et al., 2014). Given the tight link between pollination and plant fitness, it is important to evaluate the factors that influence pollination success directly or indirectly, especially for rare and endangered species as a way to gather information that may help improve natural seed production, seedling recruitment, and long-term population persistence.

For plants endemic to insular systems, the evolution of breeding systems may be influenced by ecological conditions that may characterize island ecosystems (Barrett, 1996; Charlesworth, 2006). This hypothesis, also known as Baker’s rule (Baker, 1955; Barrett, 1996), states that species with self-compatible and autonomous pollination systems should be more common in island ecosystems (relative to continental ones); where pollinator faunas are less diverse or where pollinators of species dispersing into islands are absent (Anderson et al., 2001; Ayre et al., 1994; Barrett et al., 2008; Jacquemyn et al., 2005; Wheelwright et al., 2006). Alternatively, novel pollinator interactions and generalized pollination systems are also expected in these environments (Martén-Rodríguez and Fenster, 2010; Martén-Rodríguez et al., 2009). Recent analyses comparing Gesneriaceae in mainland and island ecosystems suggested no differences in autofertiliy index between geographic areas, yet generalized systems were more evident in insular species (Martén-Rodríguez et al., 2015). While studies by Marten-Rodríguez and collaborators support some hypotheses on the evolution of plant breeding systems on islands, they also suggest that local habitats may also influence plant breeding systems. For example, rupiculous (i.e. growing on rocks) and epiphytic (i.e. growing on trees) gesneriad species exhibit autonomous breeding systems more often that terrestrial ones. One hypothesis is that on rupiculous and epiphytic habitats, autonomous breeding systems may be favored to maximize the use of available resources to reproduction under unpredictable pollinator environments (Martén-Rodríguez et al., 2015). Our target species, Gesneria pauciflora Urb., is a rupiculous species that grows along riverbanks that may experience periodic flash floods (or extended dry periods). Assuming that these habitats may offer uncertain pollinator environments as in other gesneriads, G. pauciflora may also exhibit an autonomous breeding system for reproductive assurance.

We evaluated the breeding system and pollinators of the endangered species Gesneria pauciflora Urb. (Gesneriaceae) on the island of Puerto Rico. There are five additional species of Gesneria [G. citrina Urb., G. cuneifolia (DC.) Fritsch, G. pedunculosa (DC.) Fritsch, G. reticulata (Griseb.) Urb., and G. viridiflora subsp. sintenisii (Urb) L.E. Skog], all of which are self-compatible species as one would expect on insular ecosystems (Martén-Rodríguez and Fenster, 2008). With the exception of G. reticulata, all Gesneria species reported for Puerto Rico are endemic and only G. pauciflora is classified as a threatened species under the US Endangered Species Act. This species was listed due to its narrow distribution (endemic to serpentine soils in south-western Puerto Rico) and the potential for population extinction due to large-scale natural (i.e. hurricanes, landslides or severe flooding) and human disturbances (i.e. changes in the hydrology due to water extraction) (U.S. Fish and Wildlife Services, 1995). The study of this species’ reproductive biology and ecology are identified as recovery actions in the “Recovery Plan for G. pauciflora” (U.S. Fish and Wildlife Services, 1998). However, we lack information on its reproductive biology, potential pollinators, and on vulnerabilities experienced during the pollination phase. Gesneria pauciflora is a rupiculous and riverine species that may experience periodic disturbances. Assuming that G. pauciflora’s breeding system behaves in similar ways to other rupiculous gesneriads, we hypothesized that the species may exhibit an autonomous breeding system for reproductive assurance. Herein we address the information gaps in its reproductive biology by asking the following questions: What are the main pollinator(s) of G. pauciflora? Is fruit or seed production influenced by the type of pollination (self- vs. cross)? Is the breeding system of G. pauciflora different to those reported for other Gesneria species on Puerto Rico? Our goal was to carry out a comprehensive study to evaluate the reproductive biology of G. pauciflora focusing on events occurring at the pollination stage. We also compared the breeding system characteristics of G. pauciflora to those reported for other Gesneria species in the Caribbean to explore the ecological and evolutionary context of G. pauciflora’s breeding system.