Elsevier

Aquatic Botany

Volume 166, August 2020, 103267
Aquatic Botany

Nymphaea pulchella (Nymphaeaceae) and Trigona spinipes (Apidae) interaction: From florivory to effective pollination in ponds surrounded by pasture

https://doi.org/10.1016/j.aquabot.2020.103267Get rights and content

Highlights

  • Floral biology of Nymphaea pulchella is reported at a rural area.

  • Trigona spinipes behavior matches the floral morphology and anthesis sequence.

  • Despite being a florivore, Trigona spinipes is the single effective pollinator.

  • Nymphaea pulchella is autogamous, but Trigona spinipes increases fruit set.

Abstract

Aquatic macrophytes that occur in isolated ponds in hostile pasture matrices may be subject to setbacks in the delicate balance of animal-plant interactions, such as pollination systems. In this work we took as a model Nymphaea pulchella DC., a species which occurs in isolated ponds in pastures in Northeast Brazil. We aimed to elucidate how complex pollination mechanisms can survive in human-dominated landscapes. We conducted studies involving floral biology to determine the morphological structure of the whorls and the anthesis sequence. We also analyzed behavior and frequency of floral visitors, as well as how the floral organs were used as resources, and tried to determine if there was pollinator dependence through pollen tube analyses and controlled pollination experiments. We recorded a gradient structure of floral organs and differences in the timing and extent of floral opening between days. Trigona spinipes consumes all floral whorls indiscriminately (configuring direct and indirect florivory). Despite the florivory, this bee was the most abundant floral visitor and was the only one confirmed effective pollinator. N. pulchella is autogamous with delayed self-pollination, but there were significantly more fruits formed in flowers exposed to bees than in spontaneous self-pollination, and even flowers with partially consumed ovaries produced fruits. Since interaction with T. spinipes contributes to greater fruit formation, we believe this supergeneralist native bee is an important factor in ensuring the success of N. pulchella in occupying the pasture matrix studied.

Introduction

In the context of anthropogenic landscapes, the pollination system of plant species that occur in isolated habitats may be subject to setbacks, since the delicate balance of animal-plant interactions is strongly affected by human activities (Sáyago et al., 2018; Wenzel et al., 2019). Thus, plant reproductive strategies are a key factor in the colonization of disturbed habitats, since plants generally need to deal with a low frequency, or even an absence, of pollinators (Wenzel et al., 2019; Domingos-Melo et al., 2018). Aquatic plants in rural areas are usually isolated in ponds, either naturally-occurring or created artificially through damming streams for cattle raising (De Marco et al., 2014). The sexual reproduction of these aquatic macrophytes can be heavily compromised in degraded landscapes, depending on the level of isolation of these ponds and the decline of native pollinators (De Meester et al., 2005).

Despite the hostility of the anthropogenic landscapes, some species of aquatic macrophytes can still survive in these places (McKinney and Lockwood, 1999; Bini et al., 1999), such as plants of the genus Nymphaea. This is the largest genus in Nymphaeaceae, which in turn is the largest family of Nymphaeales (Borsch et al., 2008; Löhne et al., 2008). The genus is important in our understanding of functional and evolutive perspectives of pollination, since it is an early diverging group with unusual floral biology (Taylor et al., 2015; Zini et al., 2017, 2019; Coiro and Lumaga, 2018; Maia et al., 2014).

Nymphaea fits the common floral pattern of the 'basal' angiosperms (Endress, 2010). Their flowers have many sepals, petals, stamens and carpels, forming a morphological gradient. Their anthesis can last from two to several days, usually with a female phase on the first day, followed subsequently by a male phase (Endress, 2001; Bernhardt and Thien, 1987; Wiersema, 1988; Gottsberger, 2015). In the female phase, the stigma secrets an abundant amount of liquid that helps in capturing pollinators and washing off pollen from their bodies (Wiersema, 1988). Species with diurnal flowers, such as Nymphaea subgenera Anecphya and Brachyceras, are usually pollinated by bees and flies (Wiersema, 1988; Fava and Gomes, 2017). Night‐blooming species, such as in Nymphaea subgenus Hydrocallis, are commonly pollinated by beetles, attracted through fragrances and thermogenesis in chamber-shaped flowers. These beetles usually kept trapped during the female phase during the first night of anthesis, and then are released during the male phase (Cramer et al., 1975; Hirthe and Porembski, 2003; Maia et al., 2014).

Given the complex pollination systems found in Nymphaea species, how can they reproduce in a hostile, degraded environment? A possible explanation is that other mating systems could ensure reproductive security. If the species are self-compatible, then autogamy (autofertilization by self-pollination in the single flower) and geitonogamy (pollination among flowers of the same self-compatible individual) could provide reproductive assurance when pollinators are rare. Further, vegetative propagation can maintain populations when conditions are stable (Wiersema, 1988; Grob et al., 2006; Mohammed and Awodoyin, 2008). However, details of these systems remain unknown, because there are very few accurate measurements of pollinator interactions, thus not allowing to determine their role in Nymphaea reproduction (Cramer et al., 1975; Schneider and Chaney, 1981; Schneider, 1982; Capperino and Schneider, 1985; Velde, 1986; Orban and Bouharmont, 1995; Hirthe and Porembski, 2003; Begum et al., 2010; Lima, 2015; Povilus et al., 2015; Fava and Gomes, 2017).

In this work we present the case of Nymphaea pulchella DC.. We described the floral biology of Nymphaea pulchella, reporting the morphology and the anthesis sequence. We tested the hypothesis that timing of floral opening (i.e. when the flower is open during the day), the size of the opening into the corolla (i.e. the diameter of the opening into the center of the flower) and the dehiscence of the anthers differs during the days of anthesis. We also investigated the pollination system by observing the behavior of floral visitors and tested the hypotheses that the frequency of visits differs between times and days of anthesis. Finally, we checked prezygotic control of self-incompatibility and tested the hypothesis that N. pulchella is autogamous, but does not depend on pollinators for reproduction, although reproductive success is increased by them.

Section snippets

Model species and populations studied

Nymphaea pulchella is a Neotropical species with a wide distribution, occurring in South America, Mexico, and some Caribbean islands (Wiersema et al., 2008). It has a wide natural distribution in Brazil, from northern to southern regions including Amazonia, Caatinga, Mata Atlanta and Cerrado. N. pulchella is a frequent species inhabiting isolated ponds in pastures in Brazilian Northeast, once the Brazil is a country where pasturage exceeds 160 million ha, with about 48 % of the land surface

Floral biology: morphology and anthesis sequence

The Nymphaea pulchella flowers present a complex morphological structure, with wider and longer peripheral parts that gradually change to narrower and shorter near the center of the flower (Fig. 1 – A and B). In all whorls, the length and width are highly correlated (Table 1). The floral opening differed between the days (χ2 = 433.2; df = 21; p < 0.0001) and the hours (χ2 = 198.16; df = 18; p < 0.0001). The first day shows more asynchronic opening, and in the other days the flowers open earlier

Anthesis of Nymphaea pulchella ensures a high floral complexity

The flower of Nymphaea pulchella showed numerous floral organs forming a size gradient, maintaining the pattern described for the genus (Wiersema, 1988; Lima, 2015). This floral morphology is associated with basal groups having simple floral organs without connation or synorganization (Endress, 2010). In contrast, the events that occur throughout the anthesis of N. pulchella results in a high complexity in the functioning of the flower. Such phenotypic specialization is also extended to

Funding

The research was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), through a scholarship to S.L.C. [311021/2014-0] and partial financial support [459485/2014–8] to I.C.M. This work was also supported by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) via a scholarship awarded to A.D.M. [IBPG-0550-2.03/14] and APQ 0808-2.03/16 to I.C.M. This study was also funded in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível

CRediT authorship contribution statement

Sofia Lucas Chalegre: Conceptualization, Methodology, Formal analysis, Writing - original draft. Arthur Domingos-Melo: Conceptualization, Supervision, Methodology, Formal analysis, Writing - original draft. Carla Teixeira de Lima: Writing - original draft. Ana Maria Giulietti: Writing - original draft. Machado Isabel Cristina: Supervision, Writing - original draft, Project administration, Funding acquisition.

Declaration of Competing Interest

We declare that the authors contributed to this work as follows:

Acknowledgments

To Sinzinando Lima (PPGBV/UFPE) for his help in the field. To Shalon Rodrigues (in memorian) for permission to conduct studies on her farm. To Dr. Ray Harley (Royal Botanic Gardens, Kew) for English revision.

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