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Fig Development in Two Neotropical Ficus Species, F. Yoponensis (Subgen

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Fig Development in Two Neotropical Ficus Species, F. Yoponensis (Subgen Botany Fig development in two Neotropical Ficus species, F. yoponensis (subgen. Pharmacosycea) and F. colubrinae (subgen. Spherosuke): comparing rainforest and pasture trees Journal: Botany Manuscript ID cjb-2020-0139.R2 Manuscript Type: Article Date Submitted by the 06-Feb-2021 Author: Complete List of Authors: Cervantes-Pasqualli, Juan; Instituto de Ecología, Red de Ecología Funcional Laborde, Javier;Draft Instituto de Ecología, Red de Ecología Funcional Keyword: figs, Agaonidae wasps, reproductive event, Ficus, syconium development Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 40 Botany Fig development in two Neotropical Ficus species, F. yoponensis (subgen. Pharmacosycea) and F. colubrinae (subgen. Spherosuke): comparing rainforest and pasture trees Juan Alberto Cervantes-Pasqualli1, Javier Laborde*2 1 Instituto de Ecología, A. C. – Posgrado, Carretera Antigua a Coatepec 351, Col. El Haya, CP 91073, Xalapa, Veracruz, Mexico. [email protected] ORCID: https://orcid.org/0000-0001-7687-3738 2 Instituto de Ecología, A. C. – Red de Ecología Funcional, Carretera Antigua a Coatepec 351, Col. El Haya, CP 91073, Xalapa, Veracruz, Mexico. [email protected] *Corresponding author: Javier Laborde, Instituto de Ecología, A. C., Carretera Antigua a Coatepec 351, Col. El Haya, CP 91073, Xalapa, Veracruz, DraftMexico. Phone: +52 (228) 842-1800 ext. 4205, e-mail: [email protected] ORCID: http://orcid.org/0000-0001-5401-4182 © The Author(s) or their Institution(s) Botany Page 2 of 40 Abstract In the fragmented landscape of Los Tuxtlas, adult fig trees are found in rainforest remnants and in pastures. Syconium (fig) development is known to vary between and within Ficus species, but it is not known whether it differs between rainforest and pasture trees. We describe syconium development for two Ficus species with different life forms (free-standing vs. hemi-epiphytic) in two contrasting, adjacent habitats: undisturbed rainforest and active pastures. Over three months, we monitored 15 reproductive events in Ficus yoponensis and F. colubrinae, collecting and dissecting syconia every 3-4 days (1 291 and 815 syconia per species, respectively). External and internal structural changes in the syconia are described, including foundress occurrence and the maximum duration of the receptive phase while waiting for pollinators. The duration of both the reproductive events (< 8 weeks) and the developmental phases in the two species did not differ betweenDraft rainforest and pasture trees, and are within the lower range of time reported for other Ficus species. After pollinator exclusion, the receptive phase lasted up to four times its normal duration. Syconia were slightly larger in rainforest than in pasture trees, and the infestation of F. yoponensis syconia by non-pollinating insects was higher in rainforest trees. Keywords: figs, Agaonidae wasps, reproductive event, Ficus, syconium development. © The Author(s) or their Institution(s) Page 3 of 40 Botany Introduction The genus Ficus (Moraceae) has more than 800 species worldwide that are characterized by having their inflorescences enclosed within a globular structure known by botanists as a syconium (Harrison 2005), a term derived from the ancient Greek word “sykon” meaning “fig”. The syconia (plural of syconium) are spheroidal urns that contain hundreds of unisexual flowers, whose only avenue of communication with the exterior is a narrow opening called the ostiole, located at the pole opposite the peduncle (Verkerke 1989). All Ficus species in the Neotropics are monoecious, and produce protogynous syconia whose female flowers have styles that differ in length and whose stigmas form an inner layer that lines the inside of the syconial cavity (Berg 1992; Weiblen 2001). Since the flowers are fully enclosed within the syconium, not just any animal can act as a pollinator. Only tiny (< 2 mm) wasps (Hymenoptera, Chalcidoidea, Agaonidae) specialized in entering via the ostioleDraft are able to pollinate these enclosed structures (Janzen 1979; Harrison 2005). Therefore, the genus Ficus is also characterized by its obligate mutualistic interaction with its pollinating wasps. About 90% of the fig wasp’s life cycle (egg to adult in 4 – 8 weeks) occurs inside the syconium. The wasps are unable to reproduce outside the syconium and without the pollinating fig wasps, the tree is unable to produce seeds (Herre et al. 2008). The development of syconia and their pollinating fig wasps was described by Galil and Eisikowitch (1968), using the African species F. sycomorus as a model. Based on their observations of the development of the female and male flowers, the seeds and the life cycle of the fig wasps inside the syconium, these authors defined five phases. Pre-female phase A: The axillar meristems on the fig tree branches begin to differentiate and grow to form the syconium, inside which immature female flowers begin to develop. Receptive or female phase B: The female flowers are ready to be pollinated by the adult female wasps that arrive carrying pollen from another syconium and must enter the syconial cavity via the ostiole. Inside, the wasps pollinate the flowers at the same time as they oviposit their eggs in some of the female © The Author(s) or their Institution(s) Botany Page 4 of 40 flowers. As the female wasp makes her way through the imbricating scales of the ostiole she loses her wings and antennae. Inter-floral phase C: Pollinated flowers begin to develop a seed, while flowers with a wasp egg begin to form a gall in which a larva develops. Emerging or male phase D: Adult male wasps emerge from the galls and begin to mate with female wasps who are inside their respective galls or they liberate the female from her gall and mate with her immediately. At the same time as the male wasps are fertilizing the females, the fig’s male flowers mature, their anthers exposing pollen inside the syconial cavity. After mating, male wasps dig a tunnel to exit the syconium, usually close to or through the ostiole and then die outside. These tunnels are used to exit the syconium by the adult female wasps who are loaded with pollen and are carrying the next generation of wasps, the eggs of which will be laid inside another receptive syconium (phase B). Mature or ripe phase E: The syconium infructescence ripens, with well formed seeds and no pollinating waspsDraft inside. Other non-pollinating insects are able to enter and/or oviposit within the syconium (Palmieri and Pereira 2018), and their larvae will either feed on the developing flowers (phytophagous insects) or prey on the pollinator fig wasps, interfering with the mutualistic interaction of the fig wasps with the fig tree. Reproductive events tend to be asynchronous in the fig tree population, while syconium production and development are usually synchronous within the tree crown, limiting self-pollination (Janzen 1979; Bronstein and Patel 1992; Harrison 2005). The year-round production of syconia required to maintain the short-lived pollinating wasps makes Ficus species one of the most reliable and important food sources for the large number of vertebrate frugivores that consume ripe figs (syconia) and disperse their seeds. This is why the ripe infructescences of Ficus have been identified as a key resource in maintaining diversity in the world’s tropical forests, particularly in humid forest where 75 to 80% of the tree species depend on vertebrate frugivores for seed dispersal (Janzen 1979; Shanahan et al. 2001; Harrison 2005). It is generally thought that all Ficus species follow the developmental phases described by Galil and Eisikowitch (1968). © The Author(s) or their Institution(s) Page 5 of 40 Botany However, it is known that the duration and timing of reproductive events (fruiting), the duration of each phase of syconium development, as well as the external and internal morphological characteristics of the syconium (including the number of female and male flowers, seeds and fig wasps produced) all vary greatly between species and between individuals of the same species (Ramírez 1974; Janzen 1979; Herre 1989, 1996). Even so, fruit phenology and syconium characteristics have been described thoroughly for only a few species (Baijnath and Ramcharun 1983; Zhang et al. 2006; Piedra-Malagón et al. 2019). In Mexico, the development of syconia has only been fully described for F. petiolaris, an endemic species that grows in seasonally dry tropical forest (Piedra-Malagón et al. 2019). The duration of the developmental phases of both the syconia and the wasps determines how many reproductive events are needed by the trees throughout the year to maintain the population of pollinators. The duration of the receptive phase is particularly critical, sinceDraft it determines how long the tree is able to keep syconia on its branches while waiting for pollinators to arrive, but the duration of the inter-floral phase when the wasp larvae grow and become adults is also key (Bronstein et al. 1990; Anstett et al. 1995, 1997). Of the six Ficus subgenera that have been described worldwide, only two are found in the Americas (Ibarra-Manríquez et al. 2012): Pharmacosycea and Spherosuke (previously known as Urostigma). Of the 22 Ficus species reported for Mexico, five belong to Pharmacosycea and 17 to Spherosuke (Ibarra- Manríquez et al. 2012; Pederneiras et al. 2015). In Mexico, Pharmacosycea species are free-living terrestrial trees that
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