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Effects of Fire and Pollinator Visitation on the Reproductive Success of Asimina Reticulata (Annonaceae), the Netted Pawpaw

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Effects of Fire and Pollinator Visitation on the Reproductive Success of Asimina Reticulata (Annonaceae), the Netted Pawpaw CASTANEA 83(2): 323–333. NOVEMBER Copyright 2018 Southern Appalachian Botanical Society Effects of Fire and Pollinator Visitation on the Reproductive Success of Asimina reticulata (Annonaceae), the Netted Pawpaw Louise K. Barton1 and Eric S. Menges2 1Department of Ecology and Evolution, University of Colorado, Boulder, Colorado 80309 2Plant Ecology Program, Archbold Biological Station, Venus, Florida 33960 ABSTRACT The netted pawpaw (Annonaceae, Asimina reticulata) is a widespread Florida endemic plant that produces relatively few fruits. To understand its distribution and reproductive success, we posed three questions: (a) how do time-since-fire (TSF) and pollinator visitation influence reproductive success, (b) is it pollinator dependent, and (c) does outcrossing increase reproductive success? In 2016, we studied 157 plants in three flatwoods burn units (last burned, 2015, 2012, or 2001) and one grazed pasture at Archbold Biological Station in south-central Florida. Plants in pasture and recently burned flatwoods exhibited greater flower, fruit, and seed output, suggesting that habitat openness may promote competitive release or increased pollinator visitation. Pollinator visitation was greatest on plants within the 1-yr TSF, and the hairy flower scarab (Trichiotinus viridans) was the most prevalent visitor across all sites. Autogamously crossed flowers produced no fruit, confirming that seed production is pollinator dependent. Although fruit retention (10.0%) and seed germination (27.8%) were low after geitonogamous crossing, close and far outcrossing increased retention (30.8% and 39.6%) and germination success (41.6% and 46.4%). This research suggests that A. reticulata reaches its maximum reproductive potential in open areas after outcrossing events, and that low fruit set may be due to the lack of an effective pollinator, resulting in inbreeding depression. Additionally, an investigation into raccoons (Procyon lotor) as fruit consumers and potential seed dispersers suggests that seeds may benefit from gut scarification. Key words: Annonaceae, endemic, geitonogamy, pollination ecology, prescribed fire. INTRODUCTION The southeastern Unit- beetle pollinator of the ancient Asimina flowers ed States is a global biodiversity hotspot (Noss may be long extinct, making the flowers of today et al. 2015), supporting enormous plant diversity a Pleistocene anachronism (Barlow 2002). and a vast array of regional endemics (Luna, Asimina reticulata most frequently establish- 2014). Within the genus Asimina, the only es in poorly drained flatwoods or disturbed temperate genus within the Annonaceae, seven habitats (Kral 1960, Abrahamson et al. 1984). A of the eight species are endemic to the southeast long-lived deciduous shrub, A. reticulata pro- and are primarily found in Florida (Kral 1960, duces an early spring display of showy, white, Wunderlin and Hansen 2011). One such species nodding flowers that emit a species-specific is Asimina reticulata Shuttlw. ex Chapm, which honey-like odor (Goodrich and Raguso 2009). is widespread throughout peninsular Florida and Flowers are typically 5–8 cm broad, peak in southern Georgia. Asimina reticulata exhibits abundance between February and April, and are low fruit set, possibly because of inbreeding produced before leaf emergence (Cox 1998, Kral 1960). The flowers are protogynous, with car- depression resulting from pollinator limitation, pellate-phase flowers developing into staminate- similar to its rarer congener, Asimina obovata phase flowers once the stigma is no longer (Willd.) Nash (Levitt et al. 2013). The effective receptive (Cox 1998). At a given time, stems will DOI: 10.2179/18-170 support flowers that are in a variety of stages: 323 324 CASTANEA VOL.83 bud, carpellate-phase, staminate-phase, senes- (AI) and show high levels of outcrossing (Pang cent, and fruiting. Fruits are berries that consist and Saunders 2014). A prior hand-pollination of several large (4–7-cm-long), clustered mono- study on A. reticulata determined incompatibil- carps, each of which contain two rows of 1–8 ity through AI, but not through geitonogamy, and seeds 1–2 cm long (Kral 1960). Seed dispersal found greater fruit set after cross-pollinations and germination success of this plant have not, than after geitonogamy (Cox 1998). Beyond fruit to our knowledge, been previously investigated. set, our study tracked potential inbreeding Along with the highest diversity of Asimina depression from hand-pollination treatments species, Florida supports numerous naturally through germination. Additionally, we incorpo- pyrogenic ecosystems and thus a variety of fire- rated two outcrossing treatments, close and far adapted species (Weekley and Menges 2003, crosses, to gain insight into the influence of Slapcinsky et al. 2010). After fire, many of these distance between parent plants and to assess species will resprout from belowground roots or potential for outbreeding depression. We also rhizomes (Menges and Kohfeldt 1995, Maguire used wildlife cameras to detect fruit predation and Menges 2011). Numerous studies in Florida and seed dispersal. This closer examination into have also shown that fire can also promote the reproductive biology of A. reticulata may seedling recruitment (Hartnett and Richardson provide valuable insight into why fruit set across 1989, Menges and Quintana-Ascencio 2004) and this species is notoriously low. stimulate flowering (Hartnett and Richardson METHODS 1989, McConnell and Menges 2002). Of the Study Sites Asimina species, Asimina longifolia Kral and We conducted this study in 2016 at Archbold Asimina pygmaea (W. Bartr.) Dunal are the Biological Station (ABS), a 2,101-ha preserve most fire dependent and will seldom flower in its located at the southern tip of the Lake Wales absence (Kral 1960). Postfire habitat conditions, Ridge in Highlands County, south-central Flor- including the addition of ash as a soil nutrient ida, (2781005000 N, 818210000 W). Known as a relic (Dean et al. 2015) and increases in light Pleistocene habitat, the Lake Wales Ridge and availability after the removal of high/dense associated Florida scrub support an array of vegetation (Abrahamson et al. 1984, Huffman Florida endemic plant species (Christman and and Werner 2000), may interact with effects of Judd 1990). Comprising naturally pyrogenic top removal from fire to create surges in flower ecosystems, the property is divided into pre- and fruit output. Although not fire dependent, it scribed burn units and is managed with varying is likely that A. reticulata is fire adapted and will fire regimes (Menges et al. 2017b). show similar surges in reproductive output in To examine the effects of TSF on A. retic- more recently burned plots. ulata, we randomly selected three flatwoods In this study, the effects of time-since-fire sites with differing fire histories in which A. (TSF) on flower density, pollinator visitation, reticulata was present. These sites were domi- and the reproductive success of A. reticulata nated by either wiregrass (Aristida stricta were investigated within pine flatwoods with Michx.) or palmettos (Sabal etonia Swingle ex differing prescribed fire-return intervals. Plants Nash and Serenoa repens W. Bartram) and were within a grazed pasture habitat were also burned in 2015, 2012, or 2001 (1-yr, 4-yr, and 15- sampled to assess the influence of openness in yr TSF). Comprising 25% of the ABS area, the absence of fire. Although previous studies flatwoods are characterized by flat terrain with have concluded that A. reticulata responds to poorly drained soils and a scattered overstory of fire or mowing with rapid vegetative growth, Florida slash pines (Pinus elliottii Engelm. var. more long-term reproductive responses have not densa Little & Dorman) (Abrahamson et al. yet been examined (Kral 1960), and fire effects 1984). In addition to the flatwoods sites, we also on seed viability are largely unknown. selected a grazed pasture site within the Arch- To expand existing knowledge on the breeding bold Reserve to assess the influence of openness ecology of A. reticulata andtodetermine in the absence of fire. Although these pasture potential interactions between TSF and repro- sites are fire managed (last burned in 2010), duction, we also implemented a series of hand- actively grazed regions generally burn patchily, pollination treatments. Because of strong proto- suggesting that fire history within this site was gyny, flowers of Annonaceae avoid autogamy less relevant. In February 2016, we mapped and 2018 BARTON, MENGES: REPRODUCTIVE SUCCESS OF ASMINIA RETICULATA 325 Figure 1. (A) Flowering stems of Asimina reticulata Shuttlew. ex Chapm. with buds, carpellate-phase flowers, and staminate-phase flowers. (B) Pollination by a hairy flower scarab beetle (Trichiotinus rufobrunneus). (C) A cluster of fruit produced by a single flower. tagged reproductive individuals within the 1-yr to approximate the number of flowers each plant (n ¼ 52 plants), 4-yr (n ¼ 44), and 15 yr (n ¼ 35) produced throughout the season. postfire and grazed pasture (n ¼ 26) sites, for a Pollination surveys began in late March, when total of 157 study plants. In mid-June, when fruit flowering was at its peak. Initial pollinator began ripening, we counted the number of stems observations yielded no data; therefore, we and measured the height of the tallest branch, manually checked flowers by prying open outer canopy length from the longest horizontal petals to observe pollinators within (Norman and measurement, and canopy width from the widest
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