FLOWER HEATING FOLLOWING ANTHESIS & THE EVOLUTION OF GALL MIDGEPOLLINATION IN SCHISANDRACEAE AMERICAN JOURNAL OF BOTANY -JULY 2010-
Shi Xiao Luo & Dianxiang Zhan South China Botanical Garden, Guangzhou, China Shu-Miaw Chaw Biodiversity Research Center Taipei, Taiwan Susanne S. Renner Department of Biology, University of Munich Munich, Germany
KEY TERMS• Agamospermy -the asexual formation of embryos and seeds without the occurrence of fertilization.• Anthesis - the period during which a flower is fully open and functional.• Oviposition - to deposit or lay eggs.• Saprophytic - organisms that feed on dead or decaying matter.
STAR VINE FAMILY ~90 SPECIESSchisandraceae Kadsura (22 species) - Endemic to Tropical Asia Schisandra (25 species) - Tropical Asia- (Exception - S. glabra)Illicium (42 species) - SE Asia, SE U.S., Mexico, Greater Antilles
WHY IS THIS PAPER INTERESTING? • First Data Ever Published On Thermogenesis & Pollination In Any Asian Illicium Species • TR-71U THERMO RECORDER
PREVIOUS STUDIES POLLINATION BIOLOGY (5 of 90 Species) North American Schisandraceae & Asian Schisandraceae Thien et al., 1983; White and Thien, 1985; Deringer et al.,1999; Liu et al., 2007; Yuan et al., 2007, 2008
PREVIOUS EXPERIMENTS SUPPORT: FLOWER HEATING: 1.) is a direct energy reward for ectothermic pollinators 2.) increases the volatilization of chemicals directed at pollinators3.) helps the plant mimic mammalian feces or carrion attracting saprophytic pollinators 4.) enhances the respiratory release of CO₂, which in combination with other volatile chemicals may stimulate fly oviposition
NORTH AMERICAN SPECIES (New World Illicium & Schisandra)-Pollinated predominantly by flies with beetles as co- pollinators Thien et al., 1983; White and Thien, 1985; Deringer et al.,1999; Liu et al., 2007
Illicium floridanum Jack Scheper - www.Floridata.com
FLOWER HEATING FOLLOWING ANTHESIS & THE EVOLUTION OF GALL MIDGEPOLLINATION IN SCHISANDRACEAE
POST ANTHESIS FLOWER HEATINGSchisandraceae Old World Illicium EVOLUTION OF GALL MIDGE POLLINATION
OBJECTIVESQUESTIONS AUTHORS ARE TRYING TO ANSWER1.) Given that some Schisandraceae exhibit flower heating, do AsianIllicium species also possess this trait?2.) Does any flower heating continue after a flower’s sexual functionis over, and if so, what is the adaptive significance of postantheticflower heating?3.) Are Asian Illicium species pollinated by gall midges, or do theyshow “generalized” fly and/or beetle pollination similar to New WorldIllicium?4.) Are flower heating and midge pollination functionally correlated?
STUDY SPECIES 1: Illicium dunnianumDESCRIPTION: Small shrub (0.5 – 2m high)HABITAT: Riverbanks in wooded ravines (Elevations 300-750m)LOCATION: Shiheqiguan - Nan Kun Shan National Forest Park, ChinaOBSERVED: Mid March to late April – 2008 & 2009# OBSERVED: 53 individuals total: (38 at site A, 8 at site B, 5 at site C)STUDY SPECIES 2: Illicium tsangiiDESCRIPTION: Shrub or small tree (up to 10m)HABITAT: Mixed forests or thickets (Elevations 500-800m)LOCATION: Along road - Nan Kun Shan National Forest Park,ChinaOBSERVED: April to late May – 2008 & 2009# OBSERVED: 56 individuals total
FLORAL DEVELOPMENT, FUNCTION, & TEMPERATURE Open Pollinated, Male Phase, Cross Pollinated, Nursing Phase, Bagged Pre-Anthesis Female Phase • Relative position & color of tepals, stamens, and styles. • Presence or absence of secretion. • Timing of; style movements, anther dehiscence, and floral organ wilting/abscission. • Ambient and floral temperatures in open-pollinated flowers recorded for 50 h) using TR-71U thermo recorder (AWESOME!) Readings taken every 5 sec. (male phase, nursing phase, female phase) • One-way ANOVA F-tests and t-tests – using statistical package SPSS • G-test- using Microsoft Excel Poptools 3.0
Plant Reproductive Biology -Mating Systems-1.) Randomly selected flowers and marked as controls2.) Flowers self pollinated from male-phase flower then bagged3.) Flowers bagged to test for agamospermy4.) Flowers cross pollinated then bagged
VISITORS & POLLINATORSDiurnal & nocturnal observations made over 150 hours: -Recorded Kinds & Numbers of Visitors -Duration of Visits -Insect Behavior To investigate flowers functional phases • Visitor behavior was monitored inside flowers • Flowers were bagged at end of female phase • Flowers were bagged at end of male phase • Tepal tips were trimmed in male phase flowers • Tepal tips were trimmed at beginning of nursing phase
Molecular Phylogenetics & Ancestral Trait Reconstruction• Sequenced complete internal transcribed spacer (ITS) of ribosomal DNA• Sequenced part of the chloroplast trnL region• Data set comprised 43 species – 2197 aligned nucleotides• Performed Maximum Likelihood analysis under GTR + G model of substitution• Bootstrap support values were estimated w/ 100 replicate heuristic searches
RESULTS♦ 1st night = Female flowers w/ fully receptive stigmas♦ 1st day = interim phase (female to male)♦ 2nd night = flowers entered male phase –last 2-3 nights (anther dehiscence)♦ Day 3-7= Nursing phase begins Inner tepals close, forming a chamber, Adaxial filament surfaces and inner tepal bases produce a secretion, Filaments increased in diameter in control from female to nursing phase Filaments thickened from female to male and then wilted by nursing.
FEMALE PHASE (Illicium dunnianum) Pollination occurred mostly at night Single midges entered same flower numerous times Only one midge at a time – if occupied other midges would fly away Midge eggs became visible & pollen grains appeared on stigmas after visits Single midges deposited 26 (+/- 3) pollen grains Captured midges carried numerous pollen grains on body New species of Clinodiplosis was likely discovered
MALE PHASE (Illicium dunnianum) When anthers dehisced midges again visited to oviposit 20 eggs were found per flower in the male phase, but flowers with trimmed tepals caused eggs to die The highest number of larvae/ flower were found in the bagged male-phase. Highest number of eggs was found in male phase flowers High temperatures beginning of female phase then dropped to ambient during male Produced little heat during day and throughout male stages
NURSING PHASE (Illicium dunnianum) Onset of nursing phase chamber temp. increased to higher than in female phase Midges did not try to enter nursing phase ﬂowers Larvae in nursing phase ﬂowers were seen feeding on ﬁlament and tepal secre=on.
OBJECTIVES1. Asian Illicium species do possess postanthe:c ﬂower hea:ng.2. The key stage of thermal warming was well aEer the sexual func:on was over in the two studied species. The only observable & supported beneﬁt of post‐anthe:c hea:ng is exclusive to the larvae of the pollinator. The increase in temperature provides warm enough temperatures for larvae to survive and the heat also causes ﬁlament and tepal secre:on which the larvae feed on. The hea:ng seems to be a reward for the pollinator in a plant‐ pollinator mutualis:c rela:onship. 3. In contrast to the New World Illicium, the two study species Illicium dunnianum and I. tsangii were pollinated only by Clinodiplosis gall midges. 4. Despite these ﬁndings, comparison of the ancestral state reconstruc:ons for two traits showed that ﬂower hea:ng and gall midge pollina:on are not strictly correlated.
DISCUSSION‐Flower hea:ng evolved during the evolu:on of Schisandraceae and became co opted in ﬂowers pollinated by ﬂower breeding midges?‐Floral hea:ng helps odor emission??‐Flower hea:ng aids in pollen tube growth??‐Obligate outcrossing may be enforced by self incompatability??‐Selec:ve factors behind the evolu:on of ﬂower hea:ng??‐Are midges simply co‐pollinators??