Flowering, Pollination, and Fruit Set in Tongue Orchids 'Cryptostylis' spp

2006·1.5 MB·English

by  Ac, Herberstein Gaskett

Research Report
Flowering, pollination, and fruit set in
Tongue Orchids Cryptostylis spp.
AC Gaskett and ME Herberstein
DepartmentofBiologicalSciences,MacquarieUniversity,NSW2109
Correspondingauthor:[email protected]
Abstract
Study ofAustralianTongue Orchids addressesquestions ofwidespread interestabout the evolution
ofsexually deceptive pollination, and provides information forconservation and management. We
presentrecent data on flowering, pollination, and fruitset forthree Cryptostylis species: the Bonnet
Orchid C. erecta RBr, the Small Tongue Orchid C. leptochila F Muell. Ex Benth, and the Large
Tongue Orchid C.subulata(Labill.)HG Reichb. (Jones 1988).Thesespeciesarepollinatedby male
Orchid Dupe Wasps Lissopimpla excelsa (Ichncumonidae) when they ‘pseudocopulatc’ with the
flowers. Cryptostylis subulata flowered from December to February, and C. erecta flowered from
Novemberio March. Ciyptostylisleptochilabegan flowering in December,andpollination was still
occurringin lateApril.Thisspecieshadthemostflowers,butthelowestfruitset. In mostfieldsites,
theearliest flowerson aracetnewerepollinatedmost often, although this did notoccurwhen polli-
nators were scarce. Orchids may attract pollinators more easily at the start ofthe floweringseason
before the female wasps emerge, or pollinators could learn the locations or appearance oforchids
andavoidlater-openingflowers. Wealso foundthatpollinatorabundancevariedduringandbetween
seasons, there was no evidence ofself-pollination, and C. erecta racemes were more likely to be
eatenbypredatorsafterfruitset.(The VictorianNaturalist123(3),2006,128-133)
Introduction
Species from the fascinating terrestrial and Biodiversity Conservation Act 1999.
orchid genus Cryptostylis are distributed Research into the natural history ofthese
throughout Australasia and the South species is valuable for the preparation of
Pacific (Jones 1988). There are five recovery plans, and general conservation
Australian species: the Bonnet Orchid and management activities. Furthermore,
Cryptostylis erecta RBr, Small Tongue study ofthe most common Cryptostylis
Orchid C. leptochila F Muell. Ex Benth., species in theirareasofgreatestabundance
Large Tongue Orchid C subulata (Labill.) provides information that may be applied
HG Reichb., Leafless Tongue Orchid C. to rare Cryptostylis species, and other
hunterianaNicholls and Slipper Orchid C. orchids with similar sexually deceptive
ovata RBr(Jones 1988). pollination systems.
The abundance and rarity ofCiyptostylis Whilst C. hunteriana is a leafless sapro-
species vary throughout their distributions. phyte, all other Australian Cryptostylis
Forexample, C. erectaiscommon inNSW species have a solitary, everCgreen leaf
(Bishop 2000), but is listed as ‘vulnerable’ (Jones 1988). In C. erecta and leptochi-
under Victorian legislation (Flora and la>, the leafunderside is purple. The flow-
Fauna Guarantee Act 1988). Cryptostylis ers of Cryptostylis are resupinate with a
leptochila can be locally common in very large labellurn that is predominantly
Victoria and New South Wales, but is list- red or burgundy (Jones 1988). Plants can
ed as ‘endangered’ in Tasmania’s produce a single flower raceme between
Threatened Species Protection Act 1995. August and April. The multiple inflores-
One species, C. hunteriana is extremely cences on the raceme are thought to open
rare throughout its range in ,Victoria, New sequentiallythroughoutthe floweringseason
South Wales, and Queensland (Bell 2001; (Jones 1988). The frequency offlowering in
Clark et al. 2004). It is considered ‘threat- individual plants appears to vary unpre-
ened’ under the Victorian Flora and dictably between years, a common charac-
Fauna Guarantee Act 1988 and ‘vulnera- teristic ofterrestrial orchids (for a review,
ble’ under both the NSW Threatened see KindlemannandBalounova2001).
Species Conservation Act 1995 and the Cryptostylis species attract pollinators by
Commonwealth Environment Protection sexual deception. The orchid flowers are
TheVictorian Naturalist
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Research Report
Methods
thoughtto mimic the appearance and scent Field observations were made ofnatural
of female insects. Male insects that populations ofCryptostylis erecta C. sub-
,
respond tothe mimicryand attempttocop- ulata and C. leptochila in open woodlands
ulatewiththeorchids’ flowers inadvertent- in Ne,w South Wales and Victoria. We
ly collect and distribute the pollinia. usedtwo populations ofsympatric C. erec-
Australian Cryptostylis species are polli- ta and C. subulata near Sydney and
nated by males of a single species of Nowra, and one sympatric C. leptochila
Ichneumonid wasp, the Orchid Dupe and C. subulata site near Melbourne. The
Lissopimpla excelsa (Costa) (CSIRO fourth site, near Nowra, had only C. subu-
1991). For first-hand descriptions ofpolli- lata. At each site we identified patches of
nation in Cryptostylis species see Coleman orchidsfor study. A patch wasdefinedasa
(1928, 1929, 1930), Dacy (1974), Watson cluster of plants that was more than two
(1961), and Stoutamire (1974). Although metres from any other Cryptostylis plants
Ciyptostylis species share a pollinator, and (Table 1).
often have overlapping flowering seasons In the summerof2003-04. we visited the
and distributions, no hybrids have been Sydney C. erectaand C. subulatasiteeight
reported between species (Stoutamire times throughout the flowering period and
2003)
1974; Jones 1988). Cross-pollination ofthe made detailed observations ofindividually
species by hand suggests there are strong labelled plants. Werecorded the period for
internal mechanisms that prevent hybridis- which individual flowers were open, the
ation (Stoutamire 1974; Jones 1988; Llovd interval until pollinia collection and/or
2004)
. deposition, and the occurrence offruiting,
Pollinators are initially attracted to seed set, and predation.
Cryptostylis orchids with a chemical signal During summer 2004-05, we visited all
thought to mimic sex pheromones emitted four field sites three times and made less
by female L. excelsa wasps (Schiestl et al. intensive observations offlowering, seed
. Othervisual and tactile signals, e.g. set, andpredation. Patches oforchids mea-
colours, shapes, and textures that resemble sured at the Sydney site during the first
the features of female wasps, may then field season were not remeasured during
stimulatemalestoattempt to copulate with the second year of the study. Analyses
the flower, and thus move vigorously were pooled for each species, and confi-
enough to transfer pollinia. Deception by dence intervals of95% wereused.
orchid flowers may impose costs upon At each field site, regression analyses
duped insects (e.g. Wong and Schiestl were used to determine whether the posi-
2002), and insect behaviour and learning tion ofa flower along a raceme (i.e. how
may influence pollination success (e.g. early in the season it opened) affected its
Ferdyetal. 1998). likelihood of being pollinated. For these
Here we report some interesting recent analyses, the dependent variable was the
field observations and data on flowering, proportion ofpollination that occurred for
pollination, and fruit set for three species flowers in each position along a raceme.
of Cryptostylis: C. erecta, C. leptochila, The data were pooled according to field
and C. subulata. sitebecause all Cryptostylis species share a
single pollinatorand pollinatorabundances
Table 1.NumberofpatchessurveyedforthreespeciesofTongueOrchid Cryptostylisatfoursitesin
New South Wales and Victoria, ^denotes data combined from two study seasons, Summer2003-04
andSummer2004-05.
site C. erecta C. leptochila C.subulata C. erectaand
C.subulata
Sydney 26* 5*
1
NNoowwrraa21 _1 -_ 67 _1
Melbourne - 15 8 _
Total 27 15 26 2
Vol. 123 (3) 2006 129
.
Research Report
may differ between the field sites. In two May 2005. The populations ofC. leptochi-
final regression analyses on the effect of la near Melbourne had a very long flower-
flower position, we used data from C. ingseasonthatbegan in Decemberand fin-
erecta at the Sydney site for each ofthe ished as late as April, consistent with
two study seasons to compare pollination Backhouse andJeanes (1995). Others have
between years. reported the flowering season for C. lep-
To test for self-pollination, we selected tochila to end in February (Clyne 1970;
four pairs offlowering C. erecta plants in Jones 1988), or March (Bishop 2000). In
the Sydney field site. We isolated each March, 48 racemes (92%) still had open
plant in a mesh bag that prevented insect flowers, but by May, only three racemes
access to the flowers. One plant ofeach were still active (5.8%). Successful polli-
pair was hand-pollinated during the sea- nation occurred as late as April (nine flow-
son. The second plant was not hand-polli- erson seven differentracemes).
nated, but used as a control. All the
Plantdensityandflowering
racemes were checked for fruit set during
and afterthe flowering season. The average number of plants in each
We also assessed pollinator abundance patch was highest in C. erecta, aCnd lowest
and activity in an ad hoc manner by con- in C. subulata, butone patch of subula-
sidering the time necessary to capture tahad 900 plants (Table2). Thenumberof
wasps on different days throughout the racemes per patch was similar for all three
2004-05 flowering season at the Sydney species, but C. leptochila had a higher
average number of flowers per raceme
field site. Wasps were captured with a
hand net when they arrived at our ‘bait’ (Table 2). One plant of C. leptochila had
flowers, as described by Peakall and 35 flowers, which is three times the maxi-
Handel(1993)and Bower(1996). mum number offlowers reported by Jones
(1988), and twice that reported by Bishop
Results and Discussion (2000).
Data were collected from 70 patches of After opening, the flowers of C. erecta
orchids, includingtwo patches ofmixed C. and C. subulata had pollinia collected or
erecta and C. subulate which were deposited after an average of 3.1 days.
,
excluded from subsequent analyses about Some flowers were visited on the day they
single speciespatches. SeeTable 1 opened, and the maximum time until polli-
nation was 8 days, but this was for a
Floweringseasons flower with a damaged labellum. On aver-
In all sites, C. subulata had the shortest age, each flowerwasopen for6days (min.
flowering period of the three species = I, max. = 9). Generally, each flower
(December to February). For C. erecta, opened as the previous flower on the
flowering commenced in November and raceme was closing. Sometimes a flower
had mostly finished by early March, opened up to six days before the previous
although one plant with a flower was flower closed. However, in one case, nine
found in a sheltered area near a creek in
Table2. Flowering,pollination,andfruitset inthreespeciesofTongueOrchidsCryptostylis. Values
withparenthesesare:mean(min.,max.).
C. erecta C. leptochila C.subulata
2003-04 2004-05 2004-05 2003-05 2004-05
plantssurveyed 696 806 754 271 1687
%plantsin flower 14.4 4 9.3 5.9 3.4
racemesperpatch 8.3 4 4.7 5.3 2.5
0.27) (1, 16) (MO) (1,8) (1,10)
flowersperraceme 5.5 5 9.6 7 4.7
(3, 12) (3, 11) (2,35) (3, 12) (1, 11)
pollinatedflowers 2.7 1.13 0.28 2.86 0.77
perraceme (0,9) (0, 7) (0,3) (0,9) (0,5)
%plantsthatsetfruit 72.6 71.9 27.6 75 50
%plantswithoutfruit 19.4 27.1 54 25 38
%racemespredated 8 1 18.4 0 12
130 The Victorian Naturalist
Research Report
days passed between the closing of one dromes in the temperate southern hemi-
flower and the opening ofthe next on the sphere (~40%: Neiland and Wilcock 1998)
sameraceme. and globally (-20%: Tremblay et al.
2005).
Pollinationandfruitset Forthree ofthe four field sites, the posi-
Despite the large number offlowers per tion ofa floweralongaracemesignificant-
raceme produced by C. leptochila, this ly affected the likelihood ofpollination
spoplelciineastehdadfltohweerlsopweerstraacveermaegeanndutmhbeelrowo-f N(Soywdrnaey:1:RR:=:=00..5435,,F,F,15,=,1=58..5023,, pp<<00..0055;;
estpercentageofplants with some fruit set Nowra 2: R:=0.16, F, =1.37, p>0.05;
(aTnadblCes2)u.buAlpaptraoxpilamnattsehlayd7a0t%leoafstCo.neerepcotlu- MPoelllbionuartinoen:wRas:=0m.o5s3t,lFi,ke3l37y=3f3o.r9f6l,owpe<r0s.0t5h)a.t
lGinastuebdulfaltoawewrerine2p0o0l3l-i0na4t,edbuitnotnhley250004%-0o5f oCpoelneemdanear(l1i9e2r8i)n sthueggseesatseodn t(hFiisg.wa1)s.
slienaastoino.nSrcahtieesstolfe8t5a%l. f(o2r00C4.)erreepcotrateadndpoCl- beemcearugseed tehaerlimearltehaLnisfseompailmesp,laanedxcweelrsea
subulata in the Blue Mountains near most active as pollinators until the females
Sydney in 2000. These data demonstrate were available. A second explanation may
that Cryptosty/is species have a higher rate involve the learning abilities ofthe male
ofpollination than that typically expected wasps. In several sexually deceptive polli-
for orchids with deceptive pollination syn- nation systems, pollinators initially are
a) Sydney b) Melbourne
Flower position on raceme
Fig. 1. Frequency ofpollination ofeach sequentially-opening flower positioned along racemes of
NToenwguSeouOtrhchWiadsleCsryapntodstVyi/citsoreirae.ctMaa,xC.imluepmtovchailluae, oanndx-Ca.xissubiuslamtaax,iinmufomurnusimtebserinoofpefnlowfeorresstpeirn
raceme at site. Statistically significant effect offlowerposition at<0.005 level denoted by **, at<
0.05 leveldenotedby*
Vol. 123 (3) 2006 131
Research Report
attracted strongly to a flower, but this (R2=0.195, FU2=2.671, p>0.05). As more
decreases rapidly over a short period, pre- flowers openduringtheseason, males’ fre-
sumably as the duped male pollinators quent exposure and subsequent learning
learn that the flower is not a real female mayleadtoavoidanceofmost flowers.
insect (e.g. Peakall etai 1990; Peakall and Pollinatorsappeared most activebetween
Handel 1993; Wong and Schiestl 2002). approximately9.30 am and 2 pm onwarm,
Male wasps may remember and avoid the sunny days. There were obvious peaks in
location of a false signal for some time, abundance on certain days in different
thus subsequent flowers on a raceme may regions. For example, on one day during
not be visited. Furthermore, male ability to February 2005, nine wasps were caught in
recognise flowers as false signallers may less than two hours at the Sydney field site
be frequency dependent and increase with (-4.5wasps/hour). Previouscaptureefforts
repeatedexposure(Ferdyetat. 1998). in the same area during January and
The impact of male insect learning on February resulted in only four wasps in
orchids’ pollination success also may 18.5 hours searching over eight days (-0.2
depend upon pollinator abundance. In wasps/hour).
2003-04, the effect of flower position on Only two ofthe four pairs ofbagged and
fruit set in Sydney C. erecta was highly isolated inflorescences survived the sea-
significant (R2=0.745, F, ,,=29.15, son. However, only those flowers cross
p<0.001), and the first flower to open on pollinated by hand set fruit. None of the
any raceme had a very high frequency of Bowers in the control bags set fruit. This
pollination (Fig. 2). However, during the lowsample size still corroborates evidence
second study season at this site, there were provided by Dacy (1974), Jones (1988),
fewer pollinator visits, flowers 1-8 on and Lloyd (2003).
racemes of C. erecta had similar pollina-
tion frequencies (Fig. 2), and flower posi- Predation
tion hadno significanteffect on pollination The predation ofracemes was quite low
for all species except C. leptochila (Table
2). The higher level of predation at the
Melbourne field site may have contributed
to the lower pollination success for this
species. Data from 2003-04 showed that
87.5%(n =8)ofthe C. erectaracemesthat
were eaten by predators had recently set
fruit. The fleshy fruit ofCryptostylis seem
tobe attractivefood forbrowsinganimals.
Despite their shared pollinator, and simi-
lar habitat and flowering season, the
Cryptostylis species varied considerably in
their patch sizes, flower numbers, fruit set,
and predation rates. CryplstyUs leptochila
appears to invest heavily in flowering, pro-
ducing many flowers during an extended
season. These features have been associat-
ed with strategies to maximise pollination
success in otherdeceptiveorchids(Neiland
and Wilcock 1995; Kindlemann and
Balounova 2001; Tremblay et ai. 2005).
Flower position on raceme However, C. leptochilahadthelowestfruit
set ofthe species studied. This may mean
that extra investment in flowering has little
sFeiqgu.en2t.ialFlryeqoupeennicnygofflopwoelrlipnoastitiioonneodfaelaocnhg effect on fruit set, particularly ifthere are
racemesofthe BonnetOrchidCryptostyliserec- other negative impacts, e.g. predation of
tain anopen forestsitenearSydneyduringtwo fruits.
floweringseasons: a)2003-04andb)2004-05
132 The Victorian Naturalist
Research Report
The generally high fruit set we observed ColemanE(1928) PollinationofCryptostylisleptochi-
suggests that, unlike many other orchid la.The VictorianNaturalist44,333-340.
Coleman E(1929) PollinationofCryptostylissubulata
species, pollinator limitation is not a major (Labill.)Reichb. TheVictorianNaturalist46,62-66.
conservation issue for Cryptostylis species. ColemanE(1930)PollinationofsomeWestAustralian
Management strategies could prioritise CSoIrcRhOids(.19T9h1e)VTihcetorinisaencNtsatourfaAluissttra4l6i,a:20a3-t2e0x6t.bookfor
protecting plants from predation duringthe students and research workers. (Melbourne
flowering season and conserving suitable UniversityPress:Melbourne)
open forest habitat (see Clarket al. 2004). DaCcnyptMost(v1l9i7s4)suPboulllaitnaa.tioTnheexVpiecrtiomreinatn,Npaetrurfaolrimsetd9o1n,
In addition, care should be taken if infor- 66-78.
mation about Cryptostylis species is used Ferdy .IB,Gouyon PH. Morel J and Godelle B (1998)
Pollinator behavior and deceptive pollination:
to develop conservation plans for other Learning process and floral evolution. American
orchid genera, which are likely to have Naturalist152.696-705.
considerably lower pollination rates (see Jones DL (1988) Native Orchids ofAustralia. (Reed
Tremblayetal. 2005). KiBnodolkesmaPntnyLPtdm:idFrBeanlcohusnFoovraestZ,(N2S00W1))Irregularflow-
eringpatternsinterrestrialorchids:theoriesvsempir-
Acknowledgements icaldata. WebEcology2.75-82.
Fieldworkassistancewasprimarilyprovidedby l.loydG(2003) IhepollinationbiologyofCryptostylis
Noel Gaskett, Greg Holvvell, and Katy Dika, ereetaand Cryptostylissubulata) (Orchidaceae) and
plus Katie Robinson, Peter Abrahams. Jessica the maintenance ofspecies integrity. (Unpublished
MacDowell, and Matt Kovach. Field sites were NeBilSacndHoMnoRuMrsaThnedsiWsi,lUcnoievkerCsiCty(o1f99S5y)dnMeayx)imization
suggested by Alan Stephenson, Dick and ofReproductive Success by European Orchidaceae
Marion Thomson, and Andrew Dilley underConditionsoflnlrequcnt Pollination. 187,39-
(Australasian Native Orchid Society), Craig 48.
Angus (Macquarie University), and Michelle PeakallR,AngusCJandBeattieA,l(1990)Thesignifi-
Mueller(Parks Victoria). Permission toconduct cance ofantand plant traits forant pollination in
RefediaelblidyzwaottrhiekonoJsenrvPpitrsyivBaLattedy.lBaTanhpditsinsetwaorCrhNkuorwwcrahsaawcnoadnsdRguercaatlnettdy- Peoniaa.rketacpleholirdaeR:mlloaainnjmigdpmlbifHrlcaioanartdtaiaelo.lnhOseSciNcgfhoort(ls1os9geo9il3fae)ca8t4Pi,soolen4lx.5iu7naa-Elt4vlo6oyr0ls.udtdeiicsoecpnrtii4mv7ie,-
under permit numbers SI 1401 (NSW) and 1681-1687.
10003057 (Vic). Funding for ACG is via a Schiestl FP. Peakall R and Mant J (2004) Chemical
Furniss Foundation/American Orchid Society communication in the sexually deceptive orchid
Fellowship, a Macquarie University genusCryptostylis. BotanicalJournaloftheLinnean
RPeositngsruardaunactee(R2e00s4e)a.rch Grant, and from Munich StStoohucytinaenmtiiyrde14w4Wa.sP1p9s(91-a92n075d4.)pAsuesutdroacloipanultaetrireosnt.riaAlmoerrcihicdasn,
OrchidSocietyBulletin43, 13-18.
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