Table Of ContentMadrono, Vol. 54, No. 1, pp. 22-26, 2007
THE EFFECT OF STAMINODE REMOVAL ON FEMALE REPRODUCTIVE |
SUCCESS IN A WYOMING POPULATION OF THE ENDANGERED BLOWOUT
PENSTEMON, PENSTEMON HA YDENII (SCROPHULARIACEAE)
Hawk
Jessica L.
1016 Clouet St., New Orleans, LA 70117
j
Vincent Tepedino'
J.
USDA-ARS, Bee Biology & Systematics Lab., Dept. of Biology, Utah State University, \
UT
Logan, 84322-5310
Abstract
;
We examined the effect of removing the staminode of the rare Blowout penstemon, Penstemon \\
haydenii, on female reproductive success in a south-central Wyoming population. We found no
i
significant difference in fruit set or in seeds per fruit between flowers with and without staminodes.
\
Themostfrequentflowervisitor, themegachilid bee, Osiuiahrevis,modifieditsbehaviorwhenvisiting
flowers without staminodes. In intact flowers, O. hrevis collected pollen by straddling the staminode
and rubbing its head and thorax across the anthers. In flowers without staminodes, O. hrevis, j
appeared to compensate for the increased distance to the anthers from the corolla floor by simply
stretchingits legs to makecontact withtheanthers. The smaller, nativegeneralist sweat bee{Dialictus \
pruinosus),whichcommonlycollected pollen inintact flowers, appeareddisoriented inflowerswithout r
staminodes, and frequently left without collecting pollen. Other taxa (e.g., bumblebees, Bomhus spp.,
the masarid wasp Pseudomasaris vespoides), appeared unaffected and plied the flowers without
incident. We speculate that the staminode ofBlowout penstemon is intermittently vestigial: where O.
hrevis, bumblebees, and P. vespoides are common, the staminode is oflittle consequence; where D.
pruinosus is the primary pollinator, the staminode is essential to sexual reproduction by the plant.
Key Words: bees, behavior, fecundity, Penstemon, pollinators, staminode. ^
Staminodes are stamens that have lost their the staminode, curves down to lie along the
essential male reproductive function: they no adaxial corolla "floor". The staminode is often
longer produce viable pollen and, in most densely pubescent, hence the common name,
instances, are antherless. Although not coinmon, "beardtongue,'' for the genus. The staminode
staminodes are found in about one-third of all may be exerted, as in P. eriantheriis, or extremely
Angiosperm families (Walker-Larsen and Harder short and perpendicular to the corolla roof(e.g., |
2000). They have evolved diverse shapes and P. personatus). These differences may be associ-
functions (Ronse Decraene and Smets 2001), all ated with the kind of primary pollinator that
seemingly related indirectly to sexual reproduc- visits the flowers. Many of the hypotheses cited
tion. For example, they may function as nectar above to explain the evolution of staminodes
guides (Delpino, cited in Straw 1956), act as have been presented with Penstemon in mind, but
a barrier to discourage flower entrance by nectar only recently have experimental studies begun to
orpollen thieves (Straw 1956), providea purchase uncover the role of these structures (Walker- \
to flower visitors (Pennell 1948), act as a lever Larsen and Harder 2001; Dieringer and Cabrera ||
mechanism to enhance pollination (Torchio 1974; R. 2002). i|
Walker-Larsen and Harder 2001), or provide In this paper, we evaluate whether the stami-
fodder to potential insect pollinators (Cane node ofBlowout penstemon, Penstemon haydenii |
1993). Or, they currently may serve no discernible S. Wats., plays a role in increasing female \
funScttaimoinn(oWdaelskearr-eLaprasretnicualnadrlyHarcdoemrm2o0n01)i.n the trheeprordesuuclttisvedifsfuecrcewssithofstpheicsiersaroefsfpelcoiweesr, vainsditoirf ij
atrriebethCohugehltonteoaheav(eScarcocpohumlpaarniiaceedaet)h,eewvhoelurteiotnheoyf (e.g., Dieringer and Cabrera R. 2002). |^
zygomorphic flowers (i.e., Endress 1999; Ronse perPeennnsitalemhoenrbhaoyfde"nbiliowisouatns"eairnlyspasruscecleyssvieognea-l ji
Decraene and Smets 2001). In the genus Penste- j!
tated, active sand dunes in western Nebraska and
macotner,istsitcas:mitnwoodepsaiarrseofonfeertoilfe tshteamdeenfsi,nianngucphpaerr- south-central Wyoming (Hardy et al. 1989; |p;
and a lower, are positioned along the abaxial Stubbendieck et al. 1989; Heidel 2005). It has |i
surface ofthe corolla, and the fifth sterile stamen. large (c. 25-30 mm), fragrant pale blue to i
lavender or pink flowers arranged in whorls
(verticillasters) along the inflorescence. The sta- :ij
'corresponding author: [email protected] minode is included in the corolla, and is flattened l
2007] HAWK AND TEPEDINO: STAMINODE REMOVAL IN BLOWOUT PENSTEMON 23
at the distal end where it is densely to sparsely cence were selected and marked with a paint pen.
pubescent (or even glabrous) with yellow to Fruits were collected in July 2005, air-dried in the
golden hairs. Flowers are cross-pollinated and lab and seeds were counted.
self-incompatible (Tepedino et al. 2006a, b). We compared fruits per flower and seeds per
Nebraska and Wyoming populations are visited fruit between treatments using non-parametric
by a range of insects (Lawson et. al. 1989; statistical tests. Because not all whorls on each
Tepedino et al. 2006a, b; unpublished) but are selected plant matured flowers, thedistribution of
pollinated primarily by native bees in the families treated flowers varied both across whorls and
Megachilidae, Halictidae and Apidae (Tepedino plants. We used the Chi square statistic to 1)
et al. 2006a, b). It has been listed as Endangered compare fruit set among flowers of different
under the U. S. Endangered Species Act since whorls whose staminode had been removed, and
1987. 2) between the staminode removal treatment and
controls. The Kruskal-Wallis test was used to
Methods compare seeds per fruit among different flower
whorls whose staminode had been removed.
We studied P. haydenii in the sand dunes of Seeds per fruit between removal treatment and
northwest Carbon Co., south-central Wyoming, controls were compared using the Wilcoxon
USA, in June 2005. The Bear Mountain East site Rank Sum Test (also known as the Mann-
is situated on the south slope of Bear Mountain Whitney test).
in a blowout depression in the Ferris Dunes Behavior of abundant insect foragers on
(Stokes and Gaylord 1993) at the eastern end of flowers with and without staminodes was ob-
the Ferris Mountains (2035-2270 m elevation). served and recorded soon after treatment during
The P. haydenii ramets (c. 2000; Heidel 2005) four 30-minute periods over two days.
grow among lemon scurf pea {Psoralen lancelo-
lata Pursh.), chokecherry {Primus virginiana L.), Results
silverleaf phacelia {Phacelia hastate Dougl. Ex
Lehm.), and painted milkvetch {Astragalus eer- The developmental tempo of flower matura-
amicus Sheld. var. filifolius (A. Gray) Herm.). tion accelerated with time. At the beginning of
Average precipitation in the area is about the blooming season, flowers remained open for
25 cm yr most falling in April and May. four to seven days. The outer pair of anthers
Consult Heidel (2005) for detailed site descrip- typically dehisced on the second day and the
tions with maps and pictures. inner pair the next day. The downward hook in
Observations of flower phenology were made the style, normally taken to signify stigma
twice, once at the beginning of the blooming receptivity (Straw 1956; but see Tepedino et al.
season (c. June 8) and again, about two weeks 1999) occurred by the second day (i.e., at the
later when bloom was waning. Each time, ten same time the outer pair of anthers were de-
fresh flowers (one on each of ten haphazardly hiscing). Flowers of later-blooming plants had
selected plants) were observed for several succes- flowers that opened and senesced in one to two
sive days, from the beginning of anthesis to days. Both pairs ofanthers dehisced and the style
senescence. Antherdehiscence, stigma receptivity, hooked on the first day. Both maturation
and style position were noted. sequences are unusual in Penstenion because the
To test for the role ofthe staminode in female style usually does not bend below the anthers
reproductive success, we haphazardly selected 25 until after the anthers dehisce (see also Tepedino
mature plants scattered throughout the popula- et al. 1999).
tion with an inflorescence with several mature, Plants in the treatment groups, particularly the
but unopened, buds in each of several flower open-pollinated treatment, were heavily browsed
whorls, and no open flowers. Inflorescences were by cattle and wild ungulates. Nine of the
bagged with white nylon tulle (1-mm- mesh) to inflorescences used for staminode removals and
prevent insect visitation before staminodes had almost all of the control inflorescences on
been excised. To resist the frequent strong winds, adjacent plants were cropped, forcing us to
the bag was anchored to the ground with metal compare open-pollinated control plants from
wire. An additional unbagged inflorescence of a concurrent breeding system study (Tepedino
similar age was chosen from a nearby plant as et al. 2006b) with the treatment flowers.
a control. As the buds opened on the bagged Before comparing results from the staminode
inflorescence, the staminode in two (rarely one) removal experiments with controls, we compared
open flowers per node (up to eight flowers per fruits per flower and seeds per fruit among the
inflorescence) was excised at the base with fine four flower whorls (Table 1). There was no
scissors while being held with forceps. Care was difference among whorls in fruits per flower (x~
taken not to brush against the stamens and = 7.44, df = 3, P > 0.05) or in seeds per fruit
stigma during excision. For comparison, at least (Kruskal-WalHs Test, df = 3, P > 0.40) for the
three flowers on each control treatment inflores- staminode removal treatment; we therefore com-
MADRONO
24 [Vol. 54
Table 1. The Number of Flowers Producing (Dieringer and Cabrera R. 2002 also found that
Fruits (Frts) or No Fruits (Nofrts) for Staminode small bees spent longer times on the flowers than
Removal and Open-Pollinated Treatments in did large bees.) i
A Wyoming Population of Penstemon haydenii. Two visitors did not modify their behavior. |
N = number of plants with treated flowers in each Pseudomasaris vespoides females exhibited the
category. Staminode removed treatment combines data same pollen collecting technique in flowers with
from Whorls 1-4. Seeds/Frt data are plant means and and without staminodes. Like O. brevis, they
standard deviations. i
collected pollen by scraping their heads against
Frts NoFrts N Seeds/Frt SD the anthers. However, because of their size, 'i
female P. vespoides had no difficulty in reaching
StaRmeimnoovdeed 60 26 16 12.5 2.9 the anthers. Similarly, Bombus spp. did not show i>
OpWWehhnoorrPollll21inated 221144 1173 111304 111512...900 665...532 falnoyweorsbvwiiotuhssbteahmaivnioodreaslrcehmaonvgeeds. when visiting *||
Whorl 3 14 7 11 14.5 5.5 Discussion
Whorl 4 8 5 7 12.9 3.0 \
The production of an elaborate staminode, as
in Blowout penstemon, would seem to entail
a non-trivial cost of energy and nutrients. One
bined the data for comparison with the open- expects such an expenditure to be compensated
pollinated treatinent. for by a benefit, such as an increase in re-
We found no difference in fruit set between the productive success. Recently, two groups have
staminode reinoval flowers and the open-polli- followed early studies by Clements and Long
nated treatment (Table 1; x' 0-28, df = 1, P > (1923) by removing the staminodes offive species
0.50). Nor was there a difference in seeds per fruit and examining the effects on female and male '
between treatments (Wilcoxon Rank Sum Test, P reproductive success (Dieringer and Cabrera R.
> 0.30). Apparently, female reproductive success 2001, 2002; Walker-Larsen and Harder 2001). '
was little influenced by the absence of the Their results suggest that the function of the
staminode. staminode in Penstemon species is diverse, and |
The most abundant visitors to the flowers of that even well-developed, costly staminodes may j
,;
Blowout penstemon were bees of the genera not have an obvious function. Results of
Osmia (especially O. hrevis), Dialictus spp., staminode removals by Clements and Long ;
[
Bomhus spp. and the masarid wasp, Pseudoma- (1923) were also species-specific; our findings
saris vespoides, a specialized Penstemon visitor support that interpretation.
(Cooper 1952). All were seen visiting flowerswith Walker-Larsen and Harder (2001) examined j
and without staminodes. In some cases, the floral four species, two bird-pollinated (P. centranthi-
visitors modified their behavior on the flowers folius, P. rostriflorus) and two bee-pollinated {P.
without staminodes. For example, on intact el/ipticus, P. pcdmeri), with very different results.
flowers, O. hrevis females would land on the The bird-pollinated species exhibited no effect of
staminode and rub their head and thorax back staminode removal, either on pollen deposition
and forth on the anthers to collect pollen, on the stigma, or pollen removal from the
!
concurrently contacting any stigma that had anthers. Results for the bee-pollinated species
reached the hooked stage). When visiting flowers were more complicated: pollen deposition on the
i
without a staminode, O. hrevis landed on the stigma decreased significantly for flowers without
floor of the corolla and stretched upwards to staminodes but the mechanism of action was i
reach the anthers. We saw no indication, either in different for P. ellipticus and P. palmeri. Pollen ill
observations, or when modest pressure was removal was significantly greater from anthers in
|]
applied to the staminode, of declination of the intact P. palmeri flowers than from flowers
f
stamens or style as occurs when the staminode without staminodes. However, greater pollen
ji
functions as a lever (Torchio 1974). removal rates need not translate to greater male
Dicdictus females seemed disoriented by stami- fitness: that depends on whether pollen is de- Ji:
node removal. In staminodeless flowers, they posited on a receptive stigma or is removed from '
appeared unable to gain a purchase on thecorolla the system either by grooming or by being using
ji
floor and soon left. Normally, they spent much as larval food (Thomson and Thomson 1992; i
time on the flowers, crawling around inside the Kobayashi et al. 1999). In P. ellipticus, pollen I;
corolla, perhaps to collect nectar; frequently removal was unaffected by staminode removal.
\\
resting on the staminode or walking over the The work of Dieringer and Cabrera R. (2001,
j;
stainens and anthers in an inverted position to 2002) also shows an effect ofstaminode removal
|<
become dusted with pollen on the ventral on female reproductive success ofa bee-pollinat-
i
abdomen. In general, Dialictus females spent ed species, P. digitalis. Initially (2001), they i
more time on the flowers than did other bees. showed that flowers with staminodes removed
i
2007] HAWK AND TEPEDINO: STAMINODE REMOVAL IN BLOWOUT PENSTEMON 25
produced significantly fewer seeds per fruit than Management in Rawlins WY. We especially thank
intact flowers. Subsequently, they showed that Frank Blomquist ofthat office fordiscoveringtheplant
staminode removal affected pollen deposition on in Wyoming in 1996, for initiating the study that made
the stigma but not pollen removal from the this little project possible, and for providing support
throughout. Bonnie Heidel, Wyoming Natural Di-
anthers (Dieringerand Cabrera R. 2002) and that
versity Database, Univ. of Wyoming, Laramie, was
the size of flower-visiting bees was important: also instrumental in facilitating this research.
both large and small (but not intermediate-sized)
bees deposited fewer pollen grains in staminode- Literature Cited
less flowers. Thus, for all three bee-pollinated
species studied thus far, pollen deposition per Cane, J. H. 1993. Reproductive role ofsterile pollen in
visit is reduced by staminode removal. In Sciiiraida (Actinidiaceae), a cryptically dieocious
contrast, male reproductive success may have neotropical tree. Biotropica 25:493-495.
been lower in only one ofthe three species. Clempeolnltisna,tiFo.n:E.AanndoutF.linL.e Loofntgh.e 1e9c2o3l.ogEyxpoefrifmleonwtearls
Time constraints prevented us from estimating and insects. Carnegie Institute of Washington
pollen deposition and removal. Instead, we used Publication No. 336, Washington D.C.
a simple bioassay to compare fruit set and seed Cooper, K. W. 1952. Records and flower preferences
production between flowers with staminodes and ofmasarid wasps. II. Polytrophy or oligotrophy in
flowers whose staminodes were removed (Dier- Pseudomasaris'? American Midland Naturalist
inger and Cabrera R. 2001). In contrast to 48:103-110.
Walker-Larsen and Harder (2001) and Dieringer Dieringer, G. and L. Cabrera R. 2001. Pollination
and Cabrera R. (2001, 2002), we found no effect ecology ofbristle staminodia in Penstemon digitalis
of staminode removal on female reproductive (Scrophulariaceae) and Jacaranda acutifolia
success of this bee- and wasp-pollinated beard- (BignAoNnDiaceae). Bio2t00a2m.1T2:h3e1-3i6n.teraction between
tongue. .
pollinator size and the bristle staminode of
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ofspecies-specific differences. Evidently, it is not Journal ofBotany 89:991-997.
simply that the staminode is superfluous in bird- Endress, p. K. 1999. Symmetry in flowers: diversity
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much smaller Dialictus bees completely changed the Interior, Bureau of Land Management, Raw-
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such that pollination was unlikely. Similarly, KOBAYASHI, S., K. INOUE, AND M. KATO. 1999.
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