reproductive trade-offs in a specialized plant/pollinator...
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Reproductive trade-offs in a specialized plant/pollinator systeminvolving Asplundia uncinata Harling (Cyclanthaceae)and a derelomine flower weevil (Coleoptera: Curculionidae)
N. M. Franz
Escuela de Biologıa, Universidad de Costa Rica, Ciudad Universitaria ‘‘Rodrigo Facio’’, Costa Rica;
present address: Department of Biology, University of Puerto Rico, Mayaguez, USA
Received 15 January 2007; Accepted 1 August 2007; Published online 26 October 2007
� Springer-Verlag 2007
Abstract. The reproductive interactions of a spe-
cialized plant/pollinator system involving Asplundiauncinata Harling (Cyclanthaceae) and a derelomine
flower weevil (Coleoptera: Curculionidae: Derelo-
mini) were studied at La Selva, Costa Rica. The
inflorescences of A. uncinata exhibit a suite of
cantharophilous characters including a precisely
synchronized anthesis, protogyny, thermogenesis,
olfactory attraction of visitors via modified stamin-
odes, and narrow interfloral entrances. The weevil
pollinators use the inflorescences for feeding, mating,
and oviposition. The larvae are detritivorous and
develop either in the detaching staminate flowers or,
at a more favorable rate, in the rotting infructes-
cences. The rate of infructescence abortion was high
and caused by low levels of pollination. Manual
pollination treatments yielded significantly higher
seed counts than obtained under natural conditions,
and furthermore demonstrated the inflorescences’
ability to reproduce via geitonogamy. In the longer
term, the reproductive benefits of maintaining low
levels of pollination may shift away from the weevils
and towards the plants via an increase in the size of
the pollinator population.
Keywords: Asplundia uncinata Harling; cantharo-
phily; geitonogamy; infructescence abortion; plant/
pollinator mutualism; pollinator efficiency; pollinator
reproduction; reproductive system
The reproductive interactions among the Neotrop-
ical Cyclanthaceae and their pollinators remain
largely unexplored. The more than 230 species of
cyclanths have a palm-like habitus and bear highly
derived inflorescences suggestive of beetle polli-
nation. In support of this view, Harling (1958)
reported that small weevils (Coleoptera: Curculi-
onidae) visit the inflorescences, and he repeatedly
found weevil larvae and pupae when dissecting the
fruits. Yet these observations were challenged for
many years, as other researchers found only
stingless meliponine bees on the inflorescences
(Heide 1923, Croat 1978, Schremmer 1982). In the
first reliable field study published on the family,
Beach (1982) established that scarab beetles
pollinate Cyclanthus bipartitus Poiteau, the only
species placed in the subfamily Cyclanthoideae.
Shortly thereafter, a series of reports on the
Correspondence: Nico M. Franz, Escuela de Biologıa, Universidad de Costa Rica, Ciudad Universitaria ‘‘Rodrigo Facio’’, Costa Rica;
present address: Department of Biology, University of Puerto Rico, P.O. Box 9012, Mayaguez, PR 00681, USA
e-mail: [email protected]
Pl Syst Evol 269: 183–201 (2007)
DOI 10.1007/s00606-007-0595-1
Printed in The Netherlands
Plant Systematicsand Evolution
phylogenetically opposed subfamily Carludovi-
coideae confirmed a general match with the
reproductive characteristics of tropical cantaroph-
ilous plants (Gottsberger 1977), viz. short and
crepuscular anthesis, protogyny, thermogenesis,
intense production of sweet floral fragrances, pale
floral organs, pollination chambers, protective
structures surrounding the ovaries, and non-liquid
rewards for pollinators (Gottsberger 1990, 1991;
Eriksson 1994, Seres and Ramırez 1995; Anderson
and Gomez 1997; Franz and O’Brien 2001a, b;
Franz 2003a, 2004; Franz and Valente 2005). The
pollinators were identified as members of the
pantropical weevil tribe Derelomini Lacordaire
(‘‘derelomine flower weevils’’ sensu Franz 2006),
placed within or near the genus Phyllotrox Schoen-
herr. Pollen transfer onto concealed stigmata,
feeding, and mating activities were observed
directly, and oviposition was frequently inferred
from the presence of immature weevils in either
pistillate or staminate floral organs. These initial
reports pointed towards an obligatory reproductive
interdependence among cyclanths and weevils,
with strong analogies to the famous fig/wasp
interactions (e.g. Weiblen 2002). Thus, in an early
assessment of the morphological and behavioral
specializations on each side, Eriksson (1994, p. 80)
wrote that ‘‘a co-evolved plant-pollinator relation-
ship must be taken into consideration.’’
This paper presents the first quantitative study
of the pollination biology and reproductive trade-
offs in a cyclanth/weevil mutualism involving
Asplundia uncinata Harling and its primary
pollinator. Field work undertaken at La Selva,
Costa Rica, was designed to document the
phenology, anthesis, reproductive system, and
the rate of fruit maturation versus abortion in A.uncinata plants; as well as the pollinator effi-
ciency, mating and oviposition activities, and the
larval development of the derelomine weevils.
Parallel yet less intensive observations of ten
additional cyclanth species made it possible to
assess the relative pollinator specificity and likely
mechanisms for reproductive isolation in cyc-
lanths. The results permit a more precise charac-
terization of a unique plant/pollinator interaction.
Materials and methods
Study site and plant taxa. The study was carried out
in the tropical wet forest of La Selva Biological
Station (Organization for Tropical Studies), Heredia
Province, Costa Rica (10� 260 N, 83� 590 W, ca. 50 m
above sea level; see McDade and Hartshorn 1994),
from December 1996 to October 1998. Experimental
tests of the plant reproductive system and pollinator
efficiency were conducted from May to October
1998.
The cyclanth species were identified according to
Hammel (1986); voucher specimens are available at
the Instituto Nacional de Biodiversidad (INBio) in
Santo Domingo de Heredia, Costa Rica. The focal
species A. uncinata is a perennial herb that occurs in
dense populations in the understory of La Selva
(Fig. 1A). The inflorescence of members of the
Carludovicoideae is a monoecious spadix covered by
several spathes. The small flowers are unisexual and
densely arranged in a spiral along the main axis. In
close resemblance to a chess-like mosaic, four stami-
nate flowers surround and surpass a single pistillate
flower, thereby forming reticulate air spaces above the
stigmata (Fig. 1A). Four whitish filiform staminodes
are associated with each pistillate flower and represent
the most conspicuous organs at the peak of anthesis
(Fig. 1A). Both types of flowers have tepals that may
contain apical glandular tissues secreting oily sub-
stances. Harling’s (1958) monograph provides further
detail on inflorescence morphology.
The following species were studied in addition to A.uncinata: A. euryspatha Harling, A. sleeperae Grayum
& Hammel, A. utilis (Oerst.) Harling, and A. vagansHarling – all congeners at La Selva and often trunk- or
tree-climbing; Carludovica rotundifolia H. Wendl. ex
Hook. fil. and C. sulcata Hammel – commonly named
‘‘Panama-hat palms’’ and occurring in more exposed
areas; Chorigyne pendula (Hammel) R. Eriksson, a
subcanopy epiphyte which was accessed using Perry’s
(1978) tree climbing technique; Dicranopygium um-brophilum Hammel, a small understory species, and D.wedelii Harling which inhabits emerging rocks in La
Selva’s river beds; and the tree-climbing Evodianthusfunifer Lindm.
Phenology, anthesis, and fruit set. The phenology
of A. uncinata plants was studied from July 15 to
December 3, 1997. A total of 976 plants was monitored
at five separate locations. Each plant with an
emerging inflorescence received an individual tag. The
184 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
inflorescence development and time of flowering was
checked on a daily basis. Phenological data on other
cyclanths species were recorded less frequently.
In order to obtain a full picture of the species’
reproductive biology, multiple individual inflores-
cences were studied using different observational
Fig. 1. A Population of A. uncinata plants in the understory of La Selva, Costa Rica. B Representation of 4 + 1
floral arrangement along the central axis of a cyclanth inflorescence (after Harling 1958); sf = staminate (#)
flower, pt = pistillate tepal; st = staminode; pf = pistillate ($) flower. C Opening inflorescence of A. uncinata,
pistillate phase, at 03:30 a.m. during the first day of anthesis. The inflorescence spathes are deflected and the
staminodes are extended and fragrant
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 185
techniques and treatments. The arrival of derelomine
weevil pollinators was seen as the definitive beginning
of the attraction phase (since the pollinators arrive in
response to a stimulus produced by the plant, the
actual start of the pistillate phase preceded their
arrival). On the other hand, the darkening and drying
of the stigmata marked the end of the receptive phase;
this was reaffirmed by repeated applications of a
peroxidase indicator (Sigma) until the second morning
of anthesis. The duration of the staminate phase was
measured directly by observing the sequential opening
of the anthers. Any thermogenetic activities were
documented by inserting the wire-like tip of a NiCr-Ni
thermocouple element (Ahlborn) at mid length into
the central axis of an inflorescence, approximately
1 cm past the bases of the staminate flowers. Tem-
perature readings were taken every 10 minutes from
01:30 to 08:30 a.m. on both the first and second
morning of flowering, and compared to the local
ambient temperature measured with a separate
thermometer placed nearby. The intensity and com-
position of the floral fragrances was described
subjectively.
In continuation of anthesis the marked inflores-
cences were revisited once per week and categorized
as either (1) removed by predators, (2) rotting/aborted
by the plant, or (3) maturing successfully. Categories
(1) and (2) typically occurred during the first month
after flowering. The duration of the fruiting process
was noted, including observations on infructescence
coloration and aroma, as well as potential agents for
seed dispersal.
Plant reproductive system. Opening inflo-
rescences of A. uncinata were subjected to four
distinct treatments of enclosure and subsequent
manual pollination. All treated inflorescences were
enclosed in appropriately sized cages made out of
copper wire and covered with fine-meshed stocking
permitting gas exchange (Kearns and Inouye 1993).
Isolation from potential weevil pollinators was
maintained for approximately 24 hours, from 05:00
a.m. of the first day of anthesis to 05:00 a.m. of the
second day. During this period a subset of the
inflorescence cages were lifted for a brief moment
for manual pollen application. A pair of dissecting
forceps was used to first remove all staminate flowers
at the base, without damaging the pistillate flowers.
The donor inflorescence (in staminate phase) was then
carefully and repeatedly rolled over the receptor
inflorescence (in pistillate phase), until all stigmata
had a large and clearly visible amount of pollen on
their surface. In treatments of xenopollination, the
donor and receptor inflorescences originated from
plants that were separated by a distance of at least
200 m, whereas autopollination was performed within
the same inflorescence. The treatments were as
follows: (1) without manual pollination – the control
treatment; (2) xenopollination during the pistillate
phase, at 05:00 a.m. of the first day of anthesis; (3)
xenopollination during the staminate phase, at 04:00
a.m. of the second day of anthesis; and (4)
autopollination during the staminate phase, at 04:00
a.m. of the second day of anthesis – the only phase
when autopollination is possible.
The development of the treated inflorescences was
recorded at two months after flowering, and catego-
rized as either (1) rotting/aborted by the plant, or (2)
maturing successfully. Infructescences in the latter
category were then collected to estimate the average
number of maturing seeds per ovary. For this purpose
ten berries were randomly selected and dissected
under a microscope for seed counts. As a measure of
control, the averages from the manual pollination
treatments were compared to those obtained from
infructescences pollinated under natural conditions.
Inflorescence visitors versus pollinators. The
abundance of different weevil species on A. uncinatainflorescences was assessed during three distinct
phases of anthesis: (1) attraction phase of the first
day, from 05:30 to 06:30 a.m.; (2) intermediate phase
of the first day, from 02:00 to 05:00 p.m.; and (3)
staminate phase of the second day, from 05:00 to
08:00 a.m. The number of captured visitors was
maximized by cutting off entire inflorescences and
immediately immersing them in Ziploc1 containers
with 95% ethanol. The weevils were identified to
species according to the taxonomy reviewed in
O’Brien and Wibmer (1982), Wibmer and O’Brien
(1986), and Franz (2006; see this reference for
deposition records of vouchers); and their totals
were counted.
The behavior of weevils on the inflorescences was
furthermore observed directly using a 10 · hand lens
in combination with a 3 · headband magnifier. The
observations focused on determining which floral
structures were occupied most frequently by the
individuals of different species, with particular atten-
tion to their use of the staminodes and distal parts of
the staminate flowers versus the stigmata of the
pistillate flowers. The abundance counts and behav-
ioral data were then pooled to form the following
categories: (1) primary pollinator – species with the
186 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
highest number of individuals during all phases of
anthesis and abundant contacts with the receptive
stigmata; (2) secondary pollinator(s) – species with
lower specimen counts yet also regularly contacting
the stigmata; and (3) non-pollinator(s) – species
whose individuals are largely absent during one or
more phases of anthesis and which are rarely or never
in contact with the stigmata.
Pollinator efficiency. ‘‘Pollinator efficiency’’
(Inouye at al. 1994) was understood as the quantity
of pollen transferred to the stigma (denominator)
divided by the quantity of pollen carried by the
vector (numerator). However, since A. uncinata has
approximately 60 pistillate flowers per inflorescence
and was on average visited by 75 pollinators who
remained on the cones for nearly 24 hours, it was not
possible to quantify a single event of pollen transfer. It
was also not possible to obtain all measurements related
to pollinator efficiency without slight interference with
the pollination process. As a pragmatic approach
to overcome these limitations, eight inflorescences
were selected at random. At each inflorescence, ten
individuals of the primary pollinating species were
captured at the time of arrival, i.e. 05:30 a.m. during the
attraction phase. The weevils were caught with a pair of
soft dissecting forceps while crawling towards the
stigmata, and immediately transferred into marked
and precooled Eppendorf tubes, thereby minimizing
the loss of pollen. The quantity of pollen present on
the body surface was subsequently determined using
Beattie’s (1971) method. At 04:00 a.m. of the
following day (staminate phase, prior to the departure
of pollinators), the inflorescences were cut off and
preserved in 95% ethanol (see above), which permitted
counts of the total number of pollinators present. The
total amount of pollen carried by the pollinators
(numerator) was obtained by multiplying the number
of pollinators captured at that later time by the average
of pollen grains present on the ten individuals captured
earlier. This product was then divided by the number of
pistillate flowers on each inflorescence. Finally, ten
flowers per inflorescence were selected at random and
prepared for counts of growing pollen tubes under a
fluorescence microscope (Kearns and Inouye 1993).
The rate of germination for up to 100 pollen grains per
stigma was assessed. The quantity of transferred pollen
(denominator) was calculated as the product of the
average of growing pollen tubes per stigma and the
inverse value of the average germination rate.
Pollinator reproduction. The mating behavior of
the primary pollinating species was observed using a
small light source and a 10 · hand lens. Several
staminate flowers were removed at the base with a
pair of dissecting forceps to facilitate visual access to
the pistillate flowers located underneath. More than
ten hours of weevil feeding, mating, and oviposition
activities were filmed using a Sony CCD-FX230 video
camcorder. The recordings were later analyzed in the
laboratory.
Following anthesis of A. uncinata, the presence
and development of immature life stages of the
primary pollinating species in the floral and fruiting
organs was monitored. Rotting as well as successfully
maturing infructescences were dissected at an age of
1–6 weeks. Adult weevils were also reared from
rotting infructescences collected 7–10 days after
anthesis and placed in plastic containers with a
permeable cover to allow gas exchange. The emerging
adults were collected from these structures on a daily
basis. Immatures were reared from the staminate
flowers by removing the latter with a pair of dissecting
forceps, at 2–3 days after anthesis. The flowers were
then located in plastic containers furnished with a
small amount of soil and leaf litter.
Additional studies – pollinator attraction. Two
additional studies were carried out on A. uncinataplants. One study was intended to confirm an initial
observation, i.e. that larger and thermogenetically
more active inflorescences attract more pollinators.
To this end, the peak of thermogenesis of select
inflorescences was recorded using a NiCr-Ni
thermocouple element (see above). Their volume
was estimated by measuring the spadix length (h)
and width (r), and entering these values into the
equation pr2*h, given their resemblance with the
shape of a cylinder. The number of pollinators was
assessed by cutting off the observed inflorescences
from 05:30 to 06:30 a.m. of the attraction phase,
shortly after they had reached their thermogenetic
peak, and immersing them into containers with 95%
ethanol (see above).
The other study was carried out to test whether
inflorescence coloration plays a critical role in polli-
nator attraction. The experimental set-up was modeled
after Gottsberger and Silberbauer-Gottsberger (1991).
Prior to entering the pistillate phase, select inflores-
cences were covered with an opaque cloth which
nevertheless allowed the dispersal of floral fragrances.
The experiments were run from 05:30 to 06:30 a.m.
During this period, two elongate-ovoid pieces of thin
cardboard were located next to the covered inflores-
cence. They were situated on opposed sides, at a
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 187
distance of approximately 20 cm from each other.
One piece of cardboard was white and the other grey.
The weevils arriving on each of these inflorescence
‘‘models’’ were immediately removed with an aspira-
tor, and later identified and counted.
Results
Phenology, anthesis, and fruit set. The period
of flowering of Asplundia uncinata at La Selva
extended from late May to December, with two
peaks of intensity in early August and mid
October (Fig. 2). However, no more than 335
out of 976 marked plants (34.3%) produced
inflorescences, and 243 of these flowering plants
(72.5%) had only one inflorescence (average:
1.3 ± 0.6 SD; range: 1–5 inflorescences). Two
plants (0.6%) had inflorescences opening on
consecutive mornings.
The flowering of A. uncinata inflorescences
follows a pattern typical for beetle-pollinated
plants. The spathes fold back and the staminodes
extend completely in the 48 hours prior to anthesis
(Fig. 1C). The anthesis has a duration of minimally
24 hours (N = 23), with the most critical events
occurring in the twilight of two consecutive
mornings. The attraction phase begins at 04:55 to
05:30 a.m. of the first day of flowering. At this time
the pollinators start to arrive on the staminodes and
occupy various floral structures (Fig. 3A–C).
Depending on the amount pollen transferred
during the first hours, the receptive phase may
end as soon as 08:00 a.m. of the same morning (i.e.
3 hours later), indicated by a darkening and drying
of the stigmata, or extend until 05:00 a.m. of the
second morning (i.e. 24 hours later). By this time
the staminodes have deteriorated or fallen off. The
staminate phase begins at 02:40 to 04:35 a.m. of
the second morning, before the dawning of light,
and lasts until 03:20 to 05:10 a.m. During this
period pollen is released in large quantities
(Fig. 3D), and shortly thereafter the inflorescences
appear abandoned. Within the next five days the
staminate flowers begin to rot and finally detach
(but see below).
The inflorescences of A. uncinata displayed
thermogenetic activity during both phases of
anthesis (Fig. 4). During the pistillate phase the
peak of temperature in the center of the spadix
occurred from 04:15 to 05:50 a.m. and reached
5.5 ± 1.3 �C above ambient temperature (N = 5).
The peak was slightly lower during the staminate
Fig. 2. Phenology of A. uncinata at La Selva (N = 976 plants), as observed from July 15, 1997 (= week 1 on
the x- axis) to December 03, 1997 (= week 21)
188 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
phase, reaching 5.2 ± 1.6�C above ambient
temperature, and taking place from 03:55 to
04:55 a.m. (N = 5). The highest temperatures of
the staminate phase thus came an hour earlier in
the morning than those of the pistillate phase.
Floral fragrances reminiscent of lemon and
raspberry were noted only during the pistillate
phase, from 03:30 to 07:30 a.m. The intensity of
Fig. 3. A Inflorescence of A. uncinata, attraction phase, at 06:00 a.m. during the first day of anthesis. The
staminodes are mainly occupied by individuals of Derelomini gen. 1 sp. 1 and Staminodeus vectoris. B and CAdults of the primary pollinator Derelomini gen. 2 sp. 1 entering the interfloral openings to access the receptive
stigmata. D The same inflorescence at the end of the staminate phase, at 06:00 a.m. during the second day of
anthesis. The staminodes have withered and the pollen masses have been released
Fig. 4. Thermogenetic activities of an A. uncinata during the pistillate and staminate phase, as measured on the
mornings of August 04 and 05, 1997, respectively
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 189
fragrance volatilization peaked from 06:00 to
07:00 a.m. and appeared to be closely linked to
the thermogenetic activities, with a time lag of
approximately 30 minutes.
Only 11.8% of the monitored infructescences
matured successfully (N = 448; Fig. 5A). The
remaining infructescences were either removed
by predators (37.1%) or prematurely aborted by
the plant (51.1%). The collared peccary Pecaritajacu (Linnaeus; see Wilson and Reeder 1993)
was considered the most common predator of
immature A. uncinata cones. The rotting of fruits
is an all-or-nothing phenomenon, diagnosable
within days after flowering by the incomplete
detachment of the staminate flowers from the
spadix (Fig. 5B). The period of decomposition
lasts approximately four weeks. On the other
hand, the maturation of successful infructes-
cences takes up to four months. Towards the
end of this period they turn yellowish to light
orange and emit scents remiscent of (spicy)
guanabana (Annona muricata Linnaeus). Fruit
dispersal by birds and mammals is likely (see
also Harling et al. 1998, Knogge et al. 1998).
Plant reproductive system. Without manual
pollination, none of the enclosed inflorescences of
A. uncinata matured (N = 28). In contrast, 83.3%
of the inflorescences that were xenogamously
pollinated during the pistillate phase were able
to set fruit (N = 30). This rate was significantly
higher than 47.4% successful maturation in
xenopollination treatments during the staminate
phase (N = 57; v2 = 10.6, p < 0.005). Inflo-
rescences that were autopollinated during the
staminate phase matured in 50.0% of the trials
(N = 30), with no significant differences in the
rate of fruit set between the two latter treatments
(v2 = 0.2, p > 0.5).
The number of viable seeds per berry was
significantly higher in inflorescences that were
manually pollinated during the pistillate phase
(286 ± 94 seeds; N = 25) than in those pollinated
under natural conditions (98 ± 46 seeds; N = 38;
t = 9.3, p < 0.001). Similarly lower numbers of
seeds were obtained after xenopollination during
the staminate phase (90 ± 52 seeds; N = 15;
t = 13.5, p < 0.001), and after autopollination
during the staminate phase (158 ± 93 seeds;
Fig. 5. A Successfully maturing infructescence of A. uncinata, approximately 15 days after anthesis. The
staminate flowers have faded and largely become detached. B Rotting infructescence, approximately 10 days
after anthesis. The putrified staminate flowers remain attached to the spadix. C Dissected rotting infructescence
with larvae of Derelomini gen. 2 sp. 1 feeding near the central axis (see arrow)
190 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
N = 12; t = 13.6, p < 0.001). The treatments of
enclosure and manual pollination were neverthe-
less effective, yielding higher seed counts than
observed in nature. The average of seeds per
berry never dropped below 40 in the maturing
infructescences (N = 90).
Inflorescence visitors versus pollinators. The
inflorescences of A. uncinata were regularly
visited by four different species of derelomine
flower weevils (Fig. 6). Three of these are
undescribed, including the primary pollinator
‘‘Derelomini gen. 2 sp. 1’’ sensu Franz (2006;
Fig. 7). The adults of this species arrive on the
inflorescences in higher numbers than any other
visitors. Upon landing on the fragrant staminodes
at the beginning of the attraction phase, they
immediately begin to move towards the spadix.
The weevils typically carry on their entire surface
pollen from previously visited inflorescences
which were in their staminate phase. They are
small enough to pass through the entrance holes
between the staminate flowers and thus reach the
reticulate interior spaces where the stigmata are
located (Fig. 3B and C). The adults will occupy
these spaces for the next 24 hours while engaging
in mating and oviposition activities. In the
process of moving around the cone they have
abundant contacts with the pistillate flowers and
can thereby effect pollination. Most individuals
leave the inflorescences shortly after pollen is
released by the staminate flowers (Fig. 3D).
Fresh pollen loads are deposited on their body
as they depart towards other inflorescences in
their attraction phase.
Weevils of ‘‘Derelomini gen. 2 sp. 2’’ sensuFranz (2006) were considered secondary pollin-
ators of A. uncinata. Their behavior resembles
that of the primary pollinators, yet overall they
are much less abundant on the inflorescences. On
the other hand, ‘‘Derelomini gen. 1 sp. 1’’ and
Staminodeus vectoris Franz did not function as
pollinators. Both species are specialized to feed
on and oviposit into the staminodes. The adults’
activities are restricted to these ephemeral
organs, as they never enter the inner spaces of
the inflorescences. They will detach the stamin-
odes with their mandibles, fall down, and
continue their reproductive activities in the leaf
Fig. 6. Abundance of four species of derelomine flower weevils on the inflorescences of A. uncinata during the
attraction, intermediate, and staminate phases of anthesis (see text for further detail). The average values are
displayed with standard deviation
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 191
litter. This behavior explains their absence in
samples taken during the staminate phase
(Fig. 6).
Other visitors of A. uncinata at La Selva
included members of the sap beetle genus
Mystrops Erichson (Nitidulidae) as well as an
unidentified aleocharine species (Staphylinidae).
Their patterns of visitation were irregular and not
well synchronized with the process of flowering,
rendering them ineffective as pollinators.
Pollinator efficiency. The values used to
estimate the pollinator efficiency of the primary
pollinator Derelomini gen. 2 sp. 1 are summarized
in Table 1. On average the weevils carried
61 ± 76 pollen grains on their surface at the
time of arriving on the inflorescences of A.uncinata (range: 0–470 pollen grains; N = 80).
The sampled inflorescences were visited by
77.3 ± 47.3 individuals of this species (range:
20–153 individuals; N = 8). The selected
inflorescences had 59.0 ± 11.2 pistillate flowers
(N = 8). Dissections of the latter revealed an
average of 45.8 ± 33.2 pollen tubes growing from
the stigmatic surfaces towards the ovaries (range:
0–235; N = 80). The rate of pollen germination
was 84.2 ± 9.5% (range: 53.3–98.0%; N = 80).
As a result of these measurements, the estimated
quantity of pollen carried (numerator) ranged
from 14.8 to 236.6 pollen grains, whereas the
amount of pollen transferred (denominator)
varied from 11.2 to 119.6 pollen grains per
stigma. These values translate into a pollinator
efficiency of 50.6–83.8% (Table 1).
Pollinator reproduction. In addition to
feeding on various floral structures and taking
prolonged resting periods within the inner spaces,
the adults of Derelomini gen. 2 sp. 1 mated and
oviposited into the inflorescences. Mating pairs
Fig. 7. Habitus of a male of Derelomini gen. 2 sp. 1
Table 1. Pollinator efficiency of the primary pollinating species on eight inforescences of A. uncinata. The
letters a, b, c…h are used to explain how the pollinator efficiency was calculated. See text for further details
Sample
inflores-
cence
#
individual
pollinators1
Pollen
carried
(indivi-
dual)2,3
#
pistillate
flowers
Pollen
carried
(overall/
flower)
# pollen
tubes4Germi-
nation
rate4
Pollen
trans-
ferred
Pollinator
efficiency
a b c d = (a x b)
/c
e f g = e x
(1 / f)
h = g/d
1 28 40.2 76 14.8 10.2 82.2% 12.4 83.8%
2 20 42.5 51 16.7 9.8 87.4% 11.2 67.3%
3 51 90.7 69 67.0 35.4 77.2% 45.9 68.4%
4 42 25.5 51 21.0 11.8 88.0% 13.4 63.9%
5 93 81.1 68 110.9 82.5 90.8% 90.9 81.9%
6 75 95.5 50 143.3 52.6 68.2% 77.1 53.8%
7 124 41.0 62 82.0 63.8 95.7% 66.7 81.3%
8 153 69.5 45 236.3 100.6 84.1% 119.6 50.6%
1 Taken at 4:00 a.m., staminate phase (second morning of flowering)2 Taken at 5:30 a.m., pistillate phase (first morning of flowering)3 Average taken from 10 sampled pollinators4 Average taken from 10 sampled flowers
192 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
were formed shortly after arrival and tended to
remain stable until the second morning of anthesis.
Prior to oviposition the female probed various
tissues with her rostrum, and 80.0% of the eggs
were laid into the bases of the staminate
flowers (N = 25, also for all subsequent time
periods). The process of drilling a hole lasted
11.3 ± 7.0 minutes (range: 3.5–35.0 minutes),
and following the required 180� turn, oviposition
lasted 51 ± 22 seconds (range: 25–140 seconds).
Another 180� turn permitted the sealing of the
oviposition hole with a viscous substance
manipulated by the rostrum (likely masticated
plant tissue) which took 2.4 ± 1.4 minutes (range:
0.1–4.8 minutes). Twelve females were observed
for a continuous period of 5–8 hours, yet none laid
more than a single egg. Only 42 events of
oviposition were captured in total throughout the
more than 10 hours of video recordings.
The males searched for active females and
attempted mating soon after mounting them.
There was no apparent precopulatory courtship,
and no immediate rejections by mounted females.
Following the mounting three types of male
behaviors were observed: (1) persistence – a male
remained in his position on top of the female for
2–5 hours without her initiating the oviposition
routine; (2) copula – the male inserted the
aedeagus for several minutes up to one hour,
moving it slowly and often simultaneously strik-
ing the female’s head and pronotum with his
rostrum and prolegs; and (3) guarding – during
the female’s oviposition routine the male un-
mounted her and moved his head towards her
abdomen, remaining positioned there at an angle
of 90�, until oviposition was completed. In 68.0%
of the observed oviposition events the male
subsequently remounted the same partner and
also continued copulating (N = 25).
Changes in mating pairings were uncommon
and took place either when the female remained
on the outer surface of the inflorescence or
moved rapidly between the staminate flowers.
Stable pairs showed little spatial movement.
Male-male conflicts were observed during
64.0% of the critical time intervals when females
drilled oviposition holes (N = 25). The attacking
male approached from an angle of 90� and
attempted to mount the female while displacing
the defending male with his rostrum and prolegs.
The fights lasted 15 ± 8 seconds (range:
5–32 seconds; N = 16). The defending male
remained on top of the female in 68.8% of the
observed aggressions. The defeated males had no
apparent physical damage.
Immature life stages of Derelomini gen. 2 sp.
1 were located only in the staminate flowers and
rotting infructescences, but never in maturing
infructescences (N = 64 in the latter case). The
final larval stages are therefore detritivorous.
Larvae emerging from the detached staminate
flowers completed their life cycle in the leaf litter
while feeding on decaying plant matter, whereas
those remaining on the rotting spadix moved from
its periphery towards the center (Fig. 5C). The
rates of infestation were 80.0% in staminate
flowers (N = 25) and 76.4% in rotting infructes-
cences (N = 72). When infested, the former
structures yielded 3.7 ± 2.6 adults (range: 1–9
adults; N = 20) that emerged 30.6 ± 5.8 days
after flowering (range: 23–44 days; N = 74),
whereas the latter structures produced
33.4 ± 34.1 adults (range: 1–137 adults; N = 19)
that emerged 47.4 ± 17.4 days after flowering
(range: 26–106 days; N = 634). In other words,
the rotting infructescences yielded on average
nearly ten times as many weevils, although their
life cycle was prolonged by more than 15 days in
comparison to those emerging from the leaf litter.
Additional studies – pollinator attraction.Larger inflorescences of A. uncinata were corre-
lated with higher peaks of temperature during the
pistillate phase (N = 16; r = 0.001, p < 0.001),
and also attracted more weevil pollinators (N =
16; r = 0.67, p < 0.005; Fig. 8).
Weevils arriving at fragrance-dispersing yet
cloth-covered inflorescences landed more often on
the white than on the grey inflorescence models
(43.0 ± 24.6 individuals versus 26.8 ± 15.0 indi-
viduals, respectively; N = 12; t = 3.0, p < 0.05).
However, several individuals were repeatedly
observed on the opaque cloth, indicating that
olfactory cues alone are sufficient to attract the
weevils.
Natural history of other cyclanth species atLa Selva. Additional cyclanth species at La
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 193
Selva display a variety of annual flowering
patterns (Table 2), ranging from species with a
single and relatively short blooming period (e.g.
A. euryspatha and A. vagans) to species that
produce inflorescences throughout most of the
year, particularly if they stand in direct sunlight
(e.g. C. sulcata and D. wedelii). Congeneric
species had no apparent spacing in their
reproductive periods.
All species displayed a similar sequence of
anthesis lasting minimally 24 hours (see also
above). In close resemblance to A. uncinata, the
attraction phase initiated at 05:05 to 06:05 a.m.
during the first day of flowering. Its duration
depended upon the amount of pollen received by
the arriving weevils. The staminate phase began
on the following day at 01:30 a.m. (E. funifer) to
03:55 a.m. (C. sulcata), lasting 1–3 hours. The
Fig. 8. Correlation among A. uncinata inflorescence size, thermogenetic peak, and the number of visiting
derelomine weevils during the attraction phase (N = 16). The regression equation is provided for each correlation
Table 2. Phenology of ten cyclanth species at La Selva, as observed from December 1996 to October 1998.
The corresponding numbers of plants are listed in parentheses. Proportion of plants with inflorescences: • = 1–
20%; •• = 21–50%; ••• = 51–100%
Species Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Asp. euryspatha (6) • ••Asp. sleeperae (9) • • • • • •• • •Asp. utilis (5) • •• •Asp. vagans (4) •• ••Car. rotundifolia (7) • •• •Car. sulcata1 (34) • • •• • •• ••• • •Cho. pendula (85) • ••• • •Dic. umbrophilum (13) • • • •• • • • •Dic. wedelii (155) •• • • • • • •• • •• • • •Evo. funifer (4) • •• • •1 Cultivated under high exposure to sunlight
194 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
staminate flowers detached 1–5 days following
anthesis. In the two Dicranopygium species the
inflorescence spathes did not fold back until the
second day of anthesis.
The thermogenetic activities varied distinctly
among species: either the inflorescences heated
up during both the pistillate and the staminate
phase (A. utilis, C. sulcata, and C. pendula), or no
increase in temperature was observed during
either phase (A. sleeperae, N = 2; D. umbrophi-lum, N = 2; D. wedelii, N = 2; and E. funifer,
N = 3). In the former set of species the values
were as follows: A. utilis – maximum tempera-
ture above ambient temperature 5.1 ± 0.8�C
during the pistillate phase, and 3.1 ± 0.2�C
during the staminate phase (N = 2 for each
phase); C. sulcata – 3.5 ± 1.5�C during the
pistillate phase, and a significantly higher tem-
perature of 8.2 ± 3.4�C during the staminate
phase (N = 3); and C. pendula – 10.6 ± 1.3�C
during the pistillate phase, and 7.3 ± 0.9�C
during the staminate phase (N = 2). Pleasant
floral fragrances were noticeable during the
pistillate phase only. The various Asplundia
Table 3. Abundance of 15 species of derelomine flower weevils on the inflorescences of ten cyclanth species at
La Selva, as sampled during the attraction phase, from 05:30 to 06:30 a.m. Average number of weevils: • = 1–
10; •• = 11–50; ••• = 51–200. a = primary pollinator; b = secondary pollinator; c = non-pollinator. The
corresponding sample numbers are listed in parentheses
Species Asp.
euryspatha
Asp.
sleeperae
Asp.
utilis
Asp.
vagans
Car.
rotundifolia
Car.
sulcata
Chor.
pendula
Dic.
umbrophilum
Dic.
wedelii
Evo.
funifer
Gen. 2 sp. 1 ••a
(3)
•••a
(7)
•••a
(4)
••a
(3)
•••b
(5)
•••b
(5)
••a
(12)
••a
(10)
••a
(6)
Gen. 2 sp. 2 •b
(10)
•b
(10)
Gen. 2 sp. 3 •b
(3)
•b
(2)
•b
(4)
•b
(5)
•••a
(5)
Gan. undulatus •••b
(5)
••b
(5)
Per. sulcatae1 •••a
(5)
•••a
(5)
Sys. costaricencis •c
(5)
Sta. vectoris ••c
(3)
••c
(7)
••c
(4)
•c
(2)
••c
(5)
•c
(5)
•c
(8)
•c
(10)
••c
(6)
Gen. 1 sp. 1 •c
(2)
••c
(7)
••c
(4)
•c
(2)
•c
(3)
•••c
(5)
•c
(5)
•c
(8)
•c
(4)
Gen. 1 sp. 2 ••c
(5)
••c
(5)
Gen. 1 sp. 3 •c
(1)
•c
(1)
•••c
(5)
Gen. 1 sp. 4 •c
(4)
Cot. globulicollis •c
(1)
•c
(1)
Cot. stratiotricha •c(5) •c
(3)
Gen. 3 sp. 1 ••c (5) •c
(3)
1 Including some individuals of Per. carludovicae that were not separated from the more abundant species at the
time of evaluation
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 195
species had aromas reminiscent of lemon and
raspberry, whereas Carludovica resembled the
scent of ripe papaya, Chorigyne of coconut and
almond, Dicranopygium of roses, and Evodian-thus of sweet grapefruit.
The ten cyclanth species were visited by 15
species of derelomine flower weevils, of which
only six were considered pollinators (Table 3).
None of the pollinating species were restricted
to a single host species, although several were
limited to a single host genus. Derelomini gen. 2
sp. 1 sensu Franz (2006) was the primary
pollinator of all observed species of Asplundia,
Dicranopygium, and Evodianthus, displaying the
same behavioral patterns there as on A. uncinata(see above). This species was also a secondary
pollinator of Carludovica, yet it was absent on
Chorigyne which was pollinated by a presum-
ably congeneric species. Carludovica inflores-
cences were primarily pollinated by
Perelleschus sulcatae Franz & O’Brien, with
Ganglionus undulatus Franz & O’Brien and
Perelleschus carludovicae (Gunther) as addi-
tional secondary pollinators. The natural history
of Carludovica inflorescence visitors was dis-
cussed in detail in Franz (2004), including an
analysis of putative adaptations in Carludovicaspecies in response to the obligatory seed
predator Systenotelus costaricensis Anderson &
Gomez. Staminodeus vectoris and members of
the related Derelomini gen. 1 are specialized to
exploit the staminodes of cyclanths; the adults
do not transport pollen and avoid the inner
inflorescence spaces (see Franz 2003b, Franz
and Valente 2005). Cotithene species are also
non-pollinators; the relatively large adults arrive
in low numbers, are not well synchronized with
the plants’ anthesis, and proceed to mine and
oviposit into the inflorescence axis where the
larvae will later develop (see Franz 2007a).
The rate of successfully maturing infructes-
censes was comparatively high in C. pendula(54.5% maturing, 9.1% rotting, 36.4% removed
by predators; N = 75) and in D. wedelii (53.4%
maturing, 14.6% rotting, 32.0% removed by
predators; N = 103), but was not quantified
in other species. Carludovica infructescences
matured successfully in spite of apparently low
levels of pollination or high rates of infestation
by damaging weevil species (see Franz 2004).
Discussion
The plants’ perspective. The interaction among
A. uncinata and its primary pollinator Derelomini
gen. 2 sp. 1 is characterized by specializations and
complex reproductive trade-offs on each side. The
relevant ecological conditions at La Selva, in
particular the low levels of xenopollination by the
weevils, present significant obstacles to the plants’
reproductive success. Although A. uncinata is the
predominant cyclanth species blooming in the
forest understory during the latter half of the year,
its phenology overlaps with at least one
congeneric species (A. sleeperae) and five
species in other genera – all of which share the
same pollinator. The pool of potential A. uncinatapollinators is therefore reduced by individual
weevils arriving from, or departing towards,
competing host species. Such sharing of the
same weevil pollinator seems to occur in
other cyclanth communities where multiple
species overlap in their reproductive periods
(Gottsberger 1991, Eriksson 1994, Seres and
Ramırez 1995). These cumulative observations
lend support to the hypothesis that hybridization
in cyclanths is inhibited mainly by genetic rather
than ecological mechanisms (see also Eriksson
1994).
The adults of Derelomini gen. 2 sp. 1 are
relatively inefficient pollinators of A. uncinata.Morphological studies comparing pollinators
and non-pollinators in the Derelomini confirm
that the former have no derived features that
would significantly increase the adhesion of
pollen to their body surface (Franz 2006). The
range of distinct pollinator traits is thus limited
to other variables including overall body size
(the pollinators must pass through the interfloral
entrances), fidelity to and abundance on the
host, as well as a suite of behavioral features.
The pollinators of A. uncinata reach the inner
inflorescence spaces consistently and almost
immediately upon arriving. However, even
though the pollinator efficiency measurements
are premised on an approximative method and
196 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
small sample, they clearly indicate that an
average of 75–150 visitors carrying less than
100 pollen grains per individual is not sufficient
to maximize the plants’ reproductive potential.
On the other hand, the weevils’ prolonged stay
and related behaviors between the pistillate
flowers seem to contribute to a relatively high
ratio of pollen transferred onto the stigmata. In
other words, not enough weevils and pollen
made their way from one inflorescence to
another, yet most pollen grains that actually
arrived were transferred efficiently and germi-
nated with high frequency.
Adults of Derelomini gen. 2 sp. 1 sampled at
the moment of leaving A. uncinata inflorescences
during the staminate phase had 220–1,670 pollen
grains on their surface (N = 10). These values are
much higher than those measured at the time of
arrival, when 52.5% of the individuals carried
only 0–50 grains (N = 80). The difference is due
to several factors, including the observation that
the weevils will remove pollen layers from the
rostrum, head, and legs before departing from an
inflorescence. In addition, more than 20 individ-
uals per sample remained on an inflorescence for
as many as three days following anthesis. Such a
lack of synchronization further decreases the
average pollen load. Finally, departing weevils
may be unable to locate an opening inflorescence
during the same morning. After an intermittent
period of minimally 24 hours, the amount of
pollen on their body surface may be significantly
reduced.
In light of the above, the high rate of aborted
infructescences (>50%) in A. uncinata is largely
explained by low levels of pollination. Manually
pollinated inflorescences (xenopollination, pistil-
late phase) developed nearly three times as many
seeds as those pollinated by the weevils. Con-
versely, almost two thirds of the ovaries in
naturally pollinated inflorescences never received
pollen. Furthermore, there was an apparent
threshold of approximately 40 seeds per berry,
below which the infructescences were aborted.
This is a common mechanism in other pollinator-
limited plants whose presumed adaptive
functions include saving energy resources and
selecting against detrimental pollinator behaviors
(e.g. Stephenson 1981, Bronstein 1992, Huth and
Pellmyr 2000, Knight et al. 2005). In the case of
Derelomini gen. 2 sp. 1, however, aborted
infructescences presented a favorable substrate
for larval development.
The manual pollination treatments provide
clear experimental evidence that, in spite of their
pronounced protogyny, A. uncinata inflorescenc-
es are capable of producing viable seeds via
geitonogamy. This ability to set fruit through
pollen transfer within a single inflorescence is
facultative, and depends on the amount of pollen
received during the pistillate phase. If pistillate
flowers receive sufficient pollen from another
inflorescence then the stigmata will become dry
and dark during the first morning. Yet in the
opposite case, they remain receptive until the
staminate phase. The presence of weevils is
critical at this stage, given that A. uncinatacannot reproduce via parthenogenesis or apo-
mixis in the absence of pollen vectors. The
ability to reproduce via geitonogamy is gener-
ally considered advantageous when pollinators
are limiting (e.g. Lloyd 1992). A facultative
temporal overlap of the pistillate and staminate
phases appears to exist in other cyclanth species
at La Selva, e.g. in Carludovica (see also Franz
2004), Dicranopygium, and Evodianthus, as well
as in Chorigyne (see also Eriksson 1994). There
was nevertheless a distinct drop-off in the
number of fertilized seeds in pollination treat-
ments applied during the staminate phase,
suggesting that stigma receptivity had decreased
by this time.
The thermogenetic activities in A. uncinataare readily interpreted as traits whose function
is to increase the level of pollination by
derelomine weevils. As expected, larger inflo-
rescences reached a higher temperature peak
during the pistillate phase and ultimately
attracted more potential pollinators. The long-
range attraction of weevils is mediated by the
floral fragrances whose intensity appears di-
rectly related to that of the thermogenesis (see
also Gottsberger 1991), although the physiology
of this process is still unknown in cyclanths.
The pollinators are able flyers and may travel
distances of up to 250 m between inflorescenc-
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 197
es, as evidenced by pollen-carrying individuals
arriving on an isolated plant in bloom. The
recurrent heating during the staminate phase
increases the weevils’ rate of activities. Possible
reproductive benefits for the plants include
raised levels of autopollination, as well as more
weevils leaving towards other inflorescences
(Burquez et al. 1987). The temporal spacing of
the two heating events is such that the pollin-
ators are stimulated to depart a pollen-releasing
inflorescence approximately one hour before
other opening inflorescences reach their peak
of attractiveness.
The pollinators’ perspective. The adults of
Derelomini gen. 2 sp. 1 are specialized to use the
inflorescences of A. uncinata and other cyclanth
species as a resource for feeding, mating,
oviposition, and larval development. They do
not visit other plant families (Franz and Valente
2005). The behavioral synchronization with the
flowering process of the host plants distinguishes
them from the various non-pollinating taxa.
Although superficially similar, species of the
staminode-associated Derelomini gen. 1 and
Staminodeus are placed in a separate subtribe
Staminodeina, whereas all cyclanth pollinators
are members of the Phyllotrogina (Franz 2006).
Other non-pollinating taxa such as Cotithene or
Systenotelus are also assigned to the latter
subtribe. Franz and Valente (2005) proposed
that there were two independent colonizations of
cyclanths by derelomine flower weevils. In each
case, the ability to pollinate and reproduce in
dispensable floral organs such as staminate
flowers or staminodes are ancestral character
traits. These traits are largely retained in
Derelomini gen. 2 sp. 1 which has detritivorous
larvae.
Behavioral observations of Derelomini gen. 2
sp. 1 reveal a unique reproductive strategy that is
well adjusted to the host plants. Although both
sexes are present on the inflorescences in approx-
imately equal numbers (Franz, personal observa-
tion), only a subset of the females are prepared to
oviposit on a particular day. The operational sex
ratio is therefore skewed (Andersson 1994), and
the males compete for limited access to repro-
ductively active partners. It is furthermore plau-
sible to assume that females display sperm
precedence (Parker 1970; see also Franz
2003b), where the last copulating male has the
highest probability of contributing his alleles to
the offspring. Interestingly, males seemed to have
the ability to sense that a female will oviposit
into a visited inflorescence, but were unable to
predict when exactly this event would occur
during the one to three day-long visit. Given the
relative scarcity of ovipositing females and low
probability of replacing an already mounted
competitor, a favored male stragety is to associ-
ate with a female as early as possible and remain
with her until she oviposits. This would explain
the males’ persistence and guarding of partners.
In addition, the copulatory courtship may func-
tion to stimulate oviposition in the female (see
Eberhard 1996).
The females’ selection of oviposition sites on
A. uncinata inflorescences seemed to reflect a
mixed strategy with alternative combinations of
reproductive risks and rewards. Eggs laid into the
pistillate flowers (20.0% of the observed ovipo-
sition events) had no chance of survival when the
infructescences matured successfully. It is un-
clear whether the host plants produce chemical
compounds that affect the weevils’ eggs or
larvae. In the more common event of infructes-
cence abortion, however, the larvae are able to
drill deep into the rotting tissue and develop
using a more favorable substrate than the leaf
litter. The comparatively high emergence counts
from the rotting spadices support this inference.
The lower-risk yet also lower-reward strategy for
females is to oviposit into the staminate flowers
(80.0% of the events). These structures will fully
detach if the infrucescence matures, but some
staminate flowers will remain attached in the
event of abortion. In the latter case the hatched
weevil larvae must pass through the narrow bases
of the staminate flowers in order to reach the
spadix.
Synthesis of trade-offs. The apparent relation-
ship of infructescence maturation versus abortion
and its effect on weevil reproduction could lead to
an unusual though potentially stabilizing plant/
pollinator interaction. In the short term,
individuals of Derelomini gen. 2 sp. 1 benefit
198 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
reproductively by transferring low quantities of
pollen among A. uncinata inflorescences, thereby
causing high rates of infructescence abortion. Yet
by doing so, the weevils will gradually increase
their population and therefore also the pool of
potential pollinators for coming generations of
inflorescences. In the longer term, then, the
benefits of maintaining low levels of pollination
may shift away from the weevils and towards the
plants via an increase in the size of the pollinator
population. In summary, an unfavorable rate
of pollination by the weevils is not ‘‘punished’’
directly, but should ultimately return the
interaction towards a state of balance where
more pollinating weevils are available to the
plants. Another way to describe the dynamics of
the system, suggested by one reviewer, is to say
that it pulsates at more or less regular intervals
between phases of higher or lower levels of
pollination or, inversely, pollinator reproduction.
Under this scenario, there is little evolutionary
pressure selecting for weevils that are more
efficient pollinators, or for infructescences with a
lower threshold for abortion. The favorable larval
development in rotting infructescences and
potential longer-term benefits of low pollination
levels for the hosts make this cyclanth/weevil
interaction unique even in comparison to other
weevil-pollinated systems (e.g. Syed 1979;
Norstog and Fawcett 1989; Donaldson 1997;
Dufay and Anstett 2004; Franz 2004, 2007b;
Listabarth and Weber 2007; Oberprieler et al.
2007).
The reproductive trade-offs between A. unci-nata and Derelomini gen. 2 sp. 1 are influenced
by several additional variables. The most imme-
diate of these is light availability. Plants
exposed to relatively high levels of light
appeared to attract more pollinators and subse-
quently matured at a higher rate (see also Franz
1999), as has been reported for under understory
plants at La Selva (e.g. Clark and Clark 1987).
Better lighting conditions may therefore increase
the plants’ reproductive success while having a
negative effect on pollinator development. An-
other potentially significant variable is A. unci-nata’s clonal growth (Hammel 1986); what
looks from the far like a population of dozens
of individual plants may in fact often be a large,
genetically identidental clone. Geitononomy is
therefore possible at three levels (Back et al.
1996): within the same inflorescence, among
inflorescences produced by the same shoot, and
among inflorescences pertaining to the same
large clone. In general, the clonal habitus allows
A. uncinata to spread vegetatively even when no
pollinators are available. On the other hand, the
adults of Derelomini gen. 2 sp. 1 visit and may
reproduce in other cyclanth species – the
interaction is not exclusive on either side.
Lastly, the staminode-attacking adults of Der-
elomini gen. 1 sp. 1 and S. vectoris can affect
the plants’ ability to attract pollinators, partic-
ularly when they arrive in high numbers.
Outlook. The herein presented results add
new dimensions to the existing knowledge on
cyclanth pollination and reproduction. It is now
clear the different associations of hosts,
pollinators, and floral parasites involve vastly
different trade-offs for the species involved (see
also Franz 2003b, 2004; Franz and Valente 2005).
Moreover, and in spite of high levels of
evolutionary specialization on each side, the
nature of a particular interaction may depend on
several ecological factors such as inflorescence
density and pollinator availability, light
conditions, competing host and pollinator
species, visiting floral parasites, and alternative
reproductive strategies such as clonal growth. In
this sense, cyclanth/weevil interactions are a rich
system for comparative evolutionary and
ecological studies whose complexities are for the
most part unknown. Valuable future directions for
research include chemical analyses of the floral
fragrances and of potential compounds inhibiting
larval development in the fruits, as these factors
appear to have played a major role in the attraction
and reproduction of the weevils.
The author would like to thank Gerhard Gotts-
berger for encouragement to investigate cyclanth/
weevil interactions. William Eberhard, Paul Hanson,
and Mauricio Quesada offered advice throughout the
study, and Charles O’Brien was instrumental in
introducing the author to the weevils’ taxonomy.
Maribel Vargas at the Unidad de Microscopia Elect-
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 199
ronica, Universidad de Costa Rica, assisted in
producing the SEM of the pollinating species. Com-
ments made by two anonymous reviewers improved
the manuscript. Funds to carry out field work at La
Selva were provided by the German Academic
Exchange Service, the German National Merit Foun-
dation, and the Organization for Tropical Studies. The
author’s systematic research on derelomine flower
weevils was supported by several graduate stipends
from Cornell University as well as a Doctoral
Dissertation Improvement Grant (DEB-0206093,
with Bryan Danforth) from the National Science
Foundation.
References
Anderson RS, Gomez-PLD (1997) Systenotelus, a
remarkable new genus of weevil (Coleoptera:
Curculionidae) associated with Carludovica (Cyc-
lanthaceae) in Costa Rica and Panama. Rev Biol
Trop 45: 887–904
Andersson MB (1994) Sexual selection, Princeton
University Press, New Jersey
Back AJ, Kron P, Stewart SC (1996) Phenological
regulation of opportunities for within-inflorescence
geitonogamy in the clonal species, Iris versicolor(Iridaceae). Amer J Bot 83: 1033–1040
Beach JH (1982) Beetle pollination of Cyclanthusbipartitus (Cyclanthaceae). Amer J Bot 69: 1074–
1081
Beattie AJ (1971) A technique for the study of insect-
borne pollen. Pan-Pac Entomol 47: 82
Bronstein JL (1992) Seed predators as mutualists:
ecology and evolution of the fig/pollinator interac-
tion. In: Bernays EA (ed) Insect-plant interactions,
volume IVreprint, CRC Press, Boca Raton, pp 1–44
Burquez A, Sarukhan KJ, Pedroza AL (1987) Floral
biology of a primary rain forest palm, Astrocaryummexicanum Liebm. Bot J Linn Soc 94: 407–419
Clark DE, Clark DB (1987) Temporal and environ-
mental patterns of reproduction in Zamia skinneri,a tropical rain forest cycad. J Ecol 75: 135–149
Croat TB (1978) Flora of Barro Colorado Island,
Stanford University Press, Stanford
Donaldson JS (1997) Is there a floral parasite mutu-
alism in cycad pollination? The pollination biology
of Encephalartos villosus (Zamiaceae). Amer J Bot
84: 1398–1406
Dufay M, Anstett M-C (2004) Cheating is not always
punished: killer female plants and pollination by
deceit in the dwarf palm Chameropsis humilis. J
Evol Biol 12: 862–868
Eberhard WG (1996) Female control: sexual selection
by cryptic female choice, Princeton University
Press, New Jersey
Eriksson R (1994) The remarkable weevil pollination
of the neotropical Carludovicoideae (Cyclantha-
ceae). Pl Syst Evol 189: 75–81
Franz NM (1999) Biologıa Reproductiva de Algunas
Ciclantaceas (Cyclanthaceae) y de los Picudos
Asociados (Coleoptera: Curculionidae). Unpubl
M.Sc. Thesis, University of Costa Rica, San Jose,
Costa Rica
Franz NM (2001) Description and phylogeny of
Staminodeus, a new genus of Derelomini (Coleop-
tera: Curculionidae) associated with Cyclantha-
ceae. Coleop Bull 55: 411–432
Franz NM (2003a) Systematics of Cyclanthura, a new
genus of Derelomini (Coleoptera: Curculionidae).
Insect Syst Evol 34: 153–198
Franz NM (2003b) Mating behaviour of Staminodeusvectoris (Coleoptera: Curculionidae), and the value
of systematics in behavioural studies. J Naturalist
Hist 37: 1727–1750
Franz NM (2004) Analyzing the history of the
derelomine flower weevil-Carludovica association
(Coleoptera: Curculionidae; Cyclanthaceae). Biol
J Linn Soc 81: 483–517
Franz NM (2006) Towards a phylogenetic system of
derelomine flower weevils (Coleoptera: Curculion-
idae). Syst Entomol 31: 220–287
Franz NM (2007a) Revision, phylogeny, and natural
history of Cotithene Voss (Coleoptera: Curculion-
idae). Zootaxa (in press)
Franz NM (2007b) Pollination of Anthurium by
derelomine flower weevils (Coleoptera: Curculion-
idae). Int J Tropical Biol 55: 269–271
Franz NM, O’Brien CW (2001a) Revision and
phylogeny of Perelleschus (Coleoptera: Curculion-
idae), with notes on its association with Carludo-vica (Cyclanthaceae). Trans Amer Entomol Soc
127: 255–287
Franz NM, O’Brien CW (2001b) Ganglionus, a new
genus of Derelomini (Coleoptera: Curculionidae)
associated with Carludovica (Cyclanthaceae). Ann
Entomol Soc Amer 74: 835–850
Franz NM, Valente RM (2005) Evolutionary trends in
derelomine flower weevils: from associations to
homology. Invert Syst 19: 499–530
Gottsberger G (1977) Some aspects of beetle pollina-
tion in the evolution of flowering plants. Pl Syst
Evol (Suppl 1): 211–226
200 N. M. Franz: Trade-offs in a cyclanth/weevil pollination system
Gottsberger G (1990) Flowers and beetles in the South
American tropics. Bot Acta 103: 360–365
Gottsberger G (1991) Pollination of some species of
the Carludovicoideae, and remarks on the origin
and evolution of the Cyclanthaceae. Bot Jahrb Syst
113: 221–235
Gottsberger G, Silberbauer-Gottsberger I (1991)
Olfactory and visual attraction of Erioscelis emar-ginata (Cyclocephalini, Dynastinae) to the inflo-
rescences of Philodendron selloum (Araceae).
Biotropica 23: 23–28
Hammel BE (1986) The vascular flora of La Selva
Biological Station, Costa Rica – Cyclanthaceae.
Selbyana 9: 196–202
Harling G (1958) Monograph of the Cyclanthaceae.
Acta Hort Berg 18: 1–428, 110 plates
Harling G, Wilder GJ, Eriksson R (1998) Cyclanth-
aceae. In: Kubitzki K (ed) The families and genera
of vascular plants, volume 3. Flowering plants,
monocotyledons: Lilianae (except Orchidaceae),
Springer, Hamburg, pp 202–215
Heide F (1923) Bloembestuiving in West-Java. Meded
Alg Proefstn Landbou 14: 20–37
Huth CJ, Pellmyr O (2000) Pollen-mediated selective
abortion in yuccas and its consequences for the
plant-pollinator mutualism. Ecology 81: 1100–
1107
Inouye DW, Gill DE, Dudash MR, Fenster CB (1994)
A model and lexicon for pollen fate. Amer J Bot
81: 1517–1530
Kearns CA, Inouye DW (1993) Techniques for
pollination biologists, University Press of Colo-
rado, Colorado
Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M,
Campbell DR, Dudash MR, Johnston M, Mitchell
RJ, Ashman T-L (2005) Pollen limitation of plant
reproduction: ecological and evolutionary causes
and consequences. Ann Rev Ecol Evol Syst 36:
467–497
Knogge C, Heymann EW, Tirado Herrera ER (1998)
Seed dispersal of Asplundia peruviana (Cyclanth-
aceae) by the primate Saguinus fuscicollis. J Trop
Ecol 14: 99–102
Listabarth C, Weber A (2007) Quantifying insect
reproduction in a nursery pollination system. How
Bactris palms sustain their weevil pollinators in
Venezuelan Amazonia. J Trop Ecol 23 (in press)
Lloyd DG (1992) Self- and cross-fertilization in
plants. II. The selection of self- fertilization. Int J
Pl Sci 153: 370–380
McDade LA, Hartshorn GS (1994) La Selva Biolog-
ical Station. In: McDade LA, Bawa KS, Hespenhe-
ide HA, Harsthorn GS (eds) La Selva: ecology and
natural history of a neotropical rainforest, Univer-
sity of Chicago PressChicago, pp 6–14
Norstog KJ, Fawcett PKS (1989) Insect-cycad sym-
biosis and its relation to the pollination of Zamiafurfuracea (Zamiaceae) by Rhopalotria mollis(Curculionidae). Amer J Bot 76: 1380–1394
O’Brien CW, Wibmer GJ (1982) Annotated checklist
of the weevils (Curculionidae sensu lato) of North
America, Central America, and the West Indies
(Coleoptera: Curculionoidea). Mem Amer Entomol
Inst 34: 1–382
Oberprieler RG, Schiestl FP, Wanjura WJ (2007)
Detection of cone odours of the cycad Macrozamiacommunis (Zamiaceae) by Tranes weevil pollina-
tors (Coleoptera: Curculionidae) and implications
for the mechanism of cycad pollination. Invert Syst
21 (in press)
Parker GA (1970) Sperm competition and its evolu-
tionary consequences in the insects. Biol Rev Camb
Phil Soc 45: 525–567
Perry DR (1978) A method of access into the crowns
of emergent and canopy trees. Biotropica 10: 155–
157
Schremmer F (1982) Bluhverhalten und Bestaubungs-
biologie von Carludovica palmata (Cyclanthaceae)
- ein okologisches Paradoxon. Pl Syst Evol 140:
95–107
Seres A, Ramırez N (1995) Biologıa floral y poli-
nizacion de algunas monocotiledoneas de un bos-
que nublado venezolano. Ann Missouri Bot Gard
82: 61–81
Stephenson AG (1981) Flower and fruit abortion:
proximate causes and ultimate functions. Ann Rev
Ecol Syst 12: 253–79
Syed RA (1979) Studies on oil palm pollination by
insects. Bull Entomol Res. 69: 213–224
Weiblen GD (2002) How to be a fig wasp. Ann Rev of
Entomol 47: 299–330
Wibmer GJ, O’Brien CW (1986) Annotated checklist
of the weevils (Curculionidae sensu lato) of South
America (Coleoptera: Curculionoidea). Mem Amer
Entomol Inst 39: 1–563
Wilson DE, Reeder DM (eds) (1993) Mammal species
of the world. Smithsonian Institution Press, Wash-
ington, D.C
N. M. Franz: Trade-offs in a cyclanth/weevil pollination system 201