Reproductive trade-offs in a specialized plant/pollinator...

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


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


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)


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


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)


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


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


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


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


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


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


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-


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


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-


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


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


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