Reproductive Ecology of the Endangered Enigmatic Mauritian Endemic Roussea simplex (Rousseaceae)

Abstract

Roussea simplex is the sole member of the endemic family Rousseaceae from Mauritius. Once widespread and locally common on Mauritius, today R. simplex is critically endangered, with 85–90 known remaining individuals in a few scattered populations. We documented the unusual flowering and fruiting phenology and studied the pollination and seed dispersal ecology of R. simplex in the accessible flowering and fruiting populations. Endemic diurnal Phelsuma cepediana geckos were the only pollinators and the only animals eating the pulp and dispersing the tiny seeds. In experiments with captive geckos, we confirmed that geckos ingest the seeds and pass them apparently unharmed. This makes R. simplex one of the few known plants that use the same animal species for both pollination and seed dispersal. However, none of the seeds from fruits or gut-passed seeds germinated, highlighting the large gap that remains in our understanding of the germination and regeneration of R. simplex. Conservation management must address this in the near future to avoid extinction of this unique lineage, and we highlight several options for applied conservation.

Full text

REPRODUCTIVE ECOLOGY OF THE ENDANGERED ENIGMATIC
MAURITIAN ENDEMIC ROUSSEA SIMPLEX (ROUSSEACEAE)
Dennis M. Hansen1and Christine B. Mu
¨ller2
Institute of Environmental Sciences, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
Roussea simplex is the sole member of the endemic family Rousseaceae from Mauritius. Once widespread and
locally common on Mauritius, today R. simplex is critically endangered, with 85–90 known remaining individuals
in a few scattered populations. We documented the unusual flowering and fruiting phenology and studied the
pollination and seed dispersal ecology of R. simplex in the accessible flowering and fruiting populations. Endemic
diurnal Phelsuma cepediana geckos were the only pollinators and the only animals eating the pulp and dispersing
the tiny seeds. In experiments with captive geckos, we confirmed that geckos ingest the seeds and pass them
apparentlyunharmed. This makes R. simplex one of the few known plants thatuse the same animal species for both
pollination and seed dispersal. However, none of the seeds from fruits or gut-passed seeds germinated, highlighting
the large gap that remains in our understanding of the germination and regeneration of R. simplex. Conservation
management must address this in the near future to avoid extinction of this unique lineage, and we highlight several
options for applied conservation.
Keywords: Mauritius, Phelsuma, gecko, plant-lizard interactions, aggregated pollen, conservation.
Introduction
Roussea simplex Sm. is the sole member of the enigmatic
endemic family Rousseaceae from the island of Mauritius in
the Indian Ocean. Today, R. simplex is critically endangered,
occurring in only a few populations with a total of 85–90
known adult individual plants (fig. 1; table 1; Friedmann 1988;
Scott 1997). However, R. simplex was once a widespread and
locally common species in wet high-altitude forests in Mauri-
tius. For example, Vaughan and Wiehe (1937, p. 314) remarked
that in some places ‘‘an extremely thick canopy of woody lianes
(Roussea simplex ... develops about 4–6 m. above ground-level,
causing such dense shade that both terrestrial and epiphytic
plants are practically excluded.’’
The taxonomy of R. simplex has been debated since its first
description in 1789. Recently, using molecular data, Lundberg
(2001) circumscribed Rousseaceae to include a larger mono-
phyletic clade together with Carpodetaceae, a subfamily com-
prising three small genera confined to New Guinea, the Solomon
Islands, New Zealand, and Australia (Gustafsson and Bremer
1997; Gustafsson 2007). However, the monophyly of each of
the two resulting subfamilies is as well supported as that of
the larger clade, and Koontz et al. (2007) suggest maintaining
them as two separate families. The peculiar biogeography of
the Roussea-Carpodetaceae clade is evident, with R. simplex
occurring on Mauritius and the genera Carpodetus,Cuttsia,
and Abrophyllum in Carpodetaceae found much farther east
in eastern Australia, New Guinea, and New Zealand. Although
the Roussea-Carpodetaceae clade has a possible sister rela-
tionship with Campanulaceae, the phylogenetic split between
this large basal clade and the rest of the Asterales is only
weakly supported (Lundberg and Bremer 2003).
The tentative basal position of R. simplex in the Asterales,
combined with its restricted occurrence on a young volcanic
island and critical conservation status, makes R. simplex a
very interesting species that calls for in-depth ecological study
(Bremer and Gustafsson 1997; Lundberg 2001). Little is known
about the pollination biology of R. simplex, and nothing at all
is known about its seed dispersal biology; these are both impor-
tant processes in the life cycle of many plants. Given the critical
conservation status of R. simplex, a study of its pollination and
seed dispersal biology is thus pivotal for successful conservation
management.
Preliminary studies and observations show that the flowers
are visited by several animal species, including the endemic nec-
tarivorous passerine Zosterops mauritianus; the endemic day
gecko Phelsuma cepediana; several small Diptera; the intro-
duced hymenopterans Apis mellifera (honeybee), Polistes he-
braeus (wasp), and Technomyrmex albipes (ant); and a native
lepidopteran, Henotesia narcissus (Hansen 2005; Kaiser 2006;
D. M. Hansen, personal observation). Apart from the gecko,
the bird, and the ant, the other flower visitors have been ob-
served only rarely and have never been observed receiving a
pollen load by touching the anthers. Hansen (2005) showed
that although the birds entered the flowers in a way that could
result in pollen transfer, the feathers on their foreheads became
bedraggled with a mixture of sticky pollen, nectar, and dirt that
was unlikely to effect any transfer onto stigmas. Only four ob-
servations of geckos foraging for nectar in R. simplex flowers
were reported by Hansen (2005), and no experimental evi-
dence was given. No studies have investigated the seed dis-
persal biology of R. simplex, but many hours of preliminary
1Current address: Department of Biology, Stanford University, 371
Serra Mall, Stanford, California 94305, U.S.A.; e-mail: dmhansen@
stanford.edu.
2Deceased, March 7, 2008.
Manuscript received May 2008; revised manuscript received July 2008.
42
Int. J. Plant Sci. 170(1):42–52. 2009.
Ó2009 by The University of Chicago. All rights reserved.
1058-5893/2009/17001-0004$15.00 DOI: 10.1086/593050

observations in 2004, from distances of >10 m, showed that
P. cepediana was the only animal foraging on the fruits.
Here, we therefore focus on the role of P. cepediana in
the pollination and seed dispersal biology of R. simplex and
speculate on the role of other potential seed dispersers. Our
aim is threefold: first, to investigate and document the flow-
ering and fruiting phenology and the pollination and seed
dispersal biology of R. simplex; second, to address the po-
tential implications of our findings for a wider under-
standing of the biogeography and evolutionary ecology of
the Roussea-Carpodetaceae clade; and third, to discuss appro-
priate urgent conservation measures for R. simplex based on
our results.
Material and Methods
Study Species
Roussea simplex is a climbing shrub, often leaning onto
other plants and sometimes strangling them. It has large
(7–12 33–3:5-cm), rigid leaves. Flowers are borne singly in
the leaf axis and are yellow to orange, large (;2.5 cm corolla
diameter and length), and protandrous, with large, thick sta-
mens and anthers. Anthers split open lengthwise and secrete a
sticky, slimy pollen substance that adheres to any surface
touching it. The pollen grains are spheroid and ;30 mmin
diameter, with a smooth surface and five or six pores (Hansen
2005; Koontz et al. 2007). Later, stamens fall off to reveal the
thick style and the large stigma (fig. 2). Flowers have a weak,
sweet, and slightly fermented smell and produce copious
amounts of nectar (Hansen 2005).
Phelsuma cepediana is one of five endemic Phelsuma species
in Mauritius. It is a medium-sized gecko (maximum snout-vent
lengths: males ¼58 mm, females ¼49 mm) found on the wet
central plateau and the southern highland, with a generalized
diet of invertebrates, nectar, and fruit (Vinson and Vinson 1969).
Phelsuma geckos have excellent color vision (Taniguchi et al.
1999) and acute olfactory perception (Schwenk 1993). At Pe
´trin
and elsewhere on Mauritius, P. cepediana has been observed
visiting the flowers of many different native and endemic plant spe-
cies, serving as pollinators of at least some of them (Kaiser 2006;
Hansen et al. 2007; D. M. Hansen, personal observation).
The presence of the invasive and aggressive ant Techno-
myrmex albipes foraging for nectar or fruit pulp on some R.
simplex flowers and fruits has a detrimental effect on gecko
visitation rates and lowers fruit set on ant-infested flowers.
These competitive interactions are the focus of another study
(Hansen and Mu
¨ller, forthcoming) and will not be described
in detail here. In this study, all observed and experimentally
manipulated flowers and fruits were free of ant infestation.
Study Sites
Mauritius, one of the three Mascarene Islands, is an 1865-
km
2
, 8-Myr-old volcanic island ;800 km east of Madagascar.
Today, less than 2% of the original native vegetation remains
Fig. 1 Map of Mauritius showing the locations of Roussea simplex
populations, with the Black River Gorges National Park outlined in
gray. The numbers indicate the locations of the populations: 1,Le
Pouce; 2, Trou aux Cerfs; 3,Pe
´trin; 4, Bassin Blanc; 5, Pigeon Wood;
6, Piton Savanne; 7, Kanaka Crater; 8, Grand Bassin. See also table 1.
Insert: regional map showing relative locations of Madagascar and
two of the Mascarene Islands.
Table 1
Populations of Roussea simplex in Mauritius, with the Numbers of Plants Found during Surveys in 2003
and 2004 and the Current Conservation Status of the Habitats Where They Occur
Population No. of plants Population habitat conservation status
Le Pouce 29 Forestry Service Reserve, degraded native forest
Trou aux Cerfs ;5
a
Exotic pine forest
Pe
´trin 3 Conservation management area, inside national park
Bassin Blanc 17 Highly degraded native forest, outside national park
Pigeon Wood 6 Highly degraded native forest, inside national park
Piton Savanne 23 Highly degraded native forest, outside national park
Kanaka Crater 0?
b
Highly degraded native forest, outside national park
Grand Bassin 7 Highly degraded native forest, outside national park
Note. See also figure 1.
aA ‘‘handful’’ of plants were seen on the southern edge of the crater in 2005 (V. F. Florens, personal
communication).
bLast recorded from here in 1932; despite repeated surveys, we found no plants in 2003 or 2004.
43
HANSEN & MU
¨LLER—ROUSSEA SIMPLEX REPRODUCTIVE ECOLOGY

in Mauritius, most of it within the Black River Gorges Na-
tional Park (fig. 1). Most of the native vegetation is heavily de-
graded by invasive plant species.
During surveys in 2003 and 2004, we searched most of the
known sites of R. simplex and recorded the number of indi-
vidual plants (fig. 1; table 1). Plants in most of the popula-
tions (including the largest, on Le Pouce Mountain) did not
flower during the study period. Logistical reasons prevented
us from using the one other population, apart from our study
populations, that did flower (Piton Savanne), because it could
not be accessed on an almost daily basis. We thus selected
Pe
´trin and Bassin Blanc as our main study populations. Pe
´trin
holds one of the last remaining areas of upland heath in Mau-
ritius, a 2–3-m-tall, shrubby vegetation on old, weathered
Fig. 2 Flowering and fruiting phenology of Roussea simplex.A, Bud, ready to open. B, Young male-phase flower, anthers not yet dehisced. Note
the green stigma and the reflection in the plentiful nectar at the base of the flower cup. C, Close-up of male-phase flower, showing the slimy pollen
excreted in long ‘‘sausages’’ along slits in the anthers. D, Longitudinal section of male-phase flower, with one anther removed to show pale ovary and
thick style. The entire gynoecium is very rigid and hard. E, Female-phase flower; all stamens dropped off, style now swollen and pale yellow (see fig.
3C,3D). Note the still-plentiful nectar in the flower cup. F, Developing fruit, ;1 mo after flower wilted. The stigma dries and falls off after ;1 wk, and
the developing fruit swells and turns dark green, remaining hard. G, Ripe fruit, about to burst open. When ripe, fruits turn pale cream but are still very
hard except for the style, which turns soft. H, The style bursts and the central column of the ovary is pushed out. I, The slimy pulp with the embedded
small seeds is then slowly secreted over several days. Photo in Hby C. N. Kaiser; all other photos by D. M. Hansen.
44 INTERNATIONAL JOURNAL OF PLANT SCIENCES

lava. At Pe
´trin, there is a 6.2-ha fenced and weeded conserva-
tion management area (CMA), and there are three large R.
simplex plants within the CMA (hereafter, ‘‘Pe
´trin’’ refers to
the CMA only). Bassin Blanc is a small crater lake with rela-
tively good native forest around it; the population of R. simplex
is found a few hundred meters north, on a heavily degraded,
steep slope under a sparse cover of native trees 5–8 m in height,
growing in dense, shrubby vegetation dominated by the inva-
sive Psidium cattleianum (Myrtaceae). There we found 17
adult R. simplex plants growing within an area of ;0.5 ha.
However, only seven of these plants flowered during the study
period, and only three of these had enough flowers for all ex-
perimental treatments. For observations of geckos feeding on
fruits, we also used a third population, Grand Bassin, with seven
plants scattered in three small patches of heavily degraded native
vegetation.
Phenology Data
We collected data on flowering phenology, to supplement
the preliminary nectar volume and concentration data pre-
sented by Hansen (2005), and investigated fruiting phenology.
To investigate anthesis patterns, we marked buds that were
about to open, recording the sexual phase of the flowers daily
until they wilted. For nectar, we measured the standing crop
and sugar concentration in buds that were about to open and
in male- and female-phase flowers at noon. We also measured
diel nectar production, split up into diurnal and nocturnal
nectar production, for both male- and female-phase flowers.
We either emptied flowers of nectar between 0800 and 0900
hours, bagged them, and measured nectar volume and concen-
tration between 1600 and 1700 hours (diurnal production) or
emptied flowers between 1600 and 1700 hours, bagged them,
and measured nectar volume and concentration between 0800
and 0900 hours the following day (nocturnal production). We
did three replications of all of the above phenology measure-
ments on each of three plants at Pe
´trin and on three plants at
Bassin Blanc, for a total of 18 samples for each measurement.
Different flowers were used for male- and female-phase mea-
surements. Measurements were analyzed with linear mixed-
effects models (LMMs), with plants nested within site as a
random effect. To analyze sugar composition, we collected six
5-mL samples of nectar on filter paper from three male- and
three female-phase flowers, one of each from the three plants
at Pe
´trin. The samples were taken to Switzerland, and their
sugar composition was analyzed using HPLC (Bischoff Triath-
lon 900 autosampler, Bischoff RI 8120 detector, Aminex
HPX-87H column, with 5 mM sulfuric acid as eluent). To re-
cord fruiting phenology, we marked three fruits that were about
to open (see fig. 2G) on each of three plants at Pe
´trin and on
three plants at Bassin Blanc and recorded daily whether they
still secreted fresh pulp.
Hand-Pollination Experiments and Seed Set
In November 2004, we bagged buds and applied one of three
different treatments: autogamy (selfing), geitonogamy (self-
compatibility), or xenogamy (outcrossing). For autogamy, we
simply left bagged flowers untouched throughout anthesis.
For geitonogamy and xenogamy, opening buds were emascu-
lated by cutting off the anthers. Then, when flowers entered
the female phase (in which their stamens fell off, their stigma
swelled, and their color changed from green to pale green or
cream; fig. 2E;fig.3C,3D), we transferred pollen from a freshly
opened male flower on the same plant (geitonogamy) or pollen
from another plant in the same population (xenogamy). We
setuptwoflowersofeachtreatment on the three plants at Pe
´trin
and two flowers of each treatment on five plants at Bassin
Blanc. We also investigated natural levels of seed set in flowers
to which pollinators had access. We marked three flowers on
each of the three plants at Pe
´trin and three plants at Bassin
Blanc. Developing fruits from all the treatments and the open-
pollinated control flowers were harvested and seed set was
scored in late February 2005. An LMM was used to compare
seed sets of the fruits from the different treatments and the
open-pollinated fruits, with plants nested within site as a ran-
dom effect. Sample sizes were small by necessity; the majority
of plants were small and had only a few open flowers or pulp-
secreting fruits at any one time. To obtain a baseline number
against which to compare the seed sets of the experimental
and naturally pollinated flowers, we counted the number of
ovules and ovary locules in the ovaries of freshly wilted flow-
ers, using three ovaries from three plants at both Pe
´trin and
Bassin Blanc, for a total of 18 ovaries.
Flower Visitor and Frugivore Observations
Flower visitor and frugivore observations were made with
10 332-mm Leica binoculars from a distance of 4–5 m, with
the sitting observer mostly covered by either vegetation or a
133-m lightweight camouflage net. After setting up the obser-
vation post, the observer remained as motionless and quiet as
possible for 20 min before starting to record flower visitation
and fruit feeding by geckos and other animals, to allow nearby
animals to become accustomed to the presence of a human.
Observation periods were 60 or 90 min for flower observa-
tions and 90 or 120 min for fruit observations and were
spread evenly from 0700 to 1800 hours (daylight hours) in
both populations. For both flowers and fruits, 15 observation
periods were spent over 3 d (five each day) in each population.
Flowers were observed for 17 h at Pe
´trin and 19.5 h at Bassin
Blanc, and fruits were observed for 22 and 21.5 h, respec-
tively. For flowers, we observed four to eight flowers in each
period, with equal numbers of male- and female-phase flow-
ers. For fruits, we observed three to five fruits in each period.
Preliminary observations indicated that, depending on sex
and size, geckos behave differently at flowers and fruits of R.
simplex and therefore likely differ in importance as pollinators
and seed dispersers. Adult male P. cepediana are easily identi-
fiable (fig. 3A,3F), whereas female and juvenile geckos are
much harder to distinguish because of their drab brown and
green color (fig. 3D). Therefore, we divided observed geckos
into two groups: (1) adult males and (2) females plus juveniles.
We recorded both the number of visits per observation period
and the length of the visit. A visit started when a gecko first
probed a flower or started feeding at a fruit and ended when
the animal left the flower or fruit. We analyzed the gecko vis-
itation rates at flowers and fruits with an LMM with gecko
sex/age, flowers/fruits, and study population as main effects
45
HANSEN & MU
¨LLER—ROUSSEA SIMPLEX REPRODUCTIVE ECOLOGY

and observed-plant identification as a random effect. Simi-
larly, we investigated duration of visits with an LMM, with
gecko sex/age, flowers/fruits, and study population as main ef-
fects and observed-plant identification nested in observation
period as a random effect.
Finally, the flower visitation rate of P. cepediana is known
to be affected by habitat structure at a small spatial scale. In
particular, dense patches of endemic Pandanus (Pandanaceae)
species are favored microhabitats for the geckos, because they
may offer protection from attacks by the geckos’ main native
predator, the Mauritius kestrel Falco punctatus. Hence, flow-
ering plants close to these patches are likely to receive more
visits by geckos than plants away from such Pandanus patches,
as was recently demonstrated for Trochetia blackburniana
(Malvaceae; Hansen et al. 2007). At Pe
´trin, two of the three
R. simplex plants were growing at the edges of large Pandanus
Fig. 3 Phelsuma cepediana geckos foraging at flowers and fruits of Roussea simplex.A, Adult male gecko visiting a male-phase flower, getting
a smear of the slimy pollen substance (see fig. 2C) on the forehead. B,C, Adult male gecko with the characteristic smear of pollen on the forehead
(arrow), approaching and entering a female-phase flower, where some of the pollen is then deposited on the stigma. D, Female or juvenile gecko
visiting a female-phase flower. E, The smaller female and juvenile geckos must insert their heads deeper into the flower, leaving themselves
vulnerable to harassment or attack by other geckos. F,G, Adult male geckos foraging at fruits, using a mixture of licking and chewing at the pulp
and swallowing the tiny seeds in the process.
46 INTERNATIONAL JOURNAL OF PLANT SCIENCES

patches, while the last plant was more isolated, >15 m from
the closest Pandanus patch. We therefore additionally ana-
lyzed visitation rates for flowers and fruits of R. simplex at
Pe
´trin in relation to proximity to Pandanus patches (close or
away) with ANOVAs and duration of visits in relation to prox-
imity to Pandanus patches with LMMs with observation pe-
riod as a random effect.
Feeding and Germination Experiments
The observations at the fruits showed that only P. cepediana
was feeding on the pulp of R. simplex fruits (see ‘‘Flower Visi-
tor and Frugivore Observations’’). Therefore, we experimen-
tally investigated the effect of gecko gut passage on the seeds.
Three adult P. cepediana were caught near Brise Fe
´r Field Sta-
tion, located in a rain forest ;4 km north of Pe
´trin. The
geckos were kept in cages in partly shaded conditions. Ripe R.
simplex fruits with large, fresh masses of pulp with seeds were
taken from the three plants at Pe
´trin and fed to the geckos
three times, on February 7, February 9, and February 11, 2005.
Fruits were attached to the wire mesh between 0800 and 1000
hours and removed again between 1400 and 1600 hours. The
geckos were observed feeding on the fruit pulp within 20–40
min of the attachment of the fruit. Cages were checked for
gecko droppings at ;1800–1900 hours and at ;0800–0900
hours from February 7 to February 12. Any seeds found were
extracted from the dropping, examined under a dissecting mi-
croscope, and put on moist cotton wool in petri dishes, with
roughly 1.5 cm between each seed.
We set up two additional petri dishes with seeds that had
been manually extracted from ripe pulp. Each of these con-
tained 10 seeds from one fruit from three different plants, for
a total of 30 seeds in each dish. One dish contained seeds
from the three plants at Pe
´trin, and the other contained seeds
from fruits of three random plants at Bassin Blanc. Finally,
we set up two dishes with small lumps of ripe pulp contain-
ing ;10 seeds each from the same fruits and sites mentioned
above. Each of these dishes had five lumps of pulp with seeds.
All petri dishes were kept at the Brise Fe
´r Field Station near a
window but away from direct sunlight. Seeds were checked
daily, and the cotton wool was kept moist. We also attempted
to assess seed germination in the field by putting out seeds in
three sites in moist litter beneath Pandanus patches at Pe
´trin.
However, the seeds are minute, and they disappeared from all
sites within 2–5 d, usually after heavy rains, and could not be
found again. All statistical analyses were done with R.2.3.1 (R
Development Core Team 2006).
Results
Flowering and Fruiting Phenology
At Pe
´trin and Bassin Blanc, Roussea simplex flowered from
September 2004 until late January 2005, while ripe fruits were
available from early January to mid-May. Individual plants
flowered during most of the overall flowering period and could
have both flowers and ripe fruits simultaneously in the tempo-
ral overlap between flowering and fruiting. The temporal se-
quence from bud to ripe fruit is illustrated and annotated in
figure 2. Flowers were open for 6–8 d (7:160:2; all results
presented as means 61 SE; n¼18 flowers in all cases), with
the male phase lasting 2–5 (3:360:2) d and the female phase
lasting 3–5 (3:860:2) d. Fruits presented pulp for a total of
4–7 d (5:460:2; n¼18 fruits). Flowers had very large stand-
ing crops of nectar (table 2), which was hexose dominated
with only trace amounts of sucrose (glucose ¼52:8% 61:6%,
fructose ¼47:2% 61:6%, n¼6). There were no significant ef-
fects of flower sexual phase on volume or concentration of nec-
tar standing crop (P>0:1 for both).
Nectar production probably started at least 1–2 d before
anthesis, because large unopened buds contained very large
amounts of nectar, up to just above 1 mL (table 2). During an-
thesis, more nectar was produced overnight than during the
day (F1;64 ¼7:09, P¼0:010), and male-phase flowers produced
more nectar than female-phase flowers (F1;64 ¼8:81, P¼0:004).
There were no significant effects of production time or flower
sexual phase on the concentration of nectar produced (P>0:3
for both).
Hand-Pollination Experiments and Seed Set
The ovaries of R. simplex flowers contained ;2100–3300
(2572 679) ovules in 5–10 ovary locules (6:560:3; n¼18
ovaries). We had to harvest the experimental fruits before they
ripened and opened (see fig. 2G–2I) to count all the seeds.
Table 2
Nectar Phenology of Roussea simplex Buds and Flowers
Volume (mL) Concentration (%)
Range Mean 61 SE Range Mean 61SE
Bud:
Standing crop 120–1185 511.3 667.2 6.5–11.5 8.9 6.4
Male phase:
Standing crop 21–510 195.7 632.8 7.5–12.5 9.9 6.3
Diurnal production 67–305 190.1 616.5 6.5–14 9.8 6.4
Nocturnal production 110–380 234.2 615.6 7.5–14 10 6.4
Female phase:
Standing crop 42–335 163 619.1 7.5–13 10.7 6.4
Diurnal production 70–285 155.5 613.2 6.5–12.5 9.5 6.4
Nocturnal production 130–275 185.8 69.95 7.5–13 10.1 6.3
Note. Sample size for all values is 18.
47
HANSEN & MU
¨LLER—ROUSSEA SIMPLEX REPRODUCTIVE ECOLOGY

None of the flowers in the autogamy treatment produced any
seeds. Geitonogamously pollinated flowers produced fruits with
an average of 399 629 seeds (;16% seed set, n¼16 fruits),
and xenogamous fruits produced slightly more seeds, an aver-
age of 476 647 (;19% seed set, n¼16 fruits). The devel-
oping fruits from naturally pollinated flowers contained an
average of 505 652 seeds (;20% seed set; n¼18 fruits).
Numbers of seeds in these latter three categories were not sig-
nificantly different from one another (F2;40 ¼1:38, P¼0:264).
Seeds of ripe fruits were 0.7–1.1 mm long, 0.5–0.8 mm wide,
and ;0.3 mm thick, with a thin, semihard, light brown seed
coat (fig. 2I) and white endosperm.
Flower Visitor and Frugivore Observations
At the flowers, we observed Phelsuma cepediana,Zosterops
mauritianus, and several of the previously observed inverte-
brates: honeybees, flies, the ant Technomyrmex albipes, and the
butterfly Henotesia narcissus. We never observed any of the in-
sects touching the anthers with the slimy pollen substance, and
it is highly unlikely that the birds transfer pollen (Hansen
2005). The observed flowers received only occasional nectar-
foraging visits from the introduced ant T. albipes,nowherenear
the numbers of ants found on ant-infested flowers and plants
(Hansen and Mu
¨ller, forthcoming). Thus, we give detailed re-
sults only for P. cepediana flower visitation. At ripe fruits, we
observed only P. cepediana feeding on the pulp. Several frugivo-
rous birds were observed in the vicinity of fruiting plants (Z.
mauritianus and the introduced red-whiskered bulbul Pycnono-
tus jocosus), but they did not show any interest in these fruits.
Only one gecko at a time visited a particular flower or fruit.
During most flower visits, geckos inserted their heads into the
corolla, with the forehead toward the center of the flower,
thus either receiving a slimy smear of pollen at male-phase
flowers (fig. 3A) or depositing pollen on the stigma at female-
phase flowers (fig. 3C,3D). We often saw geckos with a large
part of the forehead, neck, and upper back covered in a thin
layer of the slimy pollen substance (fig. 3B,3C). When forag-
ing at fruits, geckos usually used a mixture of licking and
eating lumps of pulp with seeds (fig. 3F,3G) and otherwise be-
haved in the same way as when they were feeding on nectar at
flowers.
The analyses of the visitation rates demonstrated that P. c e -
pediana visits were significantly more frequent to flowers than
to fruits (F1;98 ¼4:75, P¼0:032; fig. 4A,4B)andthatthere
was a significant effect of gecko sex/age, with adult male
Fig. 4 Visitation rates (A,B) and duration of visits (C,D) of adult male and female/juvenile Phelsuma cepediana geckos at flowers and fruits of
Roussea simplex in the two study populations, Pe
´trin and Bassin Blanc. Bars represent mean values 61 SE. Sample size is 15 observation periods
in Aand 12 observation periods in B. Sample sizes (number of visits) for Cand Dare shown in each bar.
48 INTERNATIONAL JOURNAL OF PLANT SCIENCES

geckos visiting more frequently than females and juveniles
(F1;98 ¼41:0, P<0:001; fig. 4A,4B). There was a marginally
significant difference between study populations, with slightly
more visits per hour at Pe
´trin than at Bassin Blanc (F1;6¼5:39,
P¼0:059; fig. 4A,4B). Duration of visits varied as well, but
contrary to visitation rate results, the geckos foraged longer at
fruits than at flowers (F1;233 ¼127:8, P<0:001; fig. 4C,4D),
and they foraged longer at Bassin Blanc than at Pe
´trin
(F1;233 ¼4:05, P¼0:045; fig. 4C,4D). However, the signifi-
cant effect of gecko sex/age was similar to that observed for for-
aging at flowers, with adult males foraging longer than females
and juveniles (F1;233 ¼46:7, P<0:001; fig. 4C,4D). All inter-
actions between main effects were nonsignificant, and values
given here are from minimum adequate models with only main
effects fitted.
At Pe
´trin, there were significant effects of proximity to Panda-
nus patches on gecko visitation rates for both flowers (close:
1:44 60:13 visits=flower=h; away: 0:64 60:09 visits=flower=h;
F1;13 ¼16:7, P¼0:001) and fruits (close: 1:15 60:11 visits=
flower=h; away: 0:63 60:06 visits=flower=h; F1;10 ¼9:46,
P¼0:012). However, there were no significant effects of prox-
imity to Pandanus patches on duration of visits to flowers
(F1;80 ¼0:02, P¼0:372) or fruits (F1;56 ¼0:23, P¼0:634).
There were no significant interactions between proximity to
Pandanus and gecko sex/age (both P>0:30); hence, the re-
ported results are for models with duration of adult male and
female/juvenile visits pooled.
Feeding and Germination Experiments
Eighteen seeds were retrieved from three gecko droppings
in the cages. A further eight droppings did not contain seeds.
Gut-passage time was a few hours or less, because seeds were
found only in the evenings after the geckos had been feeding
on the fruit pulp during the day. In the gecko droppings, we
found only whole seeds with no visible marks or damage to
the seed coat; we did not find any remains of damaged seeds
(e.g., pieces of seed coat).
All the lumps of pulp were attacked by fungi after 3–5 d,
and none of the seeds germinated. The petri dishes with manu-
ally depulped seeds and the gut-passed seeds remained free of
fungal attack (dark brown or black hyphae clearly visible un-
der a dissecting microscope) for 7–12 d, after which time seeds
were attacked by fungi, too, turning dark brown or black. Sin-
gle seeds were removed from the dish as soon as they were vis-
ibly attacked, but despite staying swollen and looking healthy
until attacked by fungi, none of the seeds germinated.
Discussion
Our results strongly suggest that Phelsuma cepediana is an
efficient pollinator of Roussea simplex. Our observations con-
firmed that the geckos were the only flower visitors to con-
sistently touch the reproductive structures. Furthermore, the
geckos were the only animals observed feeding on the fruits and
acting as seed dispersers. Our feeding experiment with captive
geckos showed that they are capable of dispersing the tiny seeds
apparently unharmed. However, the germination experiments
were unsuccessful, illustrating the large gap that still remains in
our understanding of the reproductive biology of R. simplex.
Pollination and Seed Dispersal
Our results show that a reasonably efficient within-population
pollination service is being provided by P. cepediana, at least
in the southern R. simplex populations where this gecko co-
occurs. In the northern population at Le Pouce, another en-
demic gecko, Phelsuma ornata, may be an efficient pollinator.
This gecko is known to pollinate other plant species in Mau-
ritius (Nyhagen et al. 2001; Olesen et al. 2002).
Geckos foraged at flowers and fruits for prolonged periods.
For flowers, this led to repeated contacts with anthers in male-
phase flowers and stigmas in female-phase flowers. The high
volumes of nectar are likely to induce long foraging bouts. For
fruits, it was impossible to see individual seeds being swal-
lowed during the observation periods, but close-up observa-
tions confirmed that geckos ingested small lumps of pulp that
contained seeds.
We found an increase in duration of foraging visits to fruits
compared with visit duration at flowers for female/juvenile
geckos but not for males. This is probably related to domi-
nance patterns between geckos of different sizes. Males were
usually large enough to literally keep an eye out while forag-
ing at flowers (see fig. 3A), while female/juvenile geckos were
often so small that they had to insert more of their bodies into
the corolla to reach the nectar, rendering them vulnerable to
attack (see fig. 3E) and more likely to stop foraging and as-
sume vigilance for approaching geckos or predators. Fruits,
however, do not present this dilemma to small geckos.
The difference in visitation rates between study populations
is likely due to a lower overall density of geckos at Bassin
Blanc (D. M. Hansen, personal observation). The vegetation
there is very degraded, offering few of the typically favored re-
treats of Phelsuma geckos (e.g., Pandanus patches, palms, old
trees with holes; Harmon 2005; Hansen et al. 2007; D. M.
Hansen, personal observation). The spatial arrangement of fa-
vored retreats of the geckos is likely to structure their mutualis-
tic interactions with plants, and the strong positive effects of
proximity to Pandanus patches on gecko visitation rates for
both flowers and fruits of R. simplex, albeit obtained from
only three plants, confirm the results of Hansen et al. (2007).
The large, dense stands of R. simplex recorded early in the
twentieth century (Vaughan and Wiehe 1937) may, by them-
selves, have provided a favorable microhabitat for geckos, thus
attracting and maintaining a population of ‘‘in-house’’ pollina-
tors and seed dispersers.
The flowers produced large amounts of nectar, more than
typical vertebrate-pollinated flowers of a similar size (Proctor
et al. 1996). Another unusual floral trait of R. simplex is the
pale yellow, slimy, and sticky substance in which the pollen
grains are embedded, which effectively causes pollen grains
to be aggregated (Harder and Johnson 2008). One possible
function of this could be to prevent pollen theft by insects; this
would make sense for vertebrate-pollinated, long-lived flow-
ers with a protracted male phase. Indeed, we observed a small
fly and several ants getting stuck on the viscid, slimy pollen
substance. Another possibility is that it could be an adaptation
to lizard pollination, as it could make more pollen grains ad-
here to the relatively smooth scales than if the pollen was of
the normal dry type. This could function in a parallel way to
the findings of Traveset and Sa
´ez (1997), who reported that
49
HANSEN & MU
¨LLER—ROUSSEA SIMPLEX REPRODUCTIVE ECOLOGY

more pollen grains of Euphorbia dendroides were carried on
the snouts of the pollinating lizards Podarcis lilfordi if the liz-
ard snouts had been in contact with the sticky nectar before
brushing against the anthers. Finally, the sticky aggregation of
pollen grains could be linked to the large number of ovules
per ovary in R. simplex, because it would ensure increased ac-
cess to these ovules, if deposited on a receptive stigma (Harder
and Johnson 2008).
A puzzling result was that while the autogamy treatment
did not result in the production of any seeds, fruits and pulp
still developed as in fertilized fruits. This suggests that R. sim-
plex is parthenocarpic, and it could be a way for fruiting R.
simplex plants to enhance attractiveness to seed dispersers,
by increasing both the display size and the amount of reward
offered (Jordano 1989). Other studies have also suggested
parthenocarpy to be an adaptation against seed predators
(Zangerl et al. 1991; Traveset 1993). However, contrasting em-
pirical evidence means that no clear pattern for the ecological
function of parthenocarpy has emerged (Verdu
´and Garcı
´a-
Fayos 1998).
It is also noteworthy that P. cepediana probably serves as
the sole current pollinator and seed disperser of R. simplex.
There are relatively few examples of plants being pollinated
and having their seeds dispersed by the same animal species,
e.g., some mistletoe species in New Zealand (by bellbirds;
Kelly et al. 2004) and three species of columnar cacti in South
America (by bats; Soriano and Ruiz 2002). Roussea simplex is
the first documented example of a plant having the same liz-
ard species as a pollinator and a seed disperser. It is very likely
that there are more such ‘‘double-mutualistic’’ lizard-plant in-
teractions, especially on oceanic islands, where lizards are im-
portant pollinators and seed dispersers (Olesen and Valido
2003). Overall, because of their often high abundance in many
insular ecosystems (Rodda and Dean-Bradley 2002), lizards
could thus be important pollinators and dispersers for many
endangered endemic island plants. A good example of this comes
from the Balearic Islands, where local extinction of a frugivo-
rous lizard has disrupted the seed dispersal of the endangered
shrub Daphne rodriguezii (Thymelaceae) and this disruption
has been identified as the major factor in the continued decline
of the species (Traveset and Riera 2005).
Movement patterns of geckos will influence their efficiency
as mutualists, and one concern could be that lizard-mediated
gene flow is relatively restricted, in terms of both pollen trans-
port and seed dispersal. Phelsuma ornata geckos in Mauritius
move up to 87 m in a straight line in 29 h, but most recorded
movements were much shorter, ;10–20 m within 24 h (Nyha-
gen et al. 2001). Male Phelsuma are known to be territorial
(Nyhagen et al. 2001; Harmon 2005; D. M. Hansen, personal
observation), and while territoriality may ensure high levels
of geitonogamous self-fertilization, it could also reduce the in-
cidence of interplant cross-fertilization and lead to relatively lo-
cal seed dispersal only. However, smaller males and females/
juvenile geckos may travel longer distances and thus provide a
more valuable pollinating and seed-dispersing service.
Germination and Natural Regeneration
The potential role of lizard gut passage in the reproductive
ecology of R. simplex is less clear. Gut passage through frugiv-
orous lizards can have either positive (Valido and Nogales
1994) or negative or neutral effects on seed germination (Iver-
son 1985; Valido and Nogales 1994). Our study was unable
to address effects of lizard gut passage on R. simplex seeds be-
cause none of the seeds from any of the treatments germi-
nated. Under the circumstances of working in a field camp
without access to a nursery, we provided the best possible ger-
mination conditions. If the seeds had not been attacked by
fungus, they may have germinated after a longer period, or
perhaps the seeds need to pass through the gut of a specific en-
demic animal other than P. cepediana, now locally or globally
extinct, to germinate. Alternatively, the seeds might need a
special microhabitat, or they may need certain mycorrhizal
fungi to be present before they can germinate. Dispersal to cer-
tain specific microhabitats suitable for germination and growth
may be important for R. simplex. Lizards, in particular, have
been shown to deposit seeds in protected microhabitats, such
as small cracks and crevices, with positive effects on seed ger-
mination and seedling growth (Whitaker 1987; Valido and
Nogales 1994; Wotton 2002).
Biogeography and Evolution
While the monophyly of the Roussea-Carpodetaceae clade
has strong support (Lundberg 2001; Lundberg and Bremer
2003), the biogeography of the taxa is still a mystery. It is
clear that the lineage of which R. simplex is the only known
extant member is not a neoendemic on the young island of
Mauritius. Available evidence for dating the split between the
R. simplex lineage and the Carpodetaceae is unreliable at pres-
ent; the data indicate that the split could have occurred as
early as 100 million years ago (Mya) or as recently as 20 Mya
(J. Lundberg, personal communication). It is thus impossible to
distinguish between (1) a relatively recent extreme long-distance
dispersal event of R. simplex or its ancestral form from at least
Papua New Guinea to Mauritius, with subsequent extinction
of the lineage from there, and (2) a relatively recent dispersal of
R. simplex or its ancestral form from somewhere much closer
to Mauritius, e.g., India or Madagascar, with subsequent ex-
tinction of the lineage from there.
The flowers of the Carpodetaceae (Carpodetus,Cuttsia,
and Abrophyllum) are all quite small and open and are polli-
nated by thrips, flies, and beetles (Norton 1984; Williams
et al. 2001). The only known seed disperser of any Carpodeta-
ceae is the cassowary, which eats the black berries of Abro-
phyllum ornans (Crome 1975). Lizard pollination and potential
lizard seed dispersal of R. simplex could thus have evolved in
situ in Mauritius or earlier in its evolutionary history; e.g., in
Madagascar or on some of the now disappeared islands that
existed during the past 50 Myr between India and where the
Mascarene Islands now lie.
Conservation Management
During our surveys, we found 85 adult plants of R. simplex
(table 1). It is very likely that further surveys of surrounding
areas in Bassin Blanc, Pigeon Wood, and Piton Savanne will
reveal additional individuals. It is almost certain that the pop-
ulation on Le Pouce contains additional plants on the steep
northern slopes that we could not survey. However, even if
50 INTERNATIONAL JOURNAL OF PLANT SCIENCES

additional plants are located, the known populations remain
very small and widely scattered, and genetic exchange be-
tween populations is highly unlikely. We did not find plants
in one former location (Kanaka Crater), and the population
at Bassin Blanc, described as being ‘‘full of R. simplex plants
everywhere’’ in the 1980s (M. Allet, personal communication),
now contains only 17 scattered individuals.
Currently, only the three plants at Pe
´trin are growing in a
weeded and fenced CMA. The population on Le Pouce nomi-
nally grows in a Forestry Service nature reserve, but that is a
small patch of 1–2 ha of native forest surrounded by heavily de-
graded habitats. All the other populations are growing in invaded
and degraded areas, with only the plants in Pigeon Wood grow-
ing within the boundaries of the Black River Gorges National
Park. We did not find juvenile plants or seedlings in any of the
populations. Therefore, for future assignment of International
Union for Conservation of Nature red-list status, R. simplex
should be considered critically endangered and still declining.
Apart from the massive loss of native habitat between the
seventeenth century and the 1980s, one likely cause of contin-
ued decline is competitive exclusion from the preferred sub-
canopy strata between 3 and 6 m in the wet upland forests,
where especially strawberry guava Psidium cattleianum now
forms dense canopies, excluding native species. One conserva-
tion management option is therefore weeding of the invasive
plant species, although at Le Pouce, this approach may cause
the demise of one of the last strongholds of endemic ant spe-
cies (Ward 1990) and open the habitat for incursions by inva-
sive ants (Lach and Sua
´rez 2005). In another study, we showed
that invasive Technomyrmex albipes ants have a detrimental
effect on the pollination and seed dispersal interactions between
R. simplex and P. cepediana (Hansen and Mu
¨ller, forthcom-
ing). Moreover, in the short term, wholesale removal of inva-
sive species will reduce structural habitat diversity, which leads
to lower densities of Phelsuma geckos (Padayatchy 1998; Har-
mon 2005) until native vegetation has regrown. Therefore,
gradual removal, leaving patches of dense invasive vegetation
for a number of years, may be better than removing all inva-
sive vegetation at once, as is currently practiced in habitat res-
toration efforts in Mauritius.
The only way the National Parks and Conservation Service
and the Forestry Service have been able to propagate R. sim-
plex is with cuttings from adult plants, but these are difficult to
get to grow and survive in nurseries (R. Rutty, personal com-
munication). Further research on how the seeds can be brought
to germinate either in situ or ex situ is urgently required for the
production of viable plants. Ideally, availability of healthy seed-
lings, combined with habitat restoration that takes the concerns
about weeding practices raised above into consideration, should
lead to supplementary planting within existing subpopula-
tions, reestablishment of extinct subpopulations, and possibly
establishment of new subpopulations in suitable sites.
Finally, it is imperative to take into account recently ex-
tinct animal species that could have played a role in the eco-
logical interactions and the evolution of plant traits in R.
simplex. In pristine Mauritius, now-extinct birds or fruitbats
may have mediated both local and long-distance pollination
or seed dispersal events (within the island), while lizards pol-
linated and dispersed the seeds only locally. If so, then today
there is a gap in the population dynamics of R. simplex,be-
cause only one of the local pollinators and dispersers is extant.
Similarly, as a once widespread and locally common prolifi-
cally nectar-producing plant, R. simplex may have been very
important for native and endemic nectarivorous animals.
Acknowledgments
We thank Mario Allet, Raj Rutty, Vincent Florens, and
Jean-Claude Sevathian for sharing their knowledge about sev-
eral of the Roussea simplex populations. We thank the Na-
tional Parks and Conservation Service and the Forestry Service
for permission to work in the forests and for general assistance,
and the staff and volunteers of the Mauritian Wildlife Founda-
tion for never-ending support. We thank Johannes Lundberg
and Mats Gustafsson for providing information and Christo-
pher Kaiser, Nancy Bunbury, Mauro Galetti, Anna Traveset,
Johannes Lundberg, and an anonymous reviewer for construc-
tive comments. The project was funded by the Swiss National
Science Foundation (grant 631-065950 to C. B. Mu
¨ller).
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