Bull. Natl. Mus. Nat. Sci., Ser. B, 40(3), pp. 119–123, August 22, 2014

Repeated Visitation by a Sesarmid Crab toMale Inﬂorescences of Piper sp.
Yudai Okuyama
Department of Botany, National Museum of Nature and Science,
Amakubo 4–1–1, Tsukuba, Ibaraki 305–0005, Japan
E-mail: yokuyama@kahaku.go.jp(Received 25 May 2014; accepted 25 June 2014)

Abstract Here I report an example of repeated visits to male inﬂorescences of Piper sp. (Piperaceae) by a sesarmid crab, which has been previously unappreciated as a ﬂower visitor. The ﬂowervisiting animals were monitored using time-lapse digital photography with 2 min intervals. During
the nighttime, the crab species, most likely Scandarma lintou, visited 11 times in total onto ﬁve
inﬂorescences of the plant. The inﬂorescences exerted anthers and the crab was feeding on theanthers during the visits. Notably, some of the anthers were attached onto the ventral surface of thecrab, suggesting short-distance pollen transfer by the crab is possible. Although the present observation is not extensive, it has shed light on the potential signiﬁcance of the terrestrial crabs for theplant life histories in tropical coastal forests.
Key words : coastal forest, Luzon Island, Piper, pollination, Scandarma lintou.

Introduction
It is believed that the evolutionary success of
ﬂowering plants is partly associated with theirvarious ways of utilizing diverse animals as pollinators (Crepet and Niklas, 2009). The recent
estimation showed that among the 352,000 species of ﬂowering plants, more than 80% are animal pollinated (Ollerton et al., 2011). Pollinating
animals can be assigned to as different functionalgroups, depending on their characteristics andbehaviors, and the ﬂoral adaptation to each of thefunctional groups are often visible as the evolutionary trends referred to as a pollination syndrome (Fenster et al., 2004). Therefore, to understand the evolutionary mechanisms shaping
diverse sets of ﬂoral traits present in certain
biomes and habitats, it is crucial to illustrate theoverall picture of animal diversity that can potentially be pollinators.
The association between several types of ﬂoral

morphs and the speciﬁc pollinating animals,
especially insects, birds, and small mammals has
been recognized (Proctor et al., 1996), and obviously these pollinators have contributed largely
to the formation and maintenance of most of theﬂoral forms in nature. Nevertheless, much of theﬂoral diversity, especially in tropics, remains to
be investigated in terms of their relationships tothe pollinating animals. Speciﬁcally, very few
reports have been available about the contribution of terrestrial invertebrates other than insects
to pollination.
Here, I report the ﬂoral visitation and pollen
foraging by a sesarmid crab in coastal forest inLuzon Island, Philippines.
Materials and Methods
During the botanical survey in Sierra Madre
Mountains, Isabella state, Philippines on March3, 2012, I have encountered the ﬂowering male

120Yudai Okuyama

individual of Piper sp. near Divilacan village at
17°20′52.0″N, 122°22′32.7″E (elevation of 15 m
above sea level). In order to monitor ﬂower visitors of this plant using time-lapse photography, I
set a digital camera (Optio W90, Pentax, Tokyo,Japan) in front of the ﬁve inﬂorescences (ca.
30 cm distance) mounted on a ﬂexible tripod(Gorillapod, Joby, San Francisco, USA) ﬁxed at
1.5 m above the ground level. The interval
between shots was set to 2 min and the monitoring was conducted overnight from 1505 pm on
March 3 to 0843 on March 4. The resultant 531
shots were subjected for visual inspection of any
ﬂower-visiting animals. To understand the visitation sequence of the animals, the ﬁve inﬂorescences were numbered sequentially from nearground (right) to the left (Fig. 1A).
The plant specimen was deposited at herbarium at National Museum of Nature and Science(TNS) under the temporal collection numberGK14625 (Fig. 2A).
Results
The monitored Piper species had somewhat an
unusual characteristic of the male ﬂower. That is,
the anthers were exerted on the spadix-like inﬂorescences at maturity yet they did not appear todehisce and be releasing pollen grains throughout
the monitoring period, although it is not conclusive as the resolution of the pictures taken in thisstudy was not sufﬁcient to determine this. Thisobservation was also partly supported from theheat-dried specimen of the same plant which
retained most of the anthers indehiscent (Fig.
2B).
Throughout the monitoring, I only observed
two ﬂightless invertebrate species visiting on theinﬂorescences of the Piper plant. One of thesewas a sesarmid crab, which is likely Scandarma
lintou (Fig. 1A), a species reported from southern Taiwan (Schubart et al., 2003) and Okinawa,
Japan (Maenosono and Naruse, 2011). The otherwas a cockroach nymph (Blattodae: Fig. 1B). The
ﬂower visits by the two invertebrates occurred
only during the nighttime.

Both of the ﬂower visitors repeatedly visitedthe inﬂorescences and actively moved among
them, mostly between neighboring inﬂorescences(Table 1). At least once during the move between
the inﬂorescences, the crab attached some antherson the ventral surface of the crab (Fig. 1C).
Discussion
The present observation revealed that the sesarmid crab, most likely Scandarma lintou, might
be a major ﬂower-visiting animal for some plant
species in a coastal forest as in the Piper sp.
studied here. The ﬂower visiting behavior of thisrelatively small crab species is consistent withthe original description of Scandarma lintou,
where it is reported to be mostly arboreal, andfeeds on ﬂowers (Schubart et al., 2003). Most
notably, the crab can attach anthers or clusters ofpollen grains on its body surface (Fig. 1C), indicating that at least the short-distance pollentransfer can occur with the crab.
Although the present observation is only on asingle plant individual, the visitation occurred
repeatedly and the inﬂorescences were located＞1.5 m above the ground, it is most likely thatthe crab has speciﬁcally searched on the inﬂorescences of the Piper species. One of the questions
arisen is how the crabs could locate themselves
toward the speciﬁc ﬂowers. Because the crab isnocturnal (Schubart et al., 2003) as also observedin the present study, the most probable cues areolfactory. It is notable that some terrestrial crustaceans are reported to have developed sophisticated olfactory systems parallel to those ofinsects (Stensmyr et al., 2005). Thus, it is possible that some plant species with ﬂowers accessible to general nocturnal insects with scents arealso accessible to this crab species.
Although scarce, there are several reports
about the contribution of pollination by terrestrial
invertebrates other than insects. Kato (1995)
reported that Aspidistra elatior ﬂowers are pollinated by amphipods feeding on pollen, andSuetsugu et al. (2014) reported a Clubiona spider
frequently visits on a orchid species Neottianthe

Visitation by a Sesarmid Crab to Piper sp.

121

A
2

4

35

B

1CFig. 1. The animals observed visiting on Piper sp. A, A sesarmid crab Scandarma lintou feeding on anthers ofthe Piper sp. The numbers are the inﬂorescence IDs used for Table 1. B, A cockroach nymph staying on themale inﬂorescence of the Piper sp. C, A Scandarma lintou moving between the inﬂorescences. Note that someanthers, or the clusters of pollen grains are attached onto the ventral surface of the crab (yellow arrow).

122

Yudai Okuyama

cucullata to feed on nectar and contribute to its
pollinarium transfer. The more notable observations have been made by Higashi et al. (2014) inthe coastal vegetation in Ryukyu islands, Japan.
The terrestrial hermit crabs of the genus Coenobita frequently visited and fed on the nectar of
the ﬂowers of several plant species there.
Because the pollen grains were often observed toattach onto the shell surface and the head andthoracic appendages, the ﬂower-visiting hermit
crabs are likely contributing to the pollination as
well (Higashi et al., 2014). Based on the present
study, it might be appropriate to add the sesarmid
crab such as Scandarma lintou to these examples, because of its consistent behavior towardﬂowers. Further observations will clarify whether
the sesarmid crab is important as the ﬂower visitor so that it affects the plant evolution in thetropical coastal forests. The relatively robust
ﬂower or inﬂorescence, which is sufﬁcient toTable 1. Flower visitors observed in the present
studyTime onan inﬂorescence

SpeciesInﬂorescenceNo.

1921–1925
1929–1945
1949–1951
1953
1955–1957
1959–2005
2011–20132017–2019
2025
2045
2243
2249–2305
2309–2353
2355–0021
0025–0029
0041–0057
0050–0101
0105–0111
0149
0153–0155

Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Scandarma lintou
Blattodea (nymph)
Blattodea (nymph)
Blattodea (nymph)Blattodea (nymph)
Blattodea (nymph)
Blattodea (nymph)
Blattodea (nymph)
Blattodea (nymph)
Blattodea (nymph)12454324142123432212Fig. 2. The herbarium specimen (GK14625) of the Piper sp. searched in the present study. A, A whole image. B,A magniﬁed male inﬂorescence, which is indicated with red square in Fig. 2A. Note that only the anther indicated with black arrow is releasing pollen grains.

Visitation by a Sesarmid Crab to Piper sp.

support the body of the crab, with exposedanthers and stigmas would be the plant traits necessary to pollination by the crab, as observed in
the Piper sp.
Lowland forests in tropics are one of the mostextensively destroyed biome by the human activities. Under such challenges, it is noteworthy that
the Sierra Madre Mountains studied here remains
largely unaffected by an intensive exploitation sothat the population of the terrestrial crab species
such as Scandarma lintou can sustain, as theyrequire healthy continuity between coast and forest. Therefore, special cares are necessary forconserving this globally important area also in
the light of its potentially unique plant-animalinteractions.
Acknowledgments
I thank Drs. Goro Kokubugata, Ko Nakamura,
Yukiko Saito, Masatsugu Yokota, and the staffs
in Department of Environment and NaturalResources (DENR) and Isabela State University,
Philippines for assisting the ﬁeld study, Hironori
Komatsu for identifying the crab species, andKenji Suetsugu for comments on the manuscript.
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