The causes and consequences of mass-flowering events on

pollinating and fruit eating fauna

Tropical ecology SBC711

Julia Strandmark 063083244

General flowering is a reproductive phenomenon occurring in the aseasonal tropical forests of

South East Asia (Sakai et al 2006). At irregular intervals of 2-10 years up to 80% of the
canopy will synchronously come into flower for a duration lasting from a few weeks up to 4
months (Appanah 1991; Ashton et al. 1988). The participating region can vary substantially,
from a local event extending along a river valley to a regional event covering areas the size of
peninsular Malaysia (Ashton et al 1988). A number of causes have been proposed to account
for these mass flowering events. The most popular, or at any rate most established hypothesis
is that of seed-predator satiation (Janzen 1974). According to this hypothesis plants
synchronize their flowering and fruiting, producing a surplus of resources of which a portion,
due to the high abundance, will be spared from predation. The other possible explanation is
that of optimal seedling conditions (Sakai 2002; Williamson & Ickes 2002); where plants use
environmental cues to determine the most favourable time to reproduce in order to maximize
seedling survival. The search for such cues is still ongoing with no certain conclusions, but a
number of environmental factors have been proposed to be involved. These include drought,
decreased cloud cover and a drop in mean night temperatures.
Lowland tropical forests in South East Asia are dominated by members of the family
Dipterocarpaceae (Sun et al. 2007). The majority of these species never produce flowers
outside mast years (Sakai 2002) but when general flowering does occur, one tree alone can
produce up to four million flowers (Ashton et al. 1988). As flowering intervals can last for up
to 7 years (Curran & Leighton, 2000), two important questions must be asked; 1) How do
pollinators of mass-flowering species avoid extinction during extended periods of resource
scarcity? 2) How do trees avoid competition for pollinators once flowering does occur?
Mass-flowering is followed by mass-fruiting in which vast numbers of fruits and seeds are
produced. From four million flowers, 120.000 fruits may be set (Ashton et al. 1988). This has
consequences for seed and fruit eating fauna, affecting population sizes, reproduction,
migrations and foraging patterns (Curran & Leighton 2000). Just as with pollinators one must
ask how frugivores and granivores, such as bats, birds, rodents, pigs, primates and a large
variety of invertebrates avoid starvation in mast intervals.

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Here, I will discuss the ultimate factors likely to have given rise to general flowering (GF) as
well as the proximate factors which are thought to work as triggers. I will also try answering
the above questions regarding pollinator competition and starvation avoidance by primary
consumers.
In contrast to the aseasonal rain forests, Dipterocarps in the seasonal tropics flower annually
at the end of the dry season and fruits develop at the beginning of the monsoon (Ashton 1982,
as cited in Ashton et al. 1988). This presumably provides optimal conditions for pollination
and seedling development; an adaptation seemingly comparable to spring flowering in
temperate regions in response to an increase in daylight hours. Ashton et al. (1988) suggest
that mass fruiting in the aseasonal tropics “evolved as a consequence of ecological constrains
experienced by a group which originated in the seasonal tropics”. Radiation to aseasonal
areas would have provided a phonological core, which continued to flower simultaneously in
response to some environmental cue. Once such a core of synchronously flowering
individuals was established, any advantage related to this trait would be selected for in
several other families, thus giving rise to the general flowering events seen today. But what
are these advantages on which selection can work? Considering only intra specific flowering,
it is apparent that some level of synchronisation is essential to achieve cross fertilisation and
the chances of such clearly increases with the number of individuals participating.
Considering inter specific synchronisation however, the costs associated with risk of
hybridisation and clogged up stamina must be outweighed by some benefits promoting
coordinated reproduction.
Numerous theories have been put forward for such benefits including the optimal seedling
hypothesis (Williamson & Ickes 2002), pollination enhancement hypothesis (Sakai 2002) and
predation satiation hypothesis (Janzen 1974). The first argues that predictions of favourable
conditions determine flowering time; a reasonable argument, especially when considering
proximate factors likely to trigger general flowering such as El niño effects, discussed later.
The second hypothesis argues that synchronized flowering attracts nomadic pollinators and
allows populations of resident pollinators to increase, thus ensuring higher pollination
success.
The third hypothesis- that of predator satiation, first proposed by Janzen (1974) has received
most support in accounting for synchronised flowering, at least in the family
Dipterocarpaceae.
Dipterocarps have winged seeds and rely on wind dispersal alone (Richards 1996). Any seed
predation therefore has exclusively adverse effects on tree reproduction. With this in mind, it
seems plausible that there is a substantial advantage in flowering and fruiting together, not

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only in attempts to satiate predator populations but also by suppressing predator reproduction
through long intervals between mast events. This advantage of increased seed escape has
been widely demonstrated in the field. Curran and Leighton (2000), carrying out a long term
study investigating levels of vertebrate seed predation during mast and non mast years in
Kalimantan, Indonesia, reported that seeds from asynchronously fruiting plants (e.g. Shorea
lamell; Dipterocarpaceae) were rapidly consumed by a variety of resident and nomadic
vertebrates including primates, bearded pigs (Sus barbatus), pheasants and pigeons. As a
result, no seedling recruitment was recorded in non mast years. This contrasted with the two
major mast events which occurred during the study period (1987, 1991), in which
considerable seedling recruitment was reported. They argued that pressures from two guilds
of vertebrates helped maintain the tightness of a mass flowering event. Early fruiting
dipterocarps had their seeds destroyed by resident vertebrates, gorging on the abundance after
long periods of scarcity. These, pre-dispersal seed predators all had a home range or defended
territories in the study area and included mostly aboreal species such as red leaf monkey
(Presbytis rubicunda), giant aboreal squirrel (Ratufa affinis) and orang-utans (Pongo
pygmaeus). As the seed abundance increased, resident vertebrates tended to switch to non
dipterocarp seeds. By the end of the fruiting, post-dispersal, nomadic vertebrates such as
bearded pigs and wild boar (Sus scrofa), presumed to be guided by circling and vocalizing
parakeets which fly in from far away roosts to feed on the sudden wealth, had made their way
to the masting region and immediately destroyed all late fruiting seeds. The authors thus
argue that a combination of resident and nomadic vertebrates stabilizes the synchrony of
these events. Presumably these pressures vary, but never the less; it seems likely that stresses
from two vertebrate feeding guilds could to some extent help maintain a selection pressure to
fruit as close to the middle of a mast event as possible.
Not only vertebrates are involved in seed predation however. Sun et al. (2007) surveyed
both pre and post dispersal seed predation by a variety of animals including beetles, ants and
other insects, as well as fungi and a number of vertebrates in Pasoh forest reserve, Malaysia.
By determining seed escape in three general flowering years of varying intensity they were
able to demonstrate an overall increase in survival with intensity of the event. As very few, if
any seeds survive when set outside mast events (Curran & Leighton, 2000) there does seem
to be a strong selection favouring synchronous flowering, at least for species which do not
rely on animals for dispersal. However, many other species do and for those, additional
explanations are needed. The seedling release hypothesis (Williamson & Ickes 2002) could
provide such an explanation and is strongly coupled to the most widely accepted proximate
factor involved in triggering general flowering.

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Mass flowering in the eastern parts of Malaysia and Borneo are significantly correlated with
the cycle of the El niño southern oscillation (Sakai et al. 2006). El niño occurs when changes
in air pressure over the Pacific causes westerly trade winds to weaken or change direction.
Warm (>28C) surface water is forced eastward reaching South America where it evaporates,
resulting in increased precipitation (Saunders 2000). South East Asia meanwhile experience
drought and decreased cloud cover which in turn lead to drop in night temperatures due to the
clear skies (Yasuda et al. 1999). Conversely, in El niña events the trade winds strengthen,
causing increased precipitation in South East Asia with opposite conditions in the East Pacific
(Saunders 2000). A variety of conditions accompanying El niño events have been proposed to
serve as a trigger in these areas, including prolonged drought and increased iridescence
associated with decreased cloud cover. But most importantly, it seems, floral development is
triggered by a drop in mean night temperature by at least 2°C below average (Ashton et al.
1988; Appanah 1991; Yasuda et al. 1999).
If mass flowering dipterocarps originated in seasonal tropical forests as suggested (Ashton et
al. 1988), where such reproductive coordination works as an adaptation to maximise seedling
survival by flowering at the end of the dry season in order for fruits to be set at the start of the
monsoon (Ashton et al. 1988), it seems reasonable that the current mass flowering events in
aseasonal forests could provide such benefits as well. Although there is no predictable annual
cycle of dry season followed by monsoon, prolonged droughts are usually followed by wet
weather (Sun et al. 2007). In addition, extensive droughts would cause foliage to be shed
(Williamson & Ickes 2002; Fredriksson et al. 2007), decreasing canopy coverage thus
increasing irradiance to the forest floor. Benefits associated with a drop in night temperatures
are however less apparent and although its importance in triggering general flowering is
commonly emphasized (Appanah 1991; Yasuda et al. 1999), the underlying reasons why such
conditions, or the conditions that follow, should be beneficial for seedling survival is not
speculated upon in the literature. Could it be that decreased cloud and foliage cover provides
optimal seedling conditions and a drop in night temperature is a confounding factor? At the
moment there are no studies to my knowledge which attempts to separate these causes and
indeed this may be difficult to achieve if they are correlated in nature.
Having discussed the possible ultimate factors likely to have given rise to general flowering,
as well as proximate factors thought to trigger these synchronized events, I now move on to
the consequences associated with competition for pollinators as well as avoidance of
starvation by primary consumers.

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In mass flowering events, a shortage of pollinators may be expected, especially considering
the years of scarcity usually preceding the events, which could suppress pollinator
populations. Plants flowering exclusively in synchronized events are therefore expected to
avail of pollinators which have mechanisms allowing them to maintain population densities
in years of low abundance. A number of strategies can be adopted. Pollinators with high
fecundity and short life span have the ability to rapidly increase their population numbers in
response to floral induction. Thrips will start feeding and reproducing on flower buds as soon
as these develop and will reach sufficient numbers for pollination of many dipterocarp
species in time for flower maturation (Ashton et al. 1998). Meanwhile, for pollinators with
longer life span, quickly increasing population sizes in response to flower development is not
an option and solutions including resource switching, long distance migration and food
storage are all availed of. Chrysomelid beetles will switch to feeding on young dipterocarp
leaves in non GF years whilst gorging on pollen, petals and pistils when such are available
(Momose et al. 1998). The giant honey bee (Apis dorsata) maintain populations by usually
inhabiting mountain forests, where flowering occurs in a more predictable manner, but will
migrate over 100km to reach lowland dipterocarp forests as soon as a major flowering event
commences (Momose et al. 1998). A. dorsata as well as other social bees can also survive
years of food shortage through stored resources. Stingless bees (Trigona spp.) for example
can survive for 2-5 years on stored honey (Momose et al. 1998). As honeybees possess a
remarkable ability to communicate location of food patches, their foraging can be highly
efficient in times of plenty. The evolution of the waggle dance was at first thought to have
evolved as an adaptation to the patchiness of food sources in the tropical forests where honey
bees originated (Dornhause et al. 2006). It is now believed that it evolved as a way to
communicate new nest sites (Beekman & Jin Bin Lev 2007), but the adaptive value of forager
recruitment in such an unpredictable environment is hard to deny.
Thus, numerous pollinators respond in a variety of ways to mass flowering events and have
adaptations to see them through periods of food shortage. Whether they migrate long
distances or survive on stored resources however, most of these pollinators adopt a generalist
feeding approach, to increase survival prospects in mast interims (Momose et al. 1998). As a
consequence many plants share the same pollinators and with little specificity the risk of
inappropriate pollination increases. In addition, despite the increase in pollinator numbers in
response to general flowering, in a large event there may still be competition for pollinators.
One way of decreasing such is to stagger flowering within an event. Stiles (1977) argued that
staggered flowering in hummingbird- pollinated plants in Costa Rica was likely to result from
attempts to decrease competition and the risk of inter specific hybridisation. As the flowering

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events in Costa Rica was by no means as synchronized as general flowering in Southeast
Asia, even more pronounced staggering could be expected in the latter. Both Ashton et al
(1988) and Toy (1991) reported staggered flowering in several species of the genus Shorea
(Dipterocarpaceae) in western Malaysia. In this case avoidance of inter specific mating was
assumed to be an unlikely explanation, as Shorea have pronounced post fertilisation barriers
preventing hybridisation (Ashton 1982 as cited in Ashton et al. 1998). Instead the sequential
flowering was assumed to reduce competition for their shared thrip pollinators and thus
reduce clogging of stigmas by foreign pollen.
Another way of reducing pollinator competition is to increase pollinator-plant specificity.
Plants with “pollinator syndrome” (Momose et al. 1998) i.e. highly specialized pollinator
relationships, ensure high efficiency pollination and eliminate any risk of hybridisation. Figs
(Ficus carica) are the extreme examples of specialized flower morphology, so specific that
only one pollinator- the fig wasp is able to fertilize its flowers which are located on the inside
of a closed inflorescence. Figs run no risks of futile pollination. However, there is a trade off
between pollination efficiency and frequency of flowering. Highly specialized pollinators are
unlikely to be able to sustain their populations between GF years and it follows that their host
plants usually have to provide flowers in mass flowering interims. Such is the case in the fig
which flowers continuously to support sufficient populations of the short lived wasp.
Plants like the fig, which flower and fruit outside mast events are vitally important to
frugivores and granivores. Their “fallback fruits” may be less desirable due to lower
nutritional value, increased handling times or long search times but a range of animals rely on
them in mast intervals and their availability is likely to contribute to the carrying capacity for
seed and fruit eating fauna (Fredriksson et al. 2006). Just as with pollinators, frugivores and
granivores live in super abundance during a mast event with more food than they can eat, but
have to find ways to survive the meager times inbetween. The strategies employd are not
entirely different to those of pollnators with resource switching, food storing and migrations
being common.
Nakagawa et al. (2003) survey resource use by seed eating insects in Borneo and reported
that out of 51 species nearly all switched from dipterocarp seeds during mast events to
alternative food sources in masting intervals. Fredriksson et al. (2006) evaluated the diet of
sunbears (Helarctos malayanus) and how it changed in the years following a mast event.
Feeding almost exclusively on masting fruits when such were available, the proportion of less
desirable foods such as figs, palm fruits and invertebrates were found to increase in faeces in
years following general flowering. Similarly Knott (1998) observed orang-utans exceeding

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their daily caloric intake threefold by feasting on highly nutritious mast fruits in an event in
Kalimantan, Indonesia.
This gluttony, allow fat stores to build up which can be availed of when food is less
plentiful. Likewise, food cashing squirrels (Sundsciorus lowii; S. hippurus) and rodents not
only gorge on the overabundance, but also build up food cashes to avail of in times of low
seed production, not entirely different to the honey stores of bees as mentioned above. Stores
can only last so long and the magnitude and duration of a mast interval, as well as availability
of fallback fruits will thus influence how well a species will deal with lean periods
(Fredriksson et al. 2006; Curran & Leighton 2000). Bearded pigs are nomadic and will roam
large regions in search for food, but after several non mast years emaciated bearded pigs have
been observed fighting over limited resources and famine can be so severe that death results
(Curran and Leighton 2000). In accordance with this Curran & Leighton (2000) also reported
that overabundant seed availability during mast events influenced fecundity in these nomads.
Pigs were observed initiating rutting as floral development commenced, which ensured
superabundant resources for piglets arriving in time for fruiting. Similarly, pheasants were
seen nesting with chicks hatching just as seeds started to appear. Neither pigs, nor birds were
ever seen reproducing outside of mast years during this eight year long survey. This
exemplifies how long interims may suppress seed predator populations, one component of the
predator satiation hypothesis (Janzen 1974).
It is interesting to note that the seed predation hypothesis can only explain the adaptive
advantage of general flowering in wind dispersed plants. However, many plants require the
help of animals such as gibbons (McConkey & Chivers 2007), orang-utans (Knott 1998),
fruit bats (Hodekinson & Balding 2003) and a wide variety of invertebrates for seed
dispersal. For these, it seems counterproductive to fruit in synchrony, when the chances of
dispersal could decrease due to the high number of seeds produced. This is where the optimal
seedling hypothesis is likely to complement the predator satiation hypothesis, with plants not
benefiting from simultaneous flowering in the form of “safety in numbers” still set their
flowers in response to the same environmental cue to ensure seedlings germinating in the best
possible conditions. I can think of one other possible explanation in which participation of
animal dispersed plants may also prove adaptive and it comes from the pollination
enhancement hypothesis proposed by Sakai (2002), which suggests that synchronous
flowering occur in order to attract more pollinators. Enhancement in pollinator populations
appears to me to be a more likely effect of increased resources rather than a cause for such,
but if reliant on animals for dispersal it could be adaptive to produce fruits when a high
number of dispersers are present.

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In this essay I have discussed the ultimate factors which are currently believed to have given
rise to the supra annual, mass flowering events seen in the aseasonal tropics, as well as the
consequences it has for populations demographics in fauna relying on the resources provided
by flowering plants. Our understanding of the proximate factors thought to trigger this
strange flower phenomenon seems incomplete and full of controversy. It is likely that
whatever triggers flower development is connected to subsequent optimal seedling
conditions. At the present time there seem to be a consensus that a drop in mean night
temperatures triggers floral development, but the connection to favourable seedling
conditions is still not clear. With the information available at this time, I would argue that the
final product of general flowering is one where optimal seedling conditions as well as a build
up of sufficient resources determine the timing and intensity of a general flowering event, but
where seed predator satiation maintains tight synchrony for species where seed predation is
exclusively detrimental for seedling establishment.
As the products of flowering plants are so tightly related to the population levels of a wide
variety of pollinators and fruit eating animals and with the apparently tight link between
weather and general flowering, more work should be conducted on the effects of our
changing climate on the supra annual cycle of these events. If too many years pass between
mass flowerings, many animals run risks of starvation. Conversely, if environmental
conditions favouring flower development are too frequent, reproduction of these important
plants may be threatened, as resource depletion may prevent trees from producing sufficient
numbers of seeds for seed escape, especially as seed predator populations could be
maintained at a detrimentally high level.
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Appanah, S. (1991) Mass flowering of Dipterocarp forests in the aseasonal tropics.

International Geosphere-Biosphere Project (IGBP) Symposium. Kyoto, Japan, Indian
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Ashton, P.S., Givnish, T.J. & Appanah, S. (1988) Staggered flowering in the
Dipterocarpaceae- new insights into floral induction and the evolution of mast fruiting
in the aseasonal tropics. American Naturalist, 132, 44-66.

Beekman, M. & Bin Lew, J. (2008) Foraging in honeybees - when does it pay to dance?
Behavioral Ecology, 19, 255-262.

Curran, L.M. & Leighton, M. (2000) Vertebrate responses to spatiotemporal variation in seed
production of mast-fruiting dipterocarpaceae. Ecological Monographs, 70, 101-128.

Dornhaus, A., Klugl, F., Oechslein, C., Puppe, F. & Chittka, L. (2006) Benefits of recruitment
in honey bees: effects of ecology and colony size in an individual-based model.

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 Behavioral Ecology, 17, 336-344.

Fredriksson, G.M., Danielsen, L.S. & Swenson, J.E. (2007) Impacts of El Nino related
drought and forest fires on sun bear fruit resources in lowland dipterocarp forest of
East Borneo. Biodiversity and Conservation, 16, 1823-1838.

Fredriksson, G.M., Wich, S.A. & Trisno (2006) Frugivory in sun bears (Helarctos malayanus)
is linked to El Nino related fluctuations in fruiting phenology, East Kalimantan,
Indonesia. Biological Journal of the Linnean Society, 89, 489-508.

Hodgkison, R., Balding, S.T., Zubald, A & Kunz, T.H. (2003) Fruit bats (Chiroptera :
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Janzen, D.H. (1974) Tropical blackwater rivers, animals and mast flowering by the
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Knott, C.D. (1998) Changes in orangutan caloric intake, energy balance, and ketones in
response to fluctuating fruit availability. International Journal of Primatology, 19,
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McConkey, K.R. & Chivers, D.J. (2007) Influence of gibbon ranging patterns on seed
dispersal distance and deposition site in a Bornean forest. Journal of Tropical
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Momose, K., Yumoto, T., Nagamitsu, T., Kato, M., Nagamasu, H., Sakai, S., Harrison, R.D.,
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Nakagawa, M., Itioka, T., Momose, K., Yumoto, T., Komai, F., Morimoto, K., Jordal, B.H.,
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Sakai, S. (2002) General flowering in lowland mixed dipterocarp forests of South-east Asia.
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Sakai, S., Harrison, R.D., Momose, K., Kuraji, K., Nagamasu, H., Yasunari, T., Chong, L. &
Nakashizuka, T. (2006) Irregular droughts trigger mass flowering in aseasonal tropical
forests in Asia. American Journal of Botany, 93, 1134-1139.

Saunders, M. (2000) What are El niño and La niña Events? BBC [online]
available at: http://www.bbc.co.uk/weather/features/el_niño.shtml

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plants in a tropical forest. Science, 198, 1177-1178.

Sun, I.F., Chen, Y.Y., Hubbell, S.P., Wright, S.J. & Noor, N. (2007) Seed predation during

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 general flowering events of varying magnitude in a Malaysian rain forest. Journal of
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Richards, P.W. (1996) The Tropical Rainforest. 2nded. Cambridge: Cambridge University
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Toy, R.J. (1991) Interspecific flowering patterns in the Dipterocarpaceae in the west
Malaysia- implications for predator satiation. Journal of Tropical Ecology, 7, 49-57.

Williamson, G.B. & Ickes, K. (2002) Mast fruiting and ENSO cycles - does the cue betray a
cause? Oikos, 97, 459-461.

Yasuda, M., Matsumoto, J., Osada, N., Ichikawa, S., Kachi, N., Tani, M., Okuda, T.,
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