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Florivory, nectarivory, and pollination - A review of primate-flower interactions

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Abstract

Due to their principally arboreal way of life, primates can potentially interact with flowers from a broad diversity of tropical and subtropical plants. In fact the consumption of flowers and/or nectar has been reported for many primate species, but the role in primate diets is generally underestimated. Also, evidence has been provided for the role of some primate species as pollinators. This paper aims at reviewing information on the interactions between primates and flowers and to examine factors like body mass and dietary strategy as determinants for the type of interaction, i.e. whether entire flowers or nectar are consumed. I also review the available evidence for pollination by primates and the consequences of flower predation for subsequent fruit set. I conclude that (a) the contribution of flowers and/or nectar to primate diets can be substantial, at least seasonally, and therefore (b) primate-flower interactions (flower predation, pollination) are more prevalent and may have larger impact on affected plants than previously thought.
ECOTROPICA t7: 4t 52. 201t
O Society for Tiopical Ecology
FLORTVORY NECTARTVORI AND POLLTNATION -
A REVIEW OF PRIMATE.FLOWER INTERACTIONS
Eckhard W. Heymann
Abteilung Verhaltensökologie & Soziobiologie, Deutsches Primatenzentrum,
Kellnerweg 4, D-37077 Göttingen
Abstract. Due to rheir principally arboreal way oflife, primates can potentially interact with flowers from a broad diversity
oftropical and subtropical plants. In fact the consumption offlowers and/or nectar has been reported for many primate
species, bur the role in primate diets is generally underesrimated. Also, evidence has been provided fbr the role ofsome
primate species as pollinators. This paper aims at reviewing information on the interactions berween primates and flowers
md to examine fäcrors like body mass and dietary strategy c determinants for the rype of inreraction, i.e. whether entire
flowers or nectar are consumed. I also review the available evidence for pollination by primates and the consequences of
flower predation for subsequent fruit set. I conclude that (a) the contribution offlowers and/or necrar to primate diets can
be substantial, at least seasonally, md therefore (b) primate-flower interactions (flower predation, pollination) are more
prevalent and may have larger impact on affected plants than previously thought. Accepted 27 Jantnry 201 1.
Kqtuords: animal-plant interdction, feeding eczlog1t, Primates.
INTRODUCTION
Pollination is a critical step in the plant reproductive
process, affecting not only the reproductive success
ofindividual planrs bur also gene flow and thus plant
population dynamics. Many angiosperms and some
cycads and gnetales depend on animals for pollina-
tion and have evolved adaptations, including the
offering of nectar as a nutritious reward, to attract
flower visitors and to enhance pollination (Pellmyr
2002).ln turn, many animals have evolved adapta-
tions for the exploitation ofnectar, feeding on flow-
ers non-destructively while simultaneously transfer-
ring pollen from one flower to another (Pellmyr
2002). However, other animals may exploit nectar
without pollen transfer ("nectar stealing"), may de-
srroy flowers ro obtain nectar, or may consume entire
flowers ("florivory'). Such feeding strategies can
potentially have a negative impact on plant reproduc-
tive success.
Primates are mainly rropical animals (Martin
1990) that by virtue of their principally arboreal way
of life may interact with flowers from a diverse spec-
trum of flowering plants. In fact an increasing num-
ber of field studies has documented the exploitation
of flowers and flower parts by primates. However,
evidence for pollination by primates is still mainly
anecdotal and scattered throughout the primatologi-
cal, botanical, and ecological literature. A role for
primates in pollination has been specifically sug-
gested for Madagascar, where flower-visiting bats
(which are important pollinators in many other re-
gions) are very rare (Sussman & Raven 1978). Since
Sussman and Ravent work, additional information
has emerged that suggests that some primate species
indeed may act as pollinators. So far, no systematic
arrempt has been made to synthesize these findings
and to identi$' factors influencing the rype of inter-
action between primates and flowers. In this paper I
therefbre aim at reviewing the current knowledge on
primate-flower inter:rctions, specifically addressing
the [ollowing questions:
(1) How important are flowers and nectars in pri-
mate diets?
(2) Do body size (body mass) and dietary strategies
influence florivory and nectarivory in primates?
(3) Do any primates possess morphological adapta-
tions for nectarivory (e.g. longer tongues, spe-
cific tongue surface structures)?
(4) lfhat is the evidence for pollination by primates?
(5) lXlhat impact does primate exploitation of flowers
and nectar have on plants? More specifically, do
florivory and pollination by primates impact the
seed set?
41
e-mail: eheymm@gwdg.de
Nectar is a source of readily available energy in
the form of simple carbohydrates and proteins
(Nicolson & Thornburg 2007). Nectar is generally
offered in relatively small amounts per flower, but
both amount and qualiry of nectar may be tuned to
the energetic demands of pollinators (Nicolson
2007). Nevertheless, due to the usually small amounts
of nectar per flower it may not pay ör large animais
to feed selectively on nectar. On the other hand,
petals and other structural components of flowers
mainly consist of structural carbohydrates that re-
quire bacterid breakdown to make the energy avail-
able. Since this bacterial breakdown requires space in
the gastrointestina.l tract (Chivers & Hladik 1980),
smaller animals may be constrained in the exploita-
tion of structural carbohydrates (but see Foley &
Cork 1992).'With regard to the influence of body
mass and dietary strategies, I therefore make the fol-
lowing predictions:
(a) Feeding on nectar is more prevalent in small-
bodied primates, while larger primates are more
likely to consume whole flowers.
(b) Frugivorous-faunivorous primates are more like-
ly to feed on nectat while folivorous and frugiv-
orous-folivorous primates are more likely to feed
on whole flowers.
These two predictions are not completely inde-
pendent of each othet since there is a strong link
between body mass and dietary strategy, with small-
er species tending towards frugivory-faunivory, and
larger species towards frugivory-folivory and folivory
(Terborgh 1992).
METHODS
To address the questions posed in the Introduction,
I performed intensive literature surveys in the data-
base Primatelit (http://primatelit.library.wisc.edu)
which covers the primate literature published since
1940, including non-referenced publications and
"gray literature" (e.g. theses). I also searched in the
ISI Veb of Knowledge. I used the following key
words in the literature search: [nectar* or flower] for
Primatelit; [(nectar* or flower) and primate*] for ISI
'Web of Knowledge. I also scanned the primatological
literature for data on primate diets and the quantita-
tive contribution of flowers and/or nectar to diets.
Information published before April 2010 is consid-
ered in this review. I do not pretend that my literature
search is exhaustive; older natural history literature
in particular (before 1940) may not be well repre-
sented. Nevertheless, I am confident that the review
42
by and large represents the current state ofinforma-
tion.
From the references, I extracted the following
information:
(") Typ. of flower exploitation and flower handling,
i.e., only nectar consumed, entire flowers con-
sumed or both (only nectar from some plant
species and entire flowers from other plant species
consumed).
(b) Proportion of flowers or nectar in the overall
diet and maximum proportion in a specific pe-
riod of rhe year (season or month).
(c) Information on potential morphological adapta-
tions for nectarivory.
(d) Evidence or clues for primate pollination.
(e) Evidence or clues for negative impacts of floriv-
ory on fruit set.
Most studies that reported the consumption of
flowers and/or nectar did not explicitly describe
flower handling. Therefore I assumed florivory when
only flowers were mentioned as dietary items, necta-
rivory when only nectar was mentioned. A number
of studies quoted "flowers/nectar" as a dietary item,
and others reported that flowers from some plant
species and nectar from other plant species was con-
sumed. I categorized these cases as "both' (i.e., flo-
rivory and nectarivory). The proportion of flowers
and/or nectar in the diet is reported here both for
overall (annual or across-season) diets and as sea-
sonal maximum (proportion in a limited period, i.e.
month or season).
Body mass data were taken from Smith & Jungers
(1997). I used female body mass and created the
following body mass categories for analyses: . 0.5 l€,
0.5-1 kg, 1-5 kg, 5-10 kg, > 10 kg. Primate species
for which no body mass information was available
were allocated to the body mass category of their
closest relatives. Information on the dietary category
was extracted from the specific literature on each
species. I deffned the following categories: folivores
(feeding principally on leaves); frugivores-folivores
(feeding principally on fruit pulp and/or seeds,
complemented with leaves); frugivores-faunivores
(feeding principally on fruit pulp and/or seeds,
complementing this with animal prey); and exuda-
tivores (feeding principally on exudates [gum, latex,
sapl). I calculated distributions of the number of
species over body mass and dietary categories. The
distribution over body mass was compared with an
expected distribution of the rype of flower exploita-
tion (with the null hypothesis that this is indepen-
dent of body mass) using a X2-test in Statistica 9.0.
Distributions over dietary caregories were compared
with an ," x c contingency test in SsS 2.0. Pair-wise
comparisons were performed by partitioning the
contingency table and performing a 12-test, or when
the conditions for the 12-test were not met the ex-
tended Fisher-test. The significance level was set at
0.05, and for pair-wise comparisons at 0.0083 (0.05
divided by the number of comparisons). All statistical
comparisons were performed with counts, but in the
figures percentages are shown.
I generally used the scientific primate names as
provided in the source, except where recent taxo-
nomic revisions have resulted in a change of name.
RESULTS & DISCUSSION
The irnportance offlouers and nectar in primate diex.
I found reports on the exploitation offlowers and/or
nectar by 165 species from all primate families except
the'farsiidael (Online Appendix 1). The majority of
studies reports flower consumption (680lo, N = 113),
fewer primate species consume nectar (17%, N = 28)
or both flowers and nectar (15%o, N = 24).
The contribution that flowers and/or nectar
make to the overall diet is highly diverse beween and
within primate genera and species (Online Appen-
dix 1). For the majoriry of species, flowers and/or
nectar contribute <10olo of food intake. However,
there are also a few species where flowers and/or
nectaf are the most important food resource either
overdl or seasonally. For slow lorises, Nycticebus
coazng, nectar from the palm Eugeissona tristis is the
most lrequently consumed food resource (lViens
et al. 2006). Flowers of Domohonea penieri (Euphor-
biaceae) are the single most important food item in
the diet of diademed sifakas, Propithecus diadema
(Powzyk & Mowry 2003). For severd primate spe-
cies, flowers and/or nectar may account for up to
847o ofseasona-l food intake, generally during periods
offruit scarcity (e.g. Terborgh 1983). Nectar is actu-
ally considered a fallback resource for some primate
species (Terborgh & Stern 1987, Hemingway &
Bynum 2005). This may also hold crue for flowers
(see seasonal maxima reported in Oline Appendix 1).
There can be considerable inter-annual variation
in the exploitation of flowers and nectars. Nectar
accounted for 43o/o of plant feeding in golden lion
tamarins, Leontopithecus rosalia, in one year, but no
1 TheTärsiidae, represenred by the single genus Tarsius, are
the only purely faunivorous primates.
nectar was consumed in the previous year (Dietz et al.
1997). In tamarins, Saguinus frscicollis and Saguirtus
mlstax, nectar accounted for 4.4o/o and 8.0olo respec-
tively of the diet in one year, and. <0.5o/o in both
species in the following year (Smith 1997, Knogge
& Heymann 2003). For red colobus monkeys, Colo-
bus badius, flowers are a negligible component ofthe
diet in most years, but may account for up to l5olo
offeeding records in some years (Struhsaker 2010).
Such variation is mosr likely to be related to avail-
abiliry of nectars/flowers and their profitabiliry in
comparison to alternative resources.
Apart from seasonal variation in flower consump-
tion, there may also be diurnal variation. Mantled
howler monkeys, Alouatta palliata, feed preferen-
tially on the flowers of Pithecelobium saman (Faba-
ceae) at flower opening times, which has been inter-
preted as a stratery ro maximize nutrient or energy
intake (Jones 1983).
A bizarre case of florivory has been observed in
P diadema, which feed on the inflorescences of un-
derground parasitic plants from the genera Langsdarf
fa (Balanophoraceae) and Cytinus (Cy'tinaceae) (Ir-
wtn 2007). The inflorescences are visually obscured
and detected by the sifakas through intensive olfac-
tory search.
The influence of bodl size and dietary snategy on Jlo-
riuory and nectariuory. Prirnates below 1 kg body mass
are more likely to include nectar in their diet than
medium-sized and large primates (X2 = 27.8, df = 4,
p < 0.001), while primates above 5 kg body mass are
nrore likely to consume entire flowers (X2 = 39.9, df
= 4, p < 0.001; Fig. l). Primates with a body mass
between 1.0 and 5.0 kg tend to include both nectar
and flowers in their diet, but the difference berween
observed and expected distribution is not signiffcant
(X' = 7.7, df = 4, p > 0.05).
The distributions offlorivory nectarivory or both
differ significantly between dietary categories (12 =
61.7,df = 6, p < 0.001; Fig.2). Folivorous and fru-
givorous-folivorous primates mainly feed on flowers,
while the proportion of nectar consumers is highest
in frugivorous-faunivoro us primates; amo ng exuda-
tivorous primates the proportions of flower and
nectar consumers are almost equal. For detailed sta-
tistical comparisons see Online Appendix 2.
Do primates possess morphological adaptations for nec-
tariuory?There is little evidence that primates possess
morphological adaptations for nectarivory. Red-bel-
lied lemurs, Eulemur ntbriuenter, which lick nectar
43
R TABLE 1 Reports of pollination by primates I
z
z
Plant lamily / species Primate species Flower handling Evidence or signs of pollination Region Reference
Asphodelaceae Chkrocebus aethiops
Aloe ferox faces covered with pollen
Capparaceae Phanerfurcifer flowers licked sequential feeding at difFerent flowers Madagascar Sussman & Raven 1978
Crateua greueana
Celastraceae Eulemurfuluu,s nectar licked from sequential feeding in several plants Madagascar Birkinshaw 2002
Brexiamadagascariensis llf i; o"*...
regular visits Madagascar Jumelle & Perrier de la
Bäthie 1910 quoted in
Sussman & Raven 1978
Combretaceae Ateles chamek nectar licked; faces conspicuously tinted with pollen; Peru Janson et al. lg9l
Combretumfrutirosum Cebuella pygmaea moderate to heavy abundant seed set by many plants that
Cebus albifrons loss ofdistal portions had been used; trapJine feeding
Cebus apella of flowers
Saguinus .fuscicollis
Saguinus imperator
Saimiri boliuiensis
"quite destructive" face covered with pollen;
s€quential leeding on flowers from
same and different plant individual
Euphorbiaceae Brachyteles hlpoxanthus nectar licked; face covered with pollen Brazil Torres de Assumpgäo
Mabeafisnlifera Callithrixflauiceps minor damage to 1981, Ferrari & Strier
Cebus apella inflorescences 1992
Leontopithecus chrysopygu; nectar licked; face covered with pollen Brnil Passos & Kim 1999
no damage to
inflorescences
Euphorbiaceae Saguinusfncicollis nectar licked; pollen visible on facial hair; sequential Peru Heymann, pers. obs.
Mabea sp' saguinus mvstax ;'r::ä:T.:: f;*ru*:rrs orsame and different $if::ili"ppremen-
SouthAfrica Skead 1967
Clusiaceae lemurs
Symphonia nectarifera
Combretaceae Cebtu sp,
Combretum knceoktum Brazil Prance 1980
Plant lamily / species Primate species Flower handling Evidence or signs of pollination Region Reference
Fabaceae Allenopithecus nigrouiridis nectar licked; sequential leeding on flowers of same Zaire Gautier-Hion & Maisels
Daniellia pynaertii Cercopithecus ascanius no damage to flowers; and different plant individual; 1994
Cercopithecus wolf monkeys never seen lruit set positively associated with
Lophocebus atenimus to eat any other part patterns ofmonkey visits
of the flower
Fabaceae Cebus apellz nectar licked; Surinam Mori et al. 7978
Eperua falcata Saimiri sciureus no damage to flowers
Fabaceae Aotus lemurinus no damage to flowers lace covered with pollen; sequential Colombia Marin G6mez 2008
Inga edalis leeding at different flowers
Fabaceae Perodicticus potto nectar licked face, necks, hands dusted with pollen Cameroon Grünmeier 1990
Parhia bicolor (Galago sp)
Fabaceae Eulemur macaco nectar licked
Par k ia madagas car iens is Madagascar Colquhoun1993,
Birkinshaw & Colquhoun
1 998
Fabaceae Cheirogaleus major depending on primate animals come in contact with sryles Madagascar Nilsson a a/. 1993
Strongylodon craueniae Eulemurfuluus species, nectar feeding and anthers (depending on species
Eulemur rubriuenter is never, rarely, or largely systematically or haphazardly)
Microcebus rufus destructive
Fabaceae Cheirogaleus major nectar licked; no damage sequential leeding on several flowers of Madagascar Wright & Martin 1995
Strongylodnn sp. to flowers same plant
Eulemurfiluus nectar licked; no damage face covered with pollen; sequential Madagascar Overdorff 1992
Eulemur rubriuenter to flowers feeding in different plant individuals
Malvaceae
Adansonia digitata Otolemur gamettii face covered with pollen; sequential Kenya Coe & Isaac 1965
Feeding at different flowers =
z
E
q1
Malvaceae Cheirogaleus medius
Adansoniaperrieri Phanerfurcifer
Adansonia rubro*ipa
Adansonia za
Madagascar Baum 2003 o
2
-l
Malvaceae
A Adansonia sp. Phanerfurcifer flowers licked sequential feeding at different flowers Madagascar Sussman & Raven 1978 !
o
7.
A. Plant family / species Primate species Flower handling Evidence or signs of pollination Region Reference
Malvacaceae
Ceiba pentandra Microcebus murinils
Eulemur mongoz nectar licked;
no damage to flowers Madagascar2 Sussman & Tättersall
1976, Sussman 1978
I
z
z
Ateles chameh
Cebus apelh
Saimiri boliuiensis
no damage to flowers faces conspicuously tinted with pollen Peru Janson er al. 1981
Malvaceae
Ochroma pyramidale Cebus capucinus no damage to flowers pollen on face; sequential feeding at
flowers of same and other plant
individuals
Panama Oppenheimer 1977
Malvaceae
Quararibea cordata Ateles chameh
Cebuella pygmaea
Cebw albifions
Cebw apellz
Saguinus fuscicollis
Saguinus imperator
Saimiri boliuiensis
nectar licked; faces conspicuously tinted with pollen; Peru
some flowers may be trapJine feeding
damaged, but flowers
borne in great excess
Janson et al. 1987
Passifloraceae
Passifhra adenopoda Saimii oerstedii reproductive flower
structures left intact face covered with pollen Costa Rica Happel 1983
Strelitziaceae Eulemur macaco
Rau en a la ma.dagas c ar i e ns is Madagascar Birkinshaw & Colquhoun
l 998
Varecia uariegata nectar licked; fur covered with pollen; sequential
no damage to fiowers feeding on flowers from same and
different plant individuals
Madagascar Kress et al. 1994
Strelitziaceae
Stelitzia nicolai Otolemurcrassicaudatus nectarlicked;
no damage to flowers face and hands covered with pollen Africa Frost & Frost l98l
2 Ceiba pentandra is not autochthonous to Madagmcar but has been introduced
PzuMATE'FLO\TER INTERACTIONS
FIG. 1. Distribution of the consumption of flowers (hatched bars), nectar (stippled bars), or both (cross-
hatched bars) over body mass categories; black bars indicate the expected distribution (based on the distribu-
tion of body mass).
FIG.2. Distribution of the consumption of nectar (hatched bars), flowers (stippled bars), or both (cross-
hatched bars) over dietary categories. FOL: folivores, FRU-FOL: frugivores-folivores, FRU-FAU: frugivores-
faunivores, EXU: exudativores. Horizontal bars indicate significant differences between distributions.
% Flowers
Ll-'-l Nectar
ffi gotn
I Body mass
40
a
.o
8so
o-
a
o
s20
<0.5 0.5-1.0 1.0-5.0
Body mass [kg] 5.0-10.0 >10.0
frqo
o
o
o-
a
E30
o
-o
E
=20
z
FRU-FOL FRU-FAU
FOL
47
from flowers, possess a brushlike tongue tip, in
contrast to rufous lemurs, Eulemur fuluus, which
consume entire flowers (Overdorff 1992). An "ex-
traordinary long tongue" has been suggested as evi-
dence for nectarivory in the hairy-eared dwarf lemur,
Allocebus trichotis (Meier & Albignac 1991), but
neither was tongue length quentified nor were data
presented on the importance ofnectar in the diet of
rhis Malagasy primate. Callitrichids (marmosers and
tamarins) can double the length of their tongue when
protruding it out of the mouth (Heymann & von
der Lage 2009). However, since flowers exploited for
nectar by callitrichids present nectar relatively open-
ly, this is unlikely to represent a speciffc adaptation
for nectarivory. A comparative study on cranial shape
in fruit, nectar and exudate feeders from the orders
Marsupialia, Chiroptera, and Primates did not reveal
any evidence for specific adaptations in primates
(Dumont 1997). However, Muchlinski (2002) found
that in Eulemul mAcAco and Varecia uariegata, wo
lemur species with a high percentage of nectar in the
diet, snouts are longer than predicted from the
allometric relationship with body mass, analogous to
lengthened snouts in nectarivorous bats (Howell &
Hodgkin 1976). Additionally, Muchlinski (2004)
reported structural modifications ofthe hair (divari-
cate scales) in a few seasondly nectar-feeding lemurs.
These modifications were interpreted as structures
that may aid in pollination, although they more
likely evolved for the collection of pollen that is
subsequently groomed out of the fur and consumed
(Howell & Hodgkin l9z6).
Euidence for primate pollination. Apart from non-
destructive handling offlowers (at least the reproduc-
tive parts must remain intact), additional criteria have
to be fulfilled to unequivocally consider a flower
visitor as a pollinator: demonstration of picking up
pollen at one flower and depositing it on the stigma
ofanothe! and subsequent seed production (Carthew
& Goldingay 1997). Additionally, less rigid criteria
can be used as supportive clues. Consistency ofvisits
to flowers of the same plant species, visitors' depen-
dency on nectar as a source of energy (at least during
some period of the year), and morphological struc-
tures of the flower allowing access only to certain
visitors can qualifr these visitors as potential pollina-
tors (Kress 1993).
Unequivocal evidence for pollen deposition and
for lack of fruit set can only be obtained through
experimental work (e.g. exclusion experiments, label-
48
ing of polien), but such experimentation is inher-
ently difficult with primates. Therefore evidence for
primate pollination is mainly indirect, based on
flower handling style, appearance ofpollen in the face
and fur, and sequential visits to different flowers and
individuals of the same plant species. Available infor-
mation is summarized in Täble 1. A number of stud-
ies report non-destructive feeding at flowers, leaving
et least the reproductive part intact, pollen adhesion
to primate faces and fur, and subsequent visits to
flowers of the same or different plant individuals.
Only one study reports a positive association between
primate visits to flowers and subsequent fruit set
(Gautier-Hion & Maisels 1994), suggesting a defi-
nire role of primares as pollinators.
Flowers of the Malagasy traveler's tree, Rauenala
madagascariensis (Strelitziaceae), possess large fl owers
protected by tough bracts that have to be forcibly
opened by animal visitors. Along with the observa-
tion of regular visits and the copious production of
nectar, this led Kress (1993) and Ktess et al. (1994)
to suggest lemurs, particularly ruffed lemurs, Varecia
uariegata, as the primary poilinators of this plant
species. Howwer, a close coevolutionary relationship,
as suggested by Kress (1993) and Kress et al. (1994)
between R. madagascariensis and V uariegata is lun-
likely: the distributional ranges overlap only partially
and R. madagascariensis may produce fruits in the
absence of V uariegata QörgGanzhorn, pers. comm.).
Most primates listed in Täble I are small or me-
dium-sized, and all reports of potential primate
pollination come from the Neotropics, Madagascar,
or Africa. Notably, there is no hint of pollination by
Asian primates (Table 2). Since larger primates are
more likely to consume entire flowers, the compara-
tively lower number of small and medium-sized
primates, and high number of folivorous or frugivo-
rous-folivorous primates in fuia compared with the
other geographic regions (Kappeler & Heymann
1996), possibly accounts for this pattern. Also, this
geographic pattern provides further arguments
against the hypothesis put forward by Sussman and
Raven (1978) that pollination by primates (and
other non-flying mammals) has evolved where pol-
lination by flying mammals, i.e. bats, is rare or ab-
sent, as in Madagascar (see also Janson et al. l98l).
Impact of Jloriaory Since the majority of primates
consume entire flowers, negative impacts on fruit set
are likely. Black-handed spider monkeys, Ateles geol:
froyi, may massively destroy flowers of Slmphonia
TABLE 2. Number of plant genera, and primate
genera and species for which pollination has been
suggested in different geographic regions
Region # plant
genera # pnmare # pflmare
genera species
Africa
Ämerica
Asia
Madaguar
8
t2
10
globulifera (Clusiaceae) and reduce fruit set in plant
individuals located within spider monkey home-
range areas when compared with plant individuals
located elsewhere (fuba-Hernändez & Stoner 2005).
Flower consumption by chacma baboons, Papio ur-
sinus, carses reduced fruit set in the succulent l/ae
marbth;; (Asphodelaceae) (Symes & Nicolson 2008).
Mangabeys, Cercocebus albigena, may 'virtually de-
nude individual lMilletia and Erythrina) trees of
flowers" so that practically no fruits are set ('W'aser
1977, p.195). Lion-tailed macaques, Macaca silenus,
and Nilgiri langurs, Semnopithecus johnii, together
with four sma.ll mammal species,accoufifor 48-54o/a
of destroyed flowersin Cullenia exarillata (Malvaceae
[= Bombacaceae]) (Ganesh & Davidar 1997). Raju
et al. (2005) noted that flower predation by bonnet
macaques, Macaca radiata, and Hanuman langurs,
Semnopithecus entellus, is detrimental to the reproduc-
tive success of Bombax ceiba (Bombacaceae), but did
not provide quantitative evidence.
CONCLUDING REMARKS
Of the currently recognized 390 primate species
(IUCN/SSC Primate Specialist Group 2010), 165
have been observed to feed on flowers and/or nectar.
It is quite likely that this feeding habit is found in
most primates (except lor the faunivorous tarsiers),
but obviously varies considerably between species and
even populations (see Online Appendix l). My
review revealed that flowers and/or nectar are oF
considerable importance in the diets of a number of
primate species, at least seasonally. Reviewing the
many publications on diet composition of primates,
I found that for some species flowers and/or nectar
actually rank second after lruit or leaves, making
classification as frugivores-folivores or frugivores-
faunivores inaccurate.
The importance of flowers and/or necters in
primate diets imp.lies that primate-flower interactions
are not uncommon and that there might be a con-
siderable - and hitherto probably underestimared -
impact of this interaction on the plant individual and
population level. Most primates are flower predators,
and may have a negative impact on the fitness of
individual plants or local plant populations in years
where flowers are particularly important in the diet.
The lew studies where long-term information on the
diet of a primate population is available suggest that
there is a strong inter-annual variation in florivory.
This means that the potentially negative impact is
not consistent and most iikely not detrimental to rhe
affected plants in the long run. V/hether primate
florivory may indirectly affect other flower visitors,
and thus also affect ecosystem processes centered on
anima.l-flower interactions, is completely unknown.
My rwiew conffrmed the predicted effect of body
size and dietary srrategy on the r)?e of primate-
flower interactions. These non-independent effects
can be interpreted as the result ofconstraints imposed
by body size on foraging efficiency in relation to the
size, quality and availabiliry of food resources (fuch-
ard 1985, Strier 2007). More interesting than the
general trend for large primates feeding on entire
flowers and small primates on nectar or borh is the
question of why several large primate species (e.g.
Ateles chameh, Brachlteles hypoxanthus, Lophocebus
atenimus) feed on nectar of some plant species and
even may serve as pollinators instead of consuming
entire flowers. This is even more remarkable since
related species are reported to eat entire flowers and
have not been seen feeding on nectar only. Gautier-
Hion and Maisets (1994) suggested that there must
be a great energetic reward for large primates to feed
on nectar only instead of consuming the flower. Ad-
ditionally, protecdon oFflowers by toxic compounds
may restrict flower exploitation to nectar consump-
tion (Gautier-Hion & Maisels 1994).
Another question is whether mutualistic or co-
adaptive relationships beween primate and plant
species exist. A number of floral traits have been
posited as part of a non-flying mamma.l pollination
syndrome (Sussman & Raven 1978, Janson et al.
1981, Carthew & Goldingay 1997): robust flowers
or inflorescences with at least partially fused and
cuplike perianth, upright flower orientation, exerred
stamina, visually conspicuous or strongly odorous
flowers, and copious amount of nectar. \While sev-
eral o[these traits are present in several plant species
7
8
5
4
6
6
49
for which pollination by primates has been postu-
lated, other plant species do not conform. For in-
stance, infl ores cences of Mabea fstulifera, supposed
to be pollinated by B. lrypoxanthw, Callithrixflauiceps
and, Cebus apella (^Iorres de Assumpgao 1981, Fer-
rari & Strier 1992), are relatively fragile and pre-
sented in a hanging position. They do, however,
produce large amounts of nectar (inflorescences of
the related Mabea occidenta#s produce 149 x 50 mg
sugar per night; Steiner 1981).
Given that potential primate pollinators vary in
size (from ce. 30-65 gin Microcebus to ca. 8000 g in
Brachyteles), activity pattern (nocturnal or diurnal),
the relative role ofdifferent sensory systems in forag-
ing and food selection (Dominy et al. 2006), and, in
color vision systems (Jacobs 2002), it is unlikely that
plants (potentially) pollinated by primates converge
on a small number of traits. As already stated by
Carthew and Goldingay (1997) for non-flying mam-
mals as pollinators, the variabiliry in behavior and
morphology will preclude the selection for specific
traits. Nevertheless, the importance of nectar in the
diet of a substantial number of primate species sug-
gests that there are more cases of primate pollination
than registered so far.
The legume Daniellia pynaertii rcm ins the best
documented case for primate pollination and co-
adaptation. Apart from the correlation between pri-
mate flower visits and fruit set (see above), the con-
trast between floral traits of D. pynaertii end those of
other species ofthe genus that are pollinated by but-
terflies provides tentative evidence for co-adaptations
(Gautier-Hion & Maisels 1994).
One approach to evaluating the relevance of pri-
mate pollination, and whether it has an impact on
plant reproductive traits, would be the comparison of
fruit set in plant species between areas with potential
primate pollinators and areas where these have re-
cently gone extinct (expectation: fruit set higher in
areas with primates, controlling for confounding fac-
tors), and the comparison of traits of a plant between
areas with potential primate pollinators and areas
where the same species has never interacted with
primates (expectadons: higher nectar production and
more robust flowers in areas with primate pollinators).
If expectations were met, this would actually provide
a stronger case for a role ofprimates as pollinators. A
similar comparative approach could be used to exam-
ine the impact of primate florivory on plant popula-
tions (see Riba-Hernändez & Stoner 2005). Addition-
ally, however, it will also be necessary in primate
50
studies to report the type of interaction with flowers
more precisely, and to provide good and quantitative
natural history data that can form the basis for more
quantifiable comparisons and tests of theoretical
predictions. The contribution that flowers and nectar
make to the diets of primates suggest that there is a
high potential for primate-flower interactions. Under-
standing these interactions and their ecological and
evolutionary implications will make a contribution to
both primatology and tropical ecology.
ACKNO\TLEDGMENTS
I thank Foelke von der Lage who established the
primate-flower interaction database as part of her
state examination thesis, Anne Neurath and Petra
Kubisch for help with updating this database, Leon-
ardo Oliveira and Frangoise Bayard for information
about flower handling in Leontopithecus chrysomelas
and Saguinus midas respectively, Jörg U. Ganzhorn
for information on R. madagascariensis and V uarie-
gata, and two anonymous reviewers for their helpful
comments on the manuscriPt.
S UPPLEMENTARY MÄIERTAL ON
ECOTROPICA\TEBSITE
Video: This video was recorded by Tobias 'Wom-
melsdorf in September 2010 at the Estacidn Bi-
olögica Quebrada Blanco (EBQB) in north-eastern
Peru (4'21'S, 73"09'W in the course of a field prac-
tical on primate behavior and ecolog' of the Univer-
sity of Göttingen. It first shows a saddle-back tama-
rin, Saguinus fuscicollis, feeding at a flower from a
liana of the genus Mabea (Euphorbiaceae). Shortly
after this tamarin has left, a moustached tamarin,
Saguinus mlrsta8 starts feeding on the same flower.
Appendix 1: Primate-flower database used in this study.
Appendix2: Statistics to Fig.2.
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... Primates are associated with a whole host of intangible benefits such as ecosystem services (Estrada et al., 2017), cultural values (Cormier, 2002;Fuentes, 2012), positive emotions imparted by sentience, empathy, and caregiving (Goodall, 2006;Vitale & Pollo, 2011), sacredness (Radhakrishna, 2017(Radhakrishna, , 2018, labor (Sponsel et al., 2002), biomedical breakthroughs (Ahuja, 2013), and entertainment (Fuentes, 2013;Ohnuki-Tierney, 1984). Although primates provide critical ecological benefits in the form of seed dispersal and pollination (Heymann, 2011;Sengupta et al., 2015), and are directly responsible for vital advances in human health and science (Phillips et al., 2014) it is debatable if laypeople consider these aspects consciously when they interact with primates or make decisions regarding their continued coexistence (Pröpper & Haupts, 2014). ...
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Living near primate species has positive and negative outcomes for human communities. While most studies focus on understanding people's perceptions regarding the adverse consequences of interacting with primates, less is known about people's willingness to coexist with primates or reasons that may promote human–primate coexistence. We surveyed 794 people co-living with four different primate species—rhesus macaque Macaca mulatta, bonnet macaque Macaca radiata, lion-tailed macaque Macaca silenus, and Hanuman langur Semnopithecus dussumieri—in southern and western India to understand how people perceived the costs and benefits of coexistence. The results of our semi-structured interview study revealed that although tangible costs (i.e., financial losses from primate depredation) primarily drive people's stated tolerance for primate presence, intangible benefits from primates (i.e., their ecological, existence, sentience, and religious values) also critically affect attitudes towards coexistence. Amongst the four species, people associated rhesus macaques with the greatest costs and fewest benefits, lion-tailed macaques with the lowest costs, and bonnet macaques with the highest benefits. People preferred lion-tailed macaques and Hanuman langurs more than bonnet and rhesus macaques, and affection for a species shaped how people viewed costs accruing from the species. People's preferences for species were influenced by their existence, ecological, and sentience values more than their religious value. We suggest that intangible benefits influence people's fondness for a primate species and this, in turn, shapes how people perceive costs resulting from the species. Hence strengthening people's perceptions of the intangible benefits they receive from primate species will improve human tolerance for living near primates. We argue that there is a need to understand the context of human–primate conflicts beyond the cost aspects and focus on the benefits to improve human–primate coexistence. Research Highlights In a study of how humans perceive four Indian nonhuman primates, we found that: • Tangible costs and intangible benefits affected people's tolerance for co-living with nonhuman primates. • Financial costs from primate crop damage were the biggest barrier for coexistence. • Species' existence, ecological, and sentience values shaped affection for the species, and this influenced perception of species' costs.
... Nectar was also a highly important food source for the cotton-tops of our study during the dry season, and might be important too as a source of liquid water. Combretum fruticosum, a vine appreciated by many neotropical primates, was the principal source of nectar, as it was in Montes de María Reserve (Garber 1984;Rizkalla 2000;Heymann 2011). ...
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During 2000–2004, we studied five groups of the Critically Endangered Saguinus oedipus to determine dietary items exploited in a dry tropical forest fragment in northern Bolívar, Colombia. The diet, as measured by the percentage of total multi-year feeding frequencies, consisted of 48.6% fruits (includes aril, fruits and seeds, 28.1% of the dry season diet and 59.9% of the wet season diet), 24% exudates (44.9% in the dry season and 14.9% in the wet season), 15% nectar (2.1% in the dry season and 16.9% in the wet season), 9.8% arthropods (based on multi-year consumption this was 35.7 % in the dry season and 64.3% in the wet season), 1.1% fungi, 0.7% flowers (5 species) and three frogs. Eighty-five plant species in 45 families were identified as part of the diet. The families providing the most species were Rubiaceae (8 species), Sapindaceae (7 species), Bignoniaceae (5 species), and Boraginaceae, Fabaceae, and Meliaceae (4 species each). Food items from an additional 30 families also were consumed, but they were only represented in the diet by 1−3 species per family. We found marked seasonal differences in the consumption of food types across seasons in fruit, exudates and nectar but not arthropods. In the dry season exudates served as a vital food, but they were also important during the wet season, putting into question their designation as “fallback foods.” Gum consumption may play a role other than that as a fallback food, including its medicinal properties and the provision of essential nutrients and water.