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Papilionate flowers, such as those of Robinia pseudoacacia L., show tripping mechanisms that prevent pollen release: only those bees which apply the right force on petals induce pollen to be deposited on their bodies. Apis mellifera is considered a poor visitor of such flowers, since individuals are usually too weak to trip the mechanism. Despite this, the honey bee pays frequent visits to flowers of R. pseudoacacia and produces a much appreciated unifloral honey. We investigated how bees manipulate R. pseudoacacia flowers, whether they contact the plant’s reproductive core and if there is any appreciable difference related to the manipulation of individual flowers. Honey bees showed two strategies for resource collection, namely legitimate visits and robberies. Legitimate visits were more frequent and about 63 % entailed contact with the flower’s reproductive core. We distinguished two behaviours, one to achieve successful positioning on the flower and the other for nectar intake. These behaviours were clearly perceptible and described by different curves of time frequency distribution. From the beginning to the end of anthesis, flowers were classified into four types on the basis of their morphological and phenological traits. Positioning time differed significantly depending on the flower type, with less time needed for more ageing flowers. Time spent in nectar intake was instead highly variable and independent of flower ageing. Selecting the right flower type would appear to lead to obtaining the R. pseudoacacia reward, overcoming species-specific physical inability. Moreover, the role of honey bees as pollinators of R. pseudoacacia is considered. Finally, the relations between petal characteristics and strength needed to trip the mechanism in papilionate flowers is also discussed in the light of nectar foragers.
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ORIGINAL PAPER
Honey bee handling behaviour on the papilionate flower
of Robinia pseudoacacia L.
Manuela Giovanetti Giovanna Aronne
Received: 14 June 2012 / Accepted: 25 September 2012 / Published online: 12 October 2012
ÓSpringer Science+Business Media Dordrecht 2012
Abstract Papilionate flowers, such as those of Robinia
pseudoacacia L., show tripping mechanisms that prevent
pollen release: only those bees which apply the right force
on petals induce pollen to be deposited on their bodies.
Apis mellifera is considered a poor visitor of such flowers,
since individuals are usually too weak to trip the mecha-
nism. Despite this, the honey bee pays frequent visits to
flowers of R. pseudoacacia and produces a much appreci-
ated unifloral honey. We investigated how bees manipulate
R. pseudoacacia flowers, whether they contact the plant’s
reproductive core and if there is any appreciable difference
related to the manipulation of individual flowers. Honey
bees showed two strategies for resource collection, namely
legitimate visits and robberies. Legitimate visits were more
frequent and about 63 % entailed contact with the flower’s
reproductive core. We distinguished two behaviours, one to
achieve successful positioning on the flower and the other
for nectar intake. These behaviours were clearly percepti-
ble and described by different curves of time frequency
distribution. From the beginning to the end of anthesis,
flowers were classified into four types on the basis of their
morphological and phenological traits. Positioning time
differed significantly depending on the flower type, with
less time needed for more ageing flowers. Time spent in
nectar intake was instead highly variable and independent
of flower ageing. Selecting the right flower type would
appear to lead to obtaining the R. pseudoacacia reward,
overcoming species-specific physical inability. Moreover,
the role of honey bees as pollinators of R. pseudoacacia is
considered. Finally, the relations between petal character-
istics and strength needed to trip the mechanism in pap-
ilionate flowers is also discussed in the light of nectar
foragers.
Keywords Apis mellifera L. Robinia pseudoacacia L.
Foraging Flower handling
Introduction
Papilionate flowers are zygomorphic and formed by five
petals: a flag (standard petal), standing upright, two alae
(wing petals), placed at the side of the carina, and the
carina, itself formed by two keel petals enclosing stamens
and pistil. They are reported to be adapted to bee pollina-
tion (Faegri and Van der Pijl 1979), with different parts of
the corolla designed to attract pollinators on the one hand
and prevent them from collecting the pollen on the other.
These flowers have evolved in the direction of great pollen
economy (Leppik 1966), developing specialised (tripping)
mechanisms for pollen release. The pollination mechanism
may vary depending on the species (Westerkamp 1999),
but generally requires a certain strength exerted by the
pollinator to move the keel petals and to allow stamens and
stigma to extrude (Stout 2000; Parker et al. 2002). Due to
the flowers’ morphological complexity, not all bees seem
able to tune their provisioning strategy to manipulate
papilionate flowers (Stout 2000; Parker et al. 2002).
Known as the black locust in the USA and as false acacia
in Europe, Robinia pseudoacacia L. is a species belonging to
the Fabaceae family and offering flowers with the above
characteristics. Although this species originated in North
Handling Editor: Lars Chittka
M. Giovanetti G. Aronne (&)
Dipartimento di Arboricoltura Botanica e Patologia Vegetale,
University of Naples Federico II, via Universita
`100,
80055 Portici, NA, Italy
e-mail: aronne@unina.it
123
Arthropod-Plant Interactions (2013) 7:119–124
DOI 10.1007/s11829-012-9227-y
America, it has been imported all over Europe since the
beginning of the eighteenth century. In many European
countries, it is naturalised and widespread thanks to its ability
to adapt to different environmental conditions. It has been
widely grown for its wood and for its capacity to colonise
degraded areas (Boring and Swank 1984). Robinia flowers
attract the honey bee as well as other bee species. Acacia
honey (as it is called in Europe) does not crystallise; it is
sweet but not aromatic and enjoys high consumer demand. In
Italy, the production of this honey is of primary interest, since
the quantity supplied is insufficient to meet the national
demand (Aronne et al. 2008). Nevertheless, in dealing with
Apis mellifera visits to R. pseudoacacia flowers, there is a
seeming contradiction. On the one hand, honey bees are
known to be strongly attracted by flowers of false acacia,
from which they collect significant amounts of nectar that
enable the production of the familiar unifloral honey. Indeed,
bee keepers report that when false acacia flowers start pro-
ducing their fine sweet fragrance, honey bees are extremely
busy collecting nectar on them. On the other hand, A.
mellifera is also known to be physically weak, often unable
to exert the strength needed to trip the papilionate flower
mechanisms (Parker et al. 2002;Co
´rdoba and Cocucci
2011). This deficiency has been acknowledged as the reason
why honey bees usually avoid flowering Fabaceae (Co
´rdoba
and Cocucci 2011), visit already tripped flowers (Parker et al.
2002) or turn to alternative strategies, such as robbery, to
collect nectar on them (Etcheverry et al. 2008; Aronne et al.
2012a). Previous studies on flower handling (Laverty and
Plowright 1988; Chittka et al. 1997; Chittka and Thomson
1997; Whitney et al. 2009) as well as the observation of
individually different handling strategies (Heinrich 1976;
Thomson and Chittka 2001; Leadbeater and Chittka 2008)
refer mainly to the bumble bees. Records on flower manip-
ulation by A. mellifera may actually reveal unexpected out-
comes, as was the case of honey bees visiting flowers with
anemophilous characteristics (Giovanetti and Aronne 2011,
Aronne et al. 2012b).
To our knowledge, no detailed direct observations exist
about the honey bee handling strategy of R. pseudoacacia
flowers. Co
´rdoba and Cocucci (2011) demonstrated that
various species of bees usually had enough strength to open
the floral mechanism of the Fabaceae species they visit,
with the precise exception of the honey bee. Flowers of the
same plant species may differ in their physical and chem-
ical characteristics, due to age or pollinator visits, and there
is some evidence that honey bees may recognise and visit
flowers of a different age (MacPhail et al. 2007). We could
expect honey bee visits on R. pseudoacacia to be entirely
devoted to reaching the base of the corolla where the nectar
is located. While trying to reach nectaries, honey bees may
skip the tripping mechanism. Moreover, flower manipula-
tion should deal mainly with flower petal resilience,
possibly influenced by individual flower characteristics and
ageing.
Our aim was to define honey bee manipulation of R.
pseudoacacia flowers. We investigated the hypotheses that
a) honey bees skip the tripping mechanism, performing a
visit which may well avoid contact with the reproductive
core of the flower and b) flower changes due to ageing
influence access to resources and honey bee handling
abilities.
Methods
We assessed the activity of foragers of A. mellifera L. on a
flowering patch of R. pseudoacacia L. The patch was located
in a hill area of the Colli Euganei Regional Park (Vicenza,
Italy). We first performed exploratory observations in order to
set up a protocol for data collection. From these observations,
we confirmed that only nectar foragers visit false acacia. We
detected visible differences on R. pseudoacacia flowers.
Transition from flower bud to senescent flower is a continuous
process, influenced by intrinsic (e.g. flower age, genetic
characteristics) and extrinsic (e.g. environmental conditions,
pollinator’s manipulation) factors. We considered flowers as
being in pre-anthesis until the flag reached the vertical posi-
tion. Anthesis of single flowers lasted a few days and we
distinguished four flower types according to petal ageing and
changes in morphological traits. We classified as type 1,
flowers at the beginning of anthesis with petals perfectly
distended and fresh (Fig. 1a); type 2, flowers showing the first
evidence of ageing with only one of the following features:
small isolated creases, small isolated brown spots, small rips,
stamen and pistil extrusion but intact petals (Fig. 1b); type 3,
flowers with a combination ofthe following features: creases,
small rips, margins of flag and alae starting to fold up or
getting brown, stamens and pistil visible (Fig. 1c); type 4,
flowers with loose floral parts, with stamens and pistil clearly
visible (Fig. 1d).
We were also able to detect two kinds of visits paid to the
flowers by A. mellifera:legitimate visits, when the bee
approached the flower from the front, reached a suitable
position and sucked nectar, and robberies, when the bee lan-
ded on the back ofthe flower and inserted its ligula at the base
of the petals. The legitimate visit to a flower could be easily
split into two behaviours, characterised by a sequence of
precise movements. Initially, the beelanded on the flower and
started to push its head between the flag and carina, trying to
optimise its position to reach the nectar (Fig. 2). These
movements to position itself properly could fail (RB00) or be
successful (RB01). After successful positioning, the bee’s
body remained fixed while the abdomen pushed with regular
movements (bobbing of the abdomen) indicating nectar intake
was occurring (RB02). A legitimate visit thus consists of a
120 M. Giovanetti, G. Aronne
123
positioning time (RB01) and a subsequent sucking time
(RB02). Instead, when a robbery took place, the bee did not
spend any appreciable time positioning itself, but moved
towards the back of the flower and proceeded to suck nectar
directly (RB03).
We recorded 149 visits of A. mellifera foraging on R.
pseudoacacia during its flowering peak, on three sunny days
(17, 18, 19 May 2010). Data were collected between 9 am to
5 pm (Summer Time), standing in front of R. pseudoacacia
inflorescences.Approaching the inflorescence from a distance,
the bees headed for a precise flower and then landed on it. We
classified the flower type prior to the bee’s actual landing. In
addition to the type of flower, we recorded a) on which part of
the flower the bee landed (which petals were touched first by
the legs: flag, alae or carina), b) if there was any contact with
the pistil and anthers during the visit, c) on which part of the
bee’s body pollen may have been deposited. Finally, we
measured the duration of the different behavioural units. Sta-
tistical analyses were performed using SPSS 13.0 (SPSS Inc.).
When necessary, logarithmic transformation was applied.
Results
Type 1 flowers were very rarely visited and we obtained
only three records in all. Instead, we obtained 59 records on
Fig. 1 Fine morphological changes detectable on flowers of R.
pseudoacacia during ageing; atype 1, a fresh flower; btype 2,a
flower showing small rips on the flag (arrow); ctype 3, a flower with
creases on the alae (arrow heads) and visible anthers (arrow); dtype
4, a flower with loose floral parts, with stamens and pistil clearly
visible
Honey bee handling behaviour 121
123
type 2 flowers, 41 on type 3 and 46 records on type 4. The
preferred landing surface was the alae (76 % of cases),
followed by the carina (16.4 %), rarely other flower parts.
Out of 129 visits in which nectar intake took place, legit-
imate visits were the most frequent: 81.4 %. In the
remaining 18.6 % visits, the bees did not approach the
front part of the flower, but tried instead to reach the nectar
from the back. During legitimate visits, stamens and pistil
extruding from the upper rim of the keel petals meant that
pollen could be deposited on the side of the bee’s abdomen.
Anthers and stigma frequently touched the bee’s body:
stigma in 63.1 % of cases and, similarly, anthers in 63.8 %.
With very few exceptions, each time a stigma contacted the
bee’s body, so did the anthers of the same flower
(R=0.957, p\0.0001). We verified whether there was a
part of the bee’s body more frequently associated with
pollen deposition: our results indicated that pollen could be
equally deposited on the right or left side of the bee’s
abdomen, with no statistical difference.
We compared the duration of the four behaviours observed
on flowers (Fig. 3) after normalising data through a log
transformation. There was a significant difference among
behaviours (one-way ANOVA on normalised data,
p\0.0001): positioning time (RB00 and RB01) was signif-
icantly shorter than nectar intake (RB02 and RB03). Failed
positioning showed a slightly higher average duration than
that of successful positioning (failed RB00: 6.89 ±3.50 s;
successful RB01: 5.55 ±3.49 s), although this difference
was not significant (one-wayANOVA, p=0.342). Similarly,
nectar intake duration during legitimate visits (RB02) or
robberies (RB03) did not significantly differ from one another
(one-way ANOVA, p=0.428). During field observations,
positioning and nectar intake were clearly discernible
behaviours and showed different time intervals (Fig. 4).
Records of positioning duration were represented by a sym-
metrical frequency distribution (Fig. 4a), with similar mean
and mode (mean =5.82 s; mode =5.19 s). Records of
nectar intake were instead described by a right skewed fre-
quency distribution (Fig. 4b).
The three records of visits paid to type 1 flowers resulted
in two robberies (RB03) and a failed visit (RB00). Type 1
flowers were therefore not considered, and these three
records were excluded from the analyses below.
Positioning was recorded on all remaining flower types
(types 2, 3 and 4). We recorded 19 failed positionings out of 125
total records; they were significantly associated with type 2
flowers (14 out of 19 cases; v
2
=14.645, df =2, p\0.001).
Positioning was successful in the remaining 106 visits and was
observed on all flower types. There was a statistical difference
of time taken for successful positioning (RB01) associated with
flower type (one-way ANOVA, p\0.0001). Just open, fresh
flowers (type 1) are not visited, but there is an overall declining
trendfromtype2totype4(Fig. 5).
Nectar feeding time (RB02) was recorded on type 2, 3 and 4
flowers; there was no statistical difference on average intake
duration on the three types (one-way ANOVA on normalised
data, p=0.192). Finally, robbery (RB03) was equally per-
formed on any flower type (v
2
=1.1800, df =2, p=0.554).
Fig. 2 Apis mellifera sucking nectar from a R. pseudoacacia flower.
The bee has to exert pressure on the flag petal in order to insert part of
its head at the flag base. While moving and pressing legs on the other
petals to regulate body balance, the tripping mechanism may allow
stamens and pistil to extrude, touching the side (left side, in the
picture) of the bee’s body
Fig. 3 Average duration (seconds) of the four behaviours of honey
bee on R. pseudoacacia flowers. Behaviours refer to positioning on
the flower (failed positioning, RB00, and successful positioning,
RB01) and to the nectar intake (legitimate visit, RB02, and robberies,
RB03). Different letters correspond to significantly different mean
values of the four behaviours after using one-way ANOVA on data
normalised through a log transformation
122 M. Giovanetti, G. Aronne
123
Discussion
In the flowers of Fabaceae, petal orientation is associated
with tripping mechanisms that may affect a pollinator’s
ability to come into contact with nectars and pollen. Recent
studies (Co
´rdoba and Cocucci 2011; Aronne et al. 2012a)
showed that insects do not always approach such flowers
eliciting the pollination mechanism. This confirms the
existence of different approaches to handling such flowers
and getting rewards, with not all maintaining a proper
pollination service. Although A. mellifera and R. pseudo-
acacia originated in different Continents, nowadays their
interaction is economically very important worldwide.
Understanding the honey bee handling strategy on false
acacia flowers may help understand pollination processes,
bee handling abilities and the possible success of invasive
species.
Honey bees used carina and alae as a preferred landing
surface, probably because they offer a wide and almost
horizontal surface. We expected honey bees to skip the
tripping mechanism during their visit due to their physical
deficiency. Actually, while honey bees were focusing on
finding a suitable position to reach the nectar, pushing their
head against the flag while forcing down alae and carina to
maintain body balance, they frequently tripped the mech-
anism. This way, pollen was deposited on the bee’s body
during the visit; pollen could be groomed later, but while a
nectar forager was visiting false acacia, grooming was
rarely observed, thus possibly favouring pollen transport to
the next flower. We may thus presume that the honey bee is
an effective pollinator of R. pseudoacacia.
The legitimate visits comprised two well-distinguished
behavioural units, namely exact positioning of the body
and nectar intake. Times devoted to nectar sucking may
vary considerably, possibly depending on the amount of
nectar found in any visited flower. Nectar content and sugar
composition of untouched flowers of R. pseudoacacia did
not change throughout anthesis (Aronne, unpublished
data). In a study under controlled conditions with the nectar
quantity artificially added, honey bees exploited any
available quantity of reward (Manetas and Petrapoulou
2000). The right skewed frequency distribution of our data
concerning nectar intake, as well as the absence of sig-
nificant differences among flower types, seems to confirm a
similar nectar foraging habit. By contrast, time dedicated to
finding the most suitable position on the flower was a major
component of the entire visit. It may even fail, inducing the
bee to leave before getting the reward and head towards
another flower. As we predicted, individual flowers showed
Fig. 4 Frequency distribution of durations (seconds) of honey bee
behaviours on R. pseudoacacia flowers: arecords of successful
positioning, RB01, showing a symmetrical curve, brecords of nectar
intake, RB02, showing a right skewed curve
Fig. 5 Average duration (seconds) of successful positioning behav-
iour of honey bee (RB01) on different flower types of R. pseudoaca-
cia.Different letters correspond to significantly different mean values
after using one-way ANOVA on data normalised through a log
transformation
Honey bee handling behaviour 123
123
a variation in their visible features, which could be corre-
lated with variable degrees of handling duration. Indeed,
time spent finding a suitable position showed significant
differences depending on the type of the flower: position-
ing time decreased with flower ageing. Moreover, type 2
flowers experienced significantly higher records of failed
positioning, and recently, open flowers (type 1) were not
even visited.
Ageing flowers may differ in the arrangement (Willmer
et al. 2009) and turgescence of their petals due to water loss
during flowering or due to previous visits of other pollinators.
Water loss can influence petal surface and therefore insect
handling ability (Whitneyet al. 2009). Changes in the physical
property of different types of R. pseudoacacia flowers may
explain the higher records of failed placing on type 1 and type
2 flowers, as wellas the decreasing average time of successful
positioning recorded on different flower types.Honey bees are
probably better suited to exploiting ageing flowers than
applying the force needed to unfold petalsof a fresh flower. In
a similar study, Harder (1983) also found that differences in
duration of an entire bee visit were due to the time required to
enter and leave a flower. The slight difference in our data
between failed and successful handling may depend on the
existence of a threshold limit for bees positioning themselves
on a flower, possibly dictated by previous experiences. Bees
may decide to leave a flower that requires (slightly) more time
than usual to get to the nectar. More focused observations on
positioning efforts of experienced and naive foragers may
explain both the decision to give up before reaching a correct
position on a flower, as well as the adoption of a robbing
strategy.
Co
´rdoba and Cocucci (2011) focused on the Fabaceae
flower morphology and the ability of bees: they found an
unforeseen weakness of the honey bee. In the light of our
findings, we infer that honey bees may overcome their
weakness by selecting more ageing papilionate flowers, apart
from implementing a robbing strategy. Co
´rdoba and Cocucci
(2011) also found an unexpected relationship between flag
morphological characteristics and the strength needed to trip
the mechanism. They assumed the flag’s main role is that of a
visual signal, and consequently, it is not involved in pollen
protection via the tripping mechanism. The correlation
between flag morphology and strength required to trip the
mechanism may also be explained by considering handling
behaviours adopted by nectar foragers. In our study, it was
precisely the flag which honey bees had to push hard to reach
the nectary, and by doing so, they pressed their bodies on the
other petals, affording contact with stamens and stigma. The
flag, apart from being a visual signal, may thus bemore strictly
associated than expected with the tripping mechanism.
Acknowledgments M. Giovanetti was supported by a Marie Curie
Fellowship during field work (FP7-PEOPLE-2007-2-1-IEF-220876).
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... Recent research focuses on promoting the consumption of edible flowers of R. pseudoacacia L. as a functional food and their use as a source of natural antioxidants in the food industry. Robinia flowers are utilized to prepare medicinal infusions as well as jams, honeys, and syrups (Giovanetti & Aronne, 2013;Kuś et al., 2014). Fresh flowers can be also added to salads and pastries, or even served with dessert. ...
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... Both tree species are generally regarded by local bee-keepers to serve as the primary resource of honey-bees during their respective flowering, owing to their abundance and production of copious nectar. Both plant species are mainly pollinated by bees, bumble bees and hoverflies 29,30 . ...
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... Although petal diversity has been thought to evolve in relation to the diverse visual attraction functions of pollinators, it is difficult to explain all floral diversity solely in relation to this function (Endress 1994). Petals store nectar (Kramer & Hodges 2010), apply pollen to pollinators (Tomlinson, Primack & Bunt 1979;Almeida et al. 2013), emit olfactory attractants (D€ otterl & J€ urgen 2005;Balao et al. 2011) and act as a landing foothold or platform for pollinators (Kampny 1995;Giovanetti & Aronne 2013). For example morphologically specialised petals such as the lips in Orchidaceae (Benitez-Vieyra et al. 2006) and keel petals in Fabaceae (Le Roux & Van Wyk 2012) often serve as landing platforms to specialist pollinators. ...
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Pollination is a key ecological process, and invasive alien plant species have been shown to significantly affect plant-pollinator interactions. Yet, the role of the environmental context in modulating such processes is understudied. As urbanisation is a major component of global change, being associated with a range of stressors (e.g. heat, pollution, habitat isolation), we tested whether the attractiveness of a common invasive alien plant (Robinia pseudoacacia, black locust) vs. a common native plant (Cytisus scoparius, common broom) for pollinators changes with increasing urbanisation. We exposed blossoms of both species along an urbanisation gradient and quantified different types of pollinator interaction with the flowers. Both species attracted a broad range of pollinators, with significantly more visits for R. pseudoacacia, but without significant differences in numbers of insects that immediately accessed the flowers. However, compared to native Cytisus, more pollinators only hovered in front of flowers of invasive Robinia without visiting those subsequently. The decision rate to enter flowers of the invasive species decreased with increasing urbanisation. this suggests that while invasive Robinia still attracts many pollinators in urban settings attractiveness may decrease with increasing urban stressors. Results indicated future directions to deconstruct the role of different stressors in modulating plant-pollinator interactions, and they have implications for urban development since Robinia can be still considered as a "pollinator-friendly" tree for certain urban settings.
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In this study, VOC profiles of acacia flowers, honey samples at different processing stages and related comb wax samples were studied using comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry. It was found that some monoterpene compounds like α-pinene, myrcene, cis-β-ocimene and 4-terpinelol were common for acacia flower and all acacia honey samples, and the presence of verbenone and ocimene was firstly established in acacia honey. The most enriched VOC profile was obtained for raw honey before cell capping, where the final composition of lactones was achieved. On the contrary, number of alcohols, esters, and variety of terpenes, as well as their concentration in the honey samples decrease through ripening processes. Strained honey was characterized by the absence of camphor, α-bisabolol, 3-carene, while isophorone, and hexanoic acid were identified only in this type of honey. The composition of final VOC profile of honey was also influenced by the age of comb wax. The additional aromatic and lactone compounds e.g. phenol, 1-phenylethanol, δ-hexalactone, γ-heptalactone were observed for honey maturated in old dark comb wax. This article is protected by copyright. All rights reserved.
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Important breakthroughs have recently been made in our understanding of the cognitive and sensory abilities of pollinators: how pollinators perceive, memorise and react to floral signals and rewards; how they work flowers, move among inflorescences and transport pollen. These new findings have obvious implications for the evolution of floral display and diversity, but most existing publications are scattered across a wide range of journals in very different research traditions. This book brings together for the first time outstanding scholars from many different fields of pollination biology, integrating the work of neuroethologists and evolutionary ecologists to present a multi-disciplinary approach. Aimed at graduates and researchers of behavioural and pollination ecology, plant evolutionary biology and neuroethology, it will also be a useful source of information for anyone interested in a modern view of cognitive and sensory ecology, pollination and floral evolution.
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What rules determine whether bumble bees continue exploiting plants of the species just visited or switch to another species? To tackle this question, we recorded handling times and flight times from bees foraging in a natural meadow containing five plant species. Inter- and intra-specific plant distances were quantified. The bee-subjective colors of the five species were determined; two of these species had similar colors and structures, while three species were distinct from all others. The following rules were identified: (1) The decision to switch species was correlated with previous flower handling time, which we assume is a function of the reward amount received at the flower. After short handling times, the probability of switching to another species increased, whereas it decreased after long handling times. This difference became even greater if the bee bad had a run of several short or several long handling times. (2) Constant flights (those between flowers of the same species) and transition flights (those between flowers of different species) followed stereotyped temporal patterns independent of the distances between flowers. Constant flights within five plant species consistently had median durations of about 2 seconds, whereas median transition times between species took 3-6 seconds. (3) This temporal rule broke down, however, if the flowers of two case transition flights had equal dynamics as constant flights. (4) Bees switched more frequently from rare than from common species but even more frequently between similar species. We conclude that the bees' choices were determined by a set of rules that guided them to stay with the current plant species as long as flowers were rewarding and available within close distance but to switch to another species if flowers offered low rewards encountered at close range.
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Pollination syndrome theory should explain flower characteristics on the base of the pollen vector (wind, water, animal) involved in the plant reproductive strategy. Some flowers, although exhibiting morphological traits considered best suited for wind pollen dispersal, experience visits of insects. Data on such visits are often not detailed enough to establish if they are occasional or regular events. If visitors are foraging bees, morphological constraints of anemophilous flowers may affect handling ability and foraging effort. We investigated the foraging behaviour of honey bees on Fraxinus ornus L. and Castanea saliva Miller, two species showing a double pollination strategy (wind + insect), but whose flowers retain clear anemophilous characteristics. We recorded honey bee handling time and routines on the flowers of the two tree species providing a comparison when possible. Interestingly, our results confirm the visits to these plants to be regular events. Moreover, on each of them bees express an appropriate collection strategy, adapted to the different spatial organization of the flowers. Two are the implications discussed: on one side, bees can exploit abundant pollen resources, which could increase colony growth and strength, even if the unsuited flower morphology may limit resource collection. On the other, the plants may increase their reproductive success when climatic conditions are unfavourable to wind pollen dispersal.
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Bumblebees of any one species in Maine forage for pollen and/or nectar from a large variety of morphologically diverse flowers, but individuals have limited foraging repertoires at any one time. Unspecialized individuals were sometimes unsuccessful in extracting nectar and/or pollen from highly rewarding flowers. In any one area with a variety of concurrently blooming plants, the bumblebees had apparent species preferences. Superimposed on the species preferences were individual preferences. Individuals had primary foraging specialties (their majors) and secondary specialities (their minors). Minors were often bridges to new majors. Queens in Maine necessarily have several successive majors during their lifetime since the blooming time of the plants they utilize are brief relative to their life-span as foragers. However, the blooming time of most plants available to Bombus fervidus workers are long relative to their lifetime. Switching was rarely observed in these bees, even in some individuals observed daily for up to 1 mo at the same foraging area containing other plant species in bloom that were highly attractive to other individuals of the same bumblebee species. On a per flower basis, those flowers producing the most food rewards generally had the largest number of bees majoring from them, and the food rewards available were roughly comparable between different kinds of flowers, regardless of their differences in rates of nectar production. Specializing was usually preceded by sampling a variety of rewarding as well as nonrewarding flowers. When the flowers from which bees were majoring in an area were experimentally removed many of the bees sampled flowers of other concurrently blooming plants, but they generally did not switch to flowers from which the food rewards were being depleted by specialists, unless these were experimentally fortified with syrup. Upon finding superior food rewards in enriched blossoms, they switched immediately. Flower-specificity is related to site-specificity. Many bees shared the same foraging area, but different individual bees at the same site utilized the flowers of different plant species. When the foraging area contained landmarks, the bees visited clumps of flowers in a sequence (foraging path) that was generally repeated several times on the same foraging trip when the foraging site was small. The foraging behavior of bumblebees is discussed from a comparative standpoint with other bees and in relation to food distribution and availability in the environment.
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Early forest regeneration in southern Appalachian hardwood forests is dominated by the woody nitrogen-fixing legume, black locust. Although it grows most prevalently on clear-felled areas, abandoned pasture or disturbed roadsides, it may have historically been an important colonizer of burned sites. It commonly reproduces from seed germination, but sprouting from stumps and roots is its commonest means of regeneration. Early sprout growth is rapid, reaching heights up to 8 m in 3 yr. Except for stands on high-nutrient sites, growth decreases after 10-20 yr. In less vigorous stands, stem mortality may be high due to attacks by locust stem borer Megacyllene robiniae. The high mortality of black locust is an early successional mechanism that releases codominant species such as Liriodendron tulipifera, and creates canopy gaps favourable for growth of longer-lived individuals. Total biomass accretion in 4, 17 and 38-yr-old black locust stands growing on fertile, mesic sites was 33, 174 and 399 t ha-1, respectively, in comparison to 198 t ha-1 for an older, uneven-aged mixed oak forest with a history of disturbance. Biomass accumulation was the predominant fate of fixed N in all 3 stands, with an addition to total soil N apparent only in the 38 yr old stand. Symbiotic N fixation by black locust apparently increased the concentration of NO3 in the soil. Total stand N increased at a net average annual rate of 48, 75 and 33 kg ha-1 yr-1, respectively, for ages 4, 17 and 38. Nodule biomass was 8, 106 and 4 kg ha-1 in the 4, 17 and 38-yr-old stands respectively.-from Authors