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Fatal attraction: Carnivorous plants roll out the red carpet to lure insects

  • May 2008
DOI:10.1098/rsbl.2007.0607
Authors:
H. Martin Schaefer at Fundación Jocotoco, Quito, Ecuador
H. Martin Schaefer
  • Fundación Jocotoco, Quito, Ecuador
Graeme Ruxton at University of St Andrews
Graeme Ruxton
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Abstract and Figures

We provide the first experimental test of the hypothesis that the coloration of carnivorous plants can act as a signal to lure insects and thus enhance capture rates. An experimental approach was needed to separate effects of the visual appearance of plants from those of traits that may correlate with appearance and also affect capture rates. We compared insect capture rates of pitcher plants with artificially coloured red and green pitchers in a paired design, and found that plants with red pitchers captured significantly more flying insects. Thus, we present the first experimental evidence of visual signalling in carnivorous plants. Further, it has previously been suggested that carnivorous plants use contrasting stripes or UV marks on their pitchers to lure insects; our results emphasize that insect traps do not need to sport contrasting colours to be attractive; it might be sufficient to be different from the background.
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Biol. Lett. (2008) 4, 153–155
doi:10.1098/rsbl.2007.0607
Published online 15 January 2008
Animal behaviour
Fatal attraction:
carnivorous plants roll
out the red carpet to
lure insects
H. Martin Schaefer
1,
*
and Graeme D. Ruxton
2
1
Faculty of Biology, Department of Evolutionary Biology and Animal
Ecology, University of Freiburg, Hauptstrasse 1, 79104 Freiburg,
Germany
2
Division of Environmental and Evolutionary Biology, Institute of
Biomedical & Life Sciences, University of Glasgow,
Glasgow G12 8QQ, UK
*Author for correspondence (martin.schaefer@biologie.uni-freiburg.de).
We provide the first experimental test of the
hypothesis that the coloration of carnivorous
plants can act as a signal to lure insects and thus
enhance capture rates. An experimental
approach was needed to separate effects of the
visual appearance of plants from those of traits
that may correlate with appearance and also
affect capture rat es. We compared insect capture
rates of pitcher plants with artificially coloured
red and green pitchers in a paired design, and
found tha t plants with red pitchers captured
significantly more flying insects. Thus, we
present the first experimental evidence of visual
signalling in carnivorous plants. Further, it has
previously been suggested that carnivorous
plants use contrasting stripes or UV marks on
their pitchers to lure insects; our results empha-
size that insect traps do not need to sport
contrasting colours to be attractive; it might be
sufficient to be different from the background.
Keywords: plant–animal interactions;
visual signalling; insect vision; anthocyanins; traps
1. INTRODUCTION
The multiple, independent evolution of carnivory in
plants is considered an adaptation to nutrient-poor
habitats (Ellison & Gotelli 2001). In these habitats,
the availability of animal prey is a key factor for plant
fitness as it enhances biomass, flower and seed
production (Moran & Moran 1998). To increase
capture rates, plants might use a variety of deceiving
signals to lure insects. While many carnivorous plants
have nectaries and use olfactory signals, it has
repeatedly been suggested that they also use visual
signals to attract prey ( Joel et al. 1985; Moran et al.
1999; Biesmeijer et al . 2005). This conjecture has,
however, not been tested experimentally. Hence, and
in contrast to the immense progress in understanding
plant visual signals that are used for pollination and
seed dispersal (Chittka et al. 2001; Schaefer et al.
2004), the design and efficiency of visual signals in
carnivorous plants are poorly known.
The potential role of visual signalling in the
remarkably diverse group of carnivorous plants is
intriguing as the traps of all species examined in a
large interspecific comparison sport visual characters
that are considered to be attractive to insects
(Biesmeijer et al. 2005). These include UV reflection
and strong chromatic contrasts of radiating stripes
on the traps (Joel et al.1985; Biesmeijer et al.
2005). Remarkably, many unrelated plants sport red
coloration, particularly on the structures used to
capture prey. For example, pitcher plants from the
genus Nepenthes sport no or very little UV reflec-
tance but large inter- and intraspecific variation
(from green to red) in the coloration of pitchers
(Joel et al. 1985; Moran et al . 1999). Although the
human eye perceives strong contrasts between red
colours and the generally green background of most
plants, red is considered dull or cryptic to most
insects since their colour vision does not extend as
far into the red as that of humans (Chittka et al .
2001). However, red colours are not invisible to
insects (Chittka & Waser 1997), and the capture
rates of Sarracenia pitcher plants correlated with the
amount of red venation (Cresswell 1993; Newell &
Nastase 1998). However, given that red veins are
lined with nectaries (Cresswell 1993) and red is
often not a strongly contrasting colour to insects, it
is uncertain whether the nectaries or the red colour
enhanced capture rates in these studies.
From the perspective of plant–animal communi-
cation, the development of red coloration on insect
traps might be non-adaptive since the expression of
anthocyanins, the pigments producing red hues, is
often related to stress responses in plants (Schaefer &
Rolshausen 2006). In particular, foliar anthocyanin
production is often related to N and P deficiencies
(Steyn et al. 2002). Consistent with this view, prey-
deprived individuals of Nepenthes rafflesiana were
characterized by smaller and fewer pitchers and
by increased anthocyanin production (Moran &
Moran 1998).
To test the adaptive value of red coloration in
attracting prey, we conducted an experiment
comparing capture rates in artificially coloured red
and green pitchers. If red coloration is primarily a
stress response, we expect no difference in the capture
rates of individuals with red or green pitchers. In
contrast, if red coloration is a visual signal functioning
to lure insects, we expect that red pitchers would
capture more insects than green ones do.
2. MATERIAL AND METHODS
We b o ug ht 20 sa m e- a ge d Nepenthes ventricosa plants from a
commercial supplier. In this species, originating from Southeast
Asia, pitchers differed in their coloration from red to green. To
exclude the effects of correlated selection, i.e. that traits associated
with differential coloration (e.g. olfactory cues) may bias prey
capture, we coloured pitchers artificially either completely red
(experimental group) or completely green (control group) using a
mixture of opaque white (Milan no. 306), yellow ( Eberhard Faber
no. 8801-1), and green and red paints (Buntlack, Obi). Because
both colours consisted of a mix of acrylic and tempera paints, we
minimized biases caused by different odours associated with the
paint (albeit not entirely eliminating them). Therefore, if insects
reacted differently to the colours, we assumed that this is primarily
due to visual differences. Indeed, in a previous experiment, we used
similar colours and found that aphids did not discriminate between
these artificial colours and natural red and green plant coloration
(Schaefer & Rolshausen 2007).
To measure natural and artificial pitcher colours, we used an
Avantes 2048 spectrometer (Avantes, Eerbeek, The Netherlands)
that was connected with a coaxial fibre cable to a Deuterium–
Halogen lamp (Ava-lamp DHS) as a standardized light source.
Received 4 December 2007
Accepted 2 January 2008
153 This journal is q 2008 The Royal Society
Reflectance of the natural colours of 20 pitchers and of 10 artificial
green and 10 artificial red pitchers was measured relative to a
standard white reference tile (diffuse PTFE; WS-2). The probe was
mounted inside a matt black plastic tube to exclude ambient light
(Schaefer et al. 2007). The angle of illumination and reflection was
fixed at 458. Spectra were processed with A
VASOFT v. 6.1 software
and calculated in intervals of 5 nm from 300 to 700 nm. The
artificial colours matched the natural colour variation found in
N. ventricosa (figure 1).
We categorized plants into two groups according to the number
of active pitchers. One group contained plants with one or two
pitchers; the other group included plants with three to five pitchers.
From each group, we randomly assigned plant individuals to the
experimental (red) or control (green) group. There was no
difference in the number of pitchers per plant between groups
(meanGs.e.: experimental group: 2.9G0.37 pitchers; control group
2.9G0.27 pitchers; t-test, nZ20, tZ0.0, pO0.99). It is well known
that differences in the microhabitats might influence capture rates
(Cresswell 1993). To minimize such effects, we positioned one red
and one green plant in pairs at 40 cm distance from each other
outside the Institute of Biology in Freiburg. This site was
characterized by several freshwater pools; pairs of plants were
placed at 4 m distances from other pairs and from ponds. We
randomly determined the position of plants within a pair.
At the start of the experiment, we inspected the pitchers without
removing the cap of the pitchers. We only found Collembola (in
almost every plant). After 7 days since the start of the experiment,
we removed the cap of the pitcher to examine the entire interior
and counted all insects. Some of these insects might not have been
visible at the start of the experiment. We therefore continued the
experiment until day 15 when we extracted insects with forceps and
identified the major taxonomic groups of prey. To use a conserva-
tive figure, we subtracted the number of insects caught on day 7
from the total number of insects on day 15 to obtain the number of
insects that were caught during the last 8 days of the experiment.
We used this number, which excluded all Collembola, to test for
differences between groups with paired two-sided t-tests as data
were normally distributed.
3. RESULTS
We found a total of 133 prey items in the pitchers.
Fifty of these were caught during the last 8 days
of the experiment with a mean capture rate of 2.5
(G0.4 s.e.) prey items per plant. These prey items
consisted of Diptera (58%), Homoptera and Acari
(14% each), Hymenoptera (10%, mainly Symphyta
which only occurred in red pitchers) and Araneae
(4%). Only Diptera were common enough to test
for differences in capture rates. Artificially coloured
red individuals caught more Diptera (paired t-test,
tZ3.25, p!0.01) and a higher overall number of
insects than artificially coloured green individuals
(paired t -test, tZ2.98, p!0.01; figure 2).
4. DISCUSSION
Our experiment shows that carnivorous plants can
increase their foraging success using visual signals.
More specifically, we show that red coloration can be
an adaptive trait for carnivorous plants as it increased
the overall capture rates of insects, particularly that of
Diptera. These results extend our understanding of
the evolutionary ecology of carnivorous plants for two
reasons. First, we present the first experimental
evidence of visual signalling in carnivorous plants.
Second, it has previously been suggested, based on
correlations between capture rates and pitcher color-
ation, that carnivorous plants use UV signals or
contrasting stripes to lure insects (Joel et al. 1985;
Moran et al. 1999; Biesmeijer et al. 2005). The higher
capture rates of unicoloured red pitchers in our
experiment thus extend the array of potential visual
signals that carnivorous plants might use. Our results
emphasize that insect traps do not need to sport
contrasting colours to be attractive; it might be
sufficient to be different from the background.
The higher efficiency of red pitchers might be
surprising at first glance, since it contrasts with the
traditional belief that red coloration is an inefficient
signal to insects. While humans can see colour farther
into the red than most insects, some insects such as
Symphyta also possess photoreceptors with peak
sensitivity in the red. More importantly, red colours
are not invisible to insects (e.g. Diptera) lacking such
photoreceptors (Chittka & Waser 1997). Artificial red
objects are even used for pest control owing to their
success in luring fruit flies (Cytrynowics et al.1982;
Katsoyannos & Kouloussis 2001), which is consistent
with our results of increased capture rates of Diptera
by red pitchers. Even bees that cannot discriminate
red colours based on differences in hue are able to
distinguish them based on differences in luminance,
i.e. the intensity of reflected red light. Likewise,
bees might distinguish red colours produced by
40
30
20
reflectance (%)
10
0
300 400 500
wavelen
g
th (nm)
600
green
red
700
Figure 1. Mean reflectance spectra of N. ventricosa pitchers.
The mean reflectance spectra of natural red and green
pitchers are illustrated with solid lines, those of artificial
colours with dotted lines. The shaded area represents the
standard deviation of natural pitcher coloration.
7
6
5
4
3
no. of captured insects
2
1
0
green red
g
rou
p
Figure 2. The number of insects caught per plant with
either red or green pitchers over the course of 8 days.
Illustrated are means, interquartiles, and 10th and 90th
percentiles as whiskers.
154 H. M. Schaefer & G. D. Ruxton Signals of carnivorous plants
Biol. Lett. (2008)
anthocyanins from other colours based on differences
in the blue or green part of the spectrum (Chittka &
Waser 1997). In our experiment, the reflectance of
natural and artificial red pitchers differs from that of
natural and artificial green pitchers both in the green
(520–570 nm) and in the red parts (greater than
610 nm) of the spectrum. It thus remains open
whether insects perceived red pitchers as different
because they reflected more red light or less green
light and had a lower overall luminance. In both the
cases, red pitchers are more different (i.e. red and
dark) from the background of green foliage than green
pitchers. We propose that red pitchers are more
effective because they represent, in addition to the
olfactory signals of nectaries, a visual stimulus that
might direct insects to the trap.
We conclude that the multiple, independent
evolution of carnivory in plants (with more than 600
species described to date) presents an ideal, but
hitherto overlooked, model system to analyse signal-
ling in plant–animal interactions. Elucidating the
mechanisms that plants employ to capture insects will
greatly enhance our understanding of the evolutionary
ecology of carnivory. Moreover, in light of the
increased capture rates of red pitchers the variability
of pitcher coloration in N. ventricosa is puzzling.
Carnivorous plants might thus be ideal to test
hypotheses on insect vision as well as on the proxi-
mate mechanisms of plant coloration.
We thank Julius Braun who helped us in the experiment.
H.M.S. was sponsored by a grant from the German Science
Foundation (Scha 1008/4-1). The experiment complies
with all current laws.
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Signals of carnivorous plants H. M. Schaefer & G. D. Ruxton 155
Biol. Lett. (2008)
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Full-text available
  • Dec 2022
Carnivorous plants reverse the order we expect in nature: here, animals do not feed on plants, but plants hunt and feed on animal prey, primarily insects, thereby enabling these plants to survive in nutrient-poor environments. In addition to this strategy, some carnivorous plants also form unique symbiotic relationships with animals other than insects to access nutrients. Other important interactions of carnivorous plants with insects, such as pollinators and herbivores, have received far less attention or have been largely neglected. This review describes and summarizes various ecologically relevant biotic interactions between carnivorous plants and other organisms reported in recent studies. In particular, our understanding on how carnivorous plants, for example, handle the pollinator–prey-conflict or interact with and respond to herbivores is still incomplete. Strategies and mechanisms on how carnivorous plants address these challenges are presented. Finally, future directions in carnivorous plant research are proposed. © 2022 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
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... Carnivorous plants are of extensive horticultural interest (e.g., Anthony, 1992;Bartsch et al., 2014;Northcutt et al., 2012), and their modified leaves are used to capture insects for heterotrophic nutrients. The bold red contrasts and leaf venations are traditionally viewed much like floral visual signals to attract insects (e.g., Juniper et al., 1989) and there is some evidence supporting this hypothesis in both the North American (Sarraceniaceae) and Asian (Nepenthaceae) pitcher plants (e.g., Cresswell, 1993;Edwards, 1876;J€ urgens et al., 2015;Newell and Nastase, 1998;Schaefer and Ruxton, 2008). In contrast, this relationship was not found in the adhesive trapping leaves of Drosera (Foot et al., 2014), nor in butterwort (Pinguicula planifolia), in which red leaves appeared to capture fewer prey than anthocyanin-free leaves (Annis et al., 2018). ...
... Historical work in Darlingtonia californica suggested that greater anthocyanin pigmentation was associated with increased prey capture (Edwards, 1876), whereas more recent experimental work showed that red venation in the attraction zone of decumbent S. purpurea pitchers correlates positively with the number of prey visits (Newell and Nastase, 1998) and prey captures (Cresswell, 1993). Furthermore, in Nepenthes spp., the hanging pitchers of N. ventricosa attracted more dipteran prey when colored red artificially, as compared with green-painted leaves (Schaefer and Ruxton, 2008). Nevertheless, our study results contrast with these findings, and instead support data from populations of S. alata Wood, which show no relationship between red hood contrasts and prey biomass (Bhattarai and Horner, 2009;Green and Horner, 2007), and data from S. purpurea (Bennett and Ellison, 2009;Milne, 2010), which reveal that color is less important than nectar in prey attraction. ...
Prey Capture in Anthocyanin-free Sarracenia leucophylla (Sarraceniaceae) Is Associated with Leaf Size, But Not Red Pigmentation
Article
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Anthocyanin pigmentation is a significant horticultural feature in plants and can be a crucial mediator of plant–insect interactions. In carnivorous plants, the modified leaves that capture prey can be visually striking and are traditionally considered prey attractants. Nevertheless, the question of whether bold color and venation patterns function as lures for insect prey remains ambiguous, and appears to vary across taxa. Furthermore, vegetative pigments can have alternate functions as protectants against thermal and oxidative damage. Our dual-year study compares the wild-type pitcher phenotype with a true-breeding anthocyanin-free mutant of the white-topped pitcher plant ( Sarracenia leucophylla Raf.). We bred full-sibling crosses of S. leucophylla carrying either the wild-type anthocyanin gene or the anthocyanin-free variant. In both experimental years, growth points were established in outdoor plots and pitchers were allowed to capture prey before harvest at the end of each growing season. Dry weight of prey biomass was measured from pitchers of both pigment morphs, along with nectary counts, pitcher size, and internal temperature. The presence of anthocyanins in trapping leaves did not affect the biomass of insects captured. Nor did wild-type or anthocyanin-free pitcher morphs differ in size, temperature, or nectary counts. Instead, pitcher height, and, nominally, mouth diameter were better predictors of prey biomass. Despite striking visual differences in pitcher color, wild-type and anthocyanin-free plants did not catch significantly different quantities of prey. Our study provides empirical data that anthocyanin pigmentation in S. leucophylla does not affect the capture of prey biomass, and supports a growing body of literature showing that pigmentation traits serve in multiple contexts.
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... Several speculative hypotheses exist as to how these two Sarracenia species might generate these distinct bacterial communities. One is that the different Sarracenia (Fig. 1A) could lure or trap different prey based on their physiology (15,(20)(21)(22)(23). This might directly impact the resulting plant microbiomes based on the bacteria associated with the incoming prey. ...
Selective Bacterial Community Enrichment between the Pitcher Plants Sarracenia minor and Sarracenia flava
Article
Full-text available
  • Nov 2021
This study uses amplicon sequencing to compare the bacterial communities of environmental samples from the detritus of the leaf cavities of Sarracenia minor and Sarracenia flava pitcher plants. We sampled the detritus at the same time and in the same geographic location, eliminating many environmental variables present in other comparative studies.
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... Compared to olfactory cues (Jaffé et al., 1995;Jürgens et al., 2009;Di Giusto et al., 2010), the visual 79 cues of pitcher plants as perceived by insects have received no attention to our knowledge and their role in 80 attraction is the subject of controversy. For instance, pitcher red colouration has been proposed to play an 81 important role in prey attraction by some authors (Newell & Nastase, 1998;Schaefer & Ruxton, 2008) but 82 not by others (Green & Horner, 2007). In an experiment with Sarracenia purpurea (Linnaeus), extrafloral 83 nectar, often associated to red colouration in carnivorous plants (Bennett & Ellison, 2009;Gaume et al., 84 2016), was shown to account for prey attraction, rather than the red colouration itself (Bennett & Ellison, 85 2009). ...
Variation in colour signals among Sarracenia pitcher plants and the potential role of areoles in the attraction of flying Hymenoptera
Preprint
Full-text available
  • Sep 2021
Sarracenia insectivorous plants show a diversity of visual features in their pitchers but their perception by insects and their role in attraction, have received little attention. They also vary in prey composition, with some species trapping more flying Hymenoptera, such as bees. To test the hypothesis of a link between visual signal variability and prey segregation ability, and to identify which signal could attract flying Hymenoptera, we characterised, the colour patterns of 32 pitchers belonging to four taxa, modelled their perception by flying Hymenoptera, and examined the prey they trapped. The pitchers of the four taxa differed in colour patterns, with notably two long-leaved taxa displaying clear areoles, which contrasted strongly in colour and brightness with the vegetative background and with other pitcher areas in the eyes of flying Hymenoptera. These taxa trapped high proportion of flying hymenoptera. This suggests that contrasting areoles may act as a visual lure for flying Hymenoptera, making plants particularly visible to these insects. Prey capture also differed according to pitcher stage, morphology, season and visual characteristics. Further studies on prey visitation are needed to better understand the link between prey capture and attraction feature.
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... In order to attract prey insects, leaf traps of carnivorous plants produce visual and/or olfactory signals (e.g. Jürgens et al. 2009;Schaefer and Ruxton 2008). While visual signals seem to be important for pitcher plants (Kurup et al. 2013; but see Bennett and Ellison 2009), volatile semiochemicals are ubiquitous in carnivorous plants regardless of leaf trap type (Jürgens et al. 2009). ...
Volatile and Semi-Volatile Organic Compounds May Help Reduce Pollinator-Prey Overlap in the Carnivorous Plant Drosophyllum lusitanicum (Drosophyllaceae)
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Most carnivorous plants show a conspicuous separation between flowers and leaf-traps, which has been interpreted as an adaptive response to minimize pollinator-prey conflicts which will reduce fitness. Here, we used the carnivorous subshrub Drosophyllum lusitanicum (Drosophyllaceae) to explore if and how carnivorous plants with minimal physical separation of flower and trap avoid or reduce a likely conflict of pollinator and prey. We carried out an extensive field survey in the Aljibe Mountains, at the European side of the Strait of Gibraltar, of pollinating and prey insects of D. lusitanicum. We also performed a detailed analysis of flower and leaf volatile and semi-volatile organic compounds (VOCs and SVOCs, respectively) by direct thermal desorption-gas chromatography/mass spectrometry (TD-GC/MS) to ascertain whether this species shows different VOC/SVOC profiles in flowers and leaf-traps that might attract pollinators and prey, respectively. Our results show a low overlap between pollinator and prey groups as well as clear differences in the relative abundance of VOCs and SVOCs between flowers and leaf-traps. Coleopterans and hymenopterans were the most represented groups of floral visitors, whereas dipterans were the most diverse group of prey insects. Regarding VOCs and SVOCs, while aldehydes and carboxylic acids presented higher relative contents in leaf-traps, alkanes and plumbagin were the main VOC/SVOC compounds detected in flowers. We conclude that D. lusitanicum, despite its minimal flower-trap separation, does not seem to present a marked pollinator-prey conflict. Differences in the VOCs and SVOCs produced by flowers and leaf-traps may help explain the conspicuous differences between pollinator and prey guilds.
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Psychosocial aspects of sports medicine in pediatric athletes: Current concepts in the 21st century
Article
Behavioral aspects of organized sports activity for pediatric athletes are considered in a world consumed with winning at all costs. In the first part of this treatise, we deal with a number of themes faced by our children in their sports play. These concepts include the lure of sports, sports attrition, the mental health of pediatric athletes (i.e., effects of stress, anxiety, depression, suicide in athletes, ADHD and stimulants, coping with injuries, drug use, and eating disorders), violence in sports (i.e., concepts of the abused athlete including sexual abuse), dealing with supervisors (i.e., coaches, parents), peers, the talented athlete, early sports specialization and sports clubs. In the second part of this discussion, we cover ergolytic agents consumed by young athletes in attempts to win at all costs. Sports doping agents covered include anabolic steroids (anabolic-androgenic steroids or AAS), androstenedione, dehydroepiandrostenedione (DHEA), human growth hormone (hGH; also its human recombinant homologue: rhGH), clenbuterol, creatine, gamma hydroxybutyrate (GHB), amphetamines, caffeine and ephedrine. Also considered are blood doping that includes erythropoietin (EPO) and concepts of gene doping. In the last section of this discussion, we look at disabled pediatric athletes that include such concepts as athletes with spinal cord injuries (SCIs), myelomeningocele, cerebral palsy, wheelchair athletes, and amputee athletes; also covered are pediatric athletes with visual impairment, deafness, and those with intellectual disability including Down syndrome. In addition, concepts of autonomic dysreflexia, boosting and atlantoaxial instability are emphasized. We conclude that clinicians and society should protect our precious pediatric athletes who face many challenges in their involvement with organized sports in a world obsessed with winning. There is much we can do to help our young athletes find benefit from sports play while avoiding or blunting negative consequences of organized sport activities.
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Why red flowers are not invisible to bees
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Full-text available
A pervasive idea among pollination biologists is that bees cannot see red flowers. This idea has led many workers to assume that red coloration is an adaptation by which flowers exclude bees as visitors. However, recent empirical and theoretical evidence strongly supports the alternative view, that red flowers are visible to bees. Our purpose is to marshal this evidence from physiology, behavior, and ecology. First, we define the spectral boundary between orange and red, and show that the visual spectrum of all bee species studied to date extends enough into long wavelengths to provide sensitivity to red light. Such sensitivity differs from the ability to discriminate different monochromatic lights, and we argue that bees will be unable to discriminate such lights above about 550 nm. Second, we point out that flowers do not reflect monochromatic lights. Instead many of them, particularly those that appear red, orange, yellow, and white to humans, have reflectance patterns that are essentially step functions. We predict that bees should be able to discriminate such reflectance patterns over a range of 550–650 nm, since reflectance functions with steps at such wavelengths will occupy different loci in bee color space and thus be distinguishable. In this sense, bees should distinguish between green-, yellow-, orange-, and red-reflecting objects, even if these do not reflect in shorter wavelengths (including UV). A behavioral experiment shows that bumblebees can indeed perform this task. Third, we present information on the spectral reflectance of some typical “red” flowers, combined with field observations of bee visitation to such flowers. We end with a preliminary reassessment of the adaptive significance of red flower coloration, using North American “hummingbird” flowers as an example; we also stress some of the pitfalls facing evolutionary biologists who continue to assume that bees are blind to red objects.
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Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision
Chapter
  • Jan 2001
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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Are Fruit Colors Adapted to Consumer Vision and Birds Equally Efficient in Detecting Colorful Signals?
Article
  • Jan 2007
Reproduction in plants often requires animal vectors. Fruit and flower colors are traditionally viewed as an adaptation to facilitate detection for pollinators and seed dispersers. This longstanding hypothesis predicts that fruits are easier to detect against their own leaves compared with those of different species. We tested this hypothesis by analyzing the chromatic contrasts between 130 bird‐dispersed fruits and their respective backgrounds according to avian vision. From a bird’s view, fruits are not more contrasting to their own background than to those of other plant species. Fruit colors are therefore not adapted toward maximized conspicuousness for avian seed dispersers. However, secondary structures associated with fruit displays increase their contrasts. We used fruit colors to assess whether the ultraviolet and violet types of avian visual systems are equally efficient in detecting color signals. In bright light, the chromatic contrasts between fruit and background are stronger for ultraviolet vision. This advantage is due to the lesser overlap in spectral sensitivities of the blue and ultraviolet cones, which disappears in dim light conditions. We suggest that passerines with ultraviolet cones might primarily use epigamic signals that are less conspicuous to their avian predators (presumably with violet vision). Possible examples for such signals are carotenoid‐based signals.
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The Morphological Correlates of Prey Capture and Resource Parasitism in Pitchers of the Carnivorous Plant Sarracenia purpurea
Article
  • Jan 1993
To infer the functional significance of morphological variation among pitchers of the carnivorous plant Sarracenia purpurea, I measured 8 traits on 87 pitchers and recorded prey captures and frequency of occlusion by spider webs for 47 days. A principal component analysis summarized 78% of the variance in the morphological traits on three component axes, which expressed variation in pitcher size, in pigmentation and available nectar and in pitcher height, respectively. Regression analysis found that the biomass of prey captured was significantly dependent only on the component of variation in pitcher size. However, the number of prey caught was significantly dependent on the component of variation in pitcher size and the component of variation in pigmentation and available nectar. The frequency of inhabitation by spiders was significantly dependent on the components of pitcher size and height. Thus, a relationship was demonstrated between pitcher morphology, prey capture and frequency of resource parasitism.
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Foliar Reflectance and Vector Analysis Reveal Nutrient Stress in Prey Deprived Pitcher Plants (Nepenthes rafflesiana)
Article
  • Nov 1998
Pitcher plants of the genus Nepenthes trap invertebrate prey in pitchers formed from modified leaf tips. This study investigates the benefits of carnivory to Nepenthes rafflesiana, a common Bornean lowland species. Plants were denied prey capture in their natural habitat for 18 wk and were compared with a control group that was allowed to trap, digest, and assimilate prey as usual over the same period. Resource limitation was demonstrated in prey-deprived plants, which produced significantly fewer and smaller pitchers than did control plants. Analysis of foliar spectral reflectance showed increased reflectance within part (608-738 nm) of the photosynthetically active wave band in the prey-deprived plants, signifying a reduction in chlorophyll content. Decreased reflectance at 550 nm in the prey-deprived plants also indicated increased production of anthocyanins, denoting possible nitrogen or phosphorus limitation. Although no difference was found in tissue concentrations of nitrogen or phosphorus between treatments, vector analysis identified a reduction in content of both elements as a result of reduced biomass production in prey-deprived plants. Our findings demonstrate the key role carnivory plays in the nutrition of this species in its natural habitat.
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Ultraviolet patterns in the traps of carnivorous plants
Article
A survey of u.v. patterns in the traps of carnivorous plants reveals that, similar to many flowers, certain traps show conspicuous u.v. patterns. These patterns are based on both u.v.-absorption by the plant surface itself and u.v.-absorption by nectar or pools of the digestive secretion. The results are discussed with respect to the possibility that u.v. patterns may attract prey to certain carnivorous plants.
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Aspects of Pitcher Morphology and Spectral Characteristics of Six Bornean NepenthesPitcher Plant Species: Implications for Prey Capture
Article
  • May 1999
Pitcher plants of the genusNepenthesattract and trap invertebrate prey using nectar-secreting pitchers. Pitcher morphology and spectral reflectance characteristics were investigated for sixNepenthesspecies from northwest Borneo (N. albomarginata, N. ampullaria, N. bicalcarata, N. gracilis, N. mirabilisvar.echinostomaandN. rafflesiana). Morphological measurements focused on the size of the pitcher rim (or peristome, the site of the major nectaries) in relation to pitcher length. The results show considerable interspecific variation in morphology. Spectral reflectance measurements quantified the degree of colour contrast between the peristome and pitcher body, from ultraviolet (UV) to red wavelengths. The contrast maxima for each species were compared with insect visual sensitivity maxima. The six species showed a wide range of reflectance patterns, with pitchers ofN. rafflesianapossessing the greatest degree of ‘fit’ between contrast maxima and insect sensitivity maxima, in the UV, blue and green regions of the spectrum. Based on the morphological and reflectance analyses, we hypothesized that pitchers ofN. rafflesianawould be more attractive to anthophilous (flower-visiting) invertebrates than the sympatricN. gracilis. Analysis of prey contents generally supported the hypothesis, suggesting possible interspecific resource partitioning. Morphological and spectral characteristics of the other species are discussed in relation to published studies on prey capture by those species.Copyright 1999 Annals of Botany Company
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Visual Responses of South American Fruit Flies, Anastrepha fraterculus, and Mediterranean Fruit Flies, Ceratitis capitata, to Colored Rectangles and Spheres
Article
Visual responses of South American fruit flies, Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae), and Mediterranean fruit flies, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), to sticky-coated colored rectangles and spheres were evaluated in field (both species) and laboratory experiments (A. fraterculus). Yellow rectangles were more attractive than orange, green, or red ones to both species. Yellow spheres always captued more A. fraterculus females than spheres of other colors, whereas greatest captures of C. capitata females were on red and black spheres. Spheres seem to be much more attractive to females than to males of both species. but not so rectangles. A fraterculus and C. capitata females may utilize different visual cues when seeking fruit for oviposition.
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Anthocyanins in vegetative tissues: A proposed unified function in photoprotection
Article
The function of anthocyanins in green, vegetative tissues has always been a contentious issue. Here we evaluate their proposed photoprotective function since recent findings have shown that anthocyanins reduce photoinhibition and photobleaching of chlorophyll under light stress conditions. Anthocyanins generally accumulate in peripheral tissues exposed to high irradiance, although there are some exceptions (e.g. accumulation in abaxial leaf tissues and in obligatory shade plants) and accumulation is usually transient. Anthocyanin accumulation requires light and generally coincides with periods of high excitation pressure and increased potential for photo-oxidative damage due to an imbalance between light capture, CO2 assimilation and carbohydrate utilization (e.g. greening of developing tissues, senescence and adverse environmental conditions). Light attenuation by anthocyanin may help to re-establish this balance and so reduce the risk of photo-oxidative damage. Although it has been suggested that anthocyanins may act as antioxidants, the association between anthocyanins and oxidative stress appears to relate to the ability of anthocyanins to reduce excitation pressure and, hence, the potential for oxidative damage. The various aspects of anthocyanin induction and pigmentation presented here are compatible with, and support, the proposed general role of anthocyanins as photoprotective light screens in vegetative tissues.
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