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Biological Journal of the Linnean Society, 2013, 110, 199–213. With 6 figures
Interactions between hawkmoths and flowering
plants in East Africa: polyphagy and evolutionary
specialization in an ecological context
DINO J. MARTINS* and STEVEN D. JOHNSON
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg
3209, South Africa
Received 5 December 2012; revised 6 March 2013; accepted for publication 6 March 2013
Hawkmoths (Lepidoptera, Sphingidae) are considered important pollinators in tropical regions, but the frequency
and degree of reciprocal specialization of interactions between hawkmoths and flowers remain poorly understood.
Detailed observations at two sites in Kenya over a two-year period indicate that adult hawkmoths are routinely
polyphagous and opportunistic, regardless of their proboscis length. About 700 individuals of 13 hawkmoth species
were observed visiting a wide range of plant species at the study sites, including 25 taxa that appear to be
specifically adapted for pollination by hawkmoths. We estimate that 277 plant species in Kenya (c. 4.61% of the
total angiosperm flora) are adapted for pollination by hawkmoths. Floral tube lengths of these plants have a
bimodal distribution, reflecting the existence of two hawkmoth guilds differing in tongue length. Hawkmoths
exhibited strongly crepuscular foraging patterns with activity confined to a 20-min period at dusk and, in some
cases, a similar period just before dawn. Corolla tube length appears to act as a mechanical filter as the
longest-tubed plants were visited by the fewest hawkmoth species and these were exclusively from the longtongued guild. Tube length showed a strong positive relationship with nectar volume, even after phylogenetic
correction, which implies that plants with long corolla tubes are under selection to offer relatively large amounts
of nectar to entice visits by polyphagous long-tongued hawkmoths. Our study shows that diffusely co-evolved
pollination systems involving long-tongued hawkmoths are clearly asymmetrical, with plants exhibiting a high
degree of floral specialization, while hawkmoths exhibit polyphagous behaviour. © 2013 The Linnean Society of
London, Biological Journal of the Linnean Society, 2013, 110, 199–213.
ADDITIONAL KEYWORDS: Agrius – coevolution – generalization – insect–plant interactions – Kenya –
Nephele – pollination.
INTRODUCTION
Interactions between hawkmoths and the flowers
they visit provide the most famous putative examples
of the process of coevolution (Darwin, 1877; Nilsson,
1998). From this, it might be expected that these
interactions are, as a rule, highly specialized. Here it
is shown that hawkmoths are actually highly polyphagous foragers and, with some notable exceptions,
are involved in asymmetrical relationships, with the
*Corresponding author. Current Address: Turkana Basin
Institute, PO Box 24467-00502, Nairobi, Kenya.
E-mail: [email protected]
greatest dependency and specialization occurring on
the part of the plants that depend on these animals
for pollination.
Virtually all adult hawkmoths (Lepidoptera: Sphingidae) with functional proboscides utilize flowers as
a source of food in the form of nectar. In the drylands
of East Africa, flowering patterns are closely tied
to rainfall (Cribb, 1984; Blundell, 1987; Agnew &
Agnew, 1994; Beentje, 1994; Stewart, 1996). As rainfall is highly variable and unpredictable in the
strictly seasonal parts of the region (National Atlas of
Kenya, 1969), it follows that nectar resources would
be similarly variable and unpredictable, thus favouring polyphagy by nectarivores.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
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D. J. MARTINS and S. D. JOHNSON
Synchronous flowering in strongly seasonal environments can also give rise to competition among
plants for attraction of nectarivores (Cruz-Neto et al.,
2011). Hawkmoths, which can gain access to nectar in
most flowers because of their long tongues, are able
to make foraging decisions based on rewards in
flowers (Miller, 1981, 1985, 1997; Goyret, Markwell &
Raguso, 2007; Riffell et al., 2008). Thus, plants specialized for hawkmoth pollination may need to offer
substantial nectar rewards if they are to compete for
attraction of these insects. Selection for substantial
nectar rewards should be particularly strong in rare
plant taxa that are specialized for hawkmoth pollination. There is evidence that insects feeding from
flowers learn patterns of distribution and follow these
for varying periods of time depending on the species
involved (Heinrich, 1976; Papaj & Prokopy, 1989;
White et al., 1994; Goyret & Raguso, 2006). Learning
behaviour in hawkmoths has been demonstrated
experimentally for the diurnal species Macroglossum
stellatarum (Kelber, 1996, 1997; Kelber & Pfaff, 1997;
Kelber, Balkenius & Warrant, 2002) as well as the
nocturnal species Manduca sexta (Daly, Durtschi &
Smith, 2001; Goyret et al., 2008; Riffell et al., 2008).
Hawkmoths are powerful flyers and have the ability
to disperse widely and visit widely spaced plants;
combined with their learning behaviour, this means
that hawkmoth pollinators can serve as effective pollinators, enhancing gene flow between fragmented
populations of specialized plants (Kitching & Cadiou,
2000; Martins & Johnson, 2007, 2009).
Interactions between hawkmoths and flowers are,
in general, very poorly documented. Only four previous studies have attempted to systematically document these interactions at the level of communities or
local floras and these were carried out in Costa Rica
(Haber & Frankie, 1989; Agosta & Janzen, 2005),
Brazil (Oliveira, Gibbs & Barbosa, 2004), and southern Arizona (Alarcon, Davidowitz & Bronstein, 2008).
Hawkmoth proboscis length data from Madagascar
have also been analysed in relation to the Guanacaste
assemblage and were found to be similar (Agosta &
Janzen, 2005). Other studies have been limited to
particular plant groups, such as orchids (Nilsson
et al., 1985, 1987; Nilsson, 1992, 1998; Nilsson,
Rabakonandrianina & Pettersson, 1992; Martins &
Johnson, 2007).
The African flora appears to be particularly rich in
moth-pollinated plant taxa (Johnson & Nilsson, 1999;
Luyt & Johnson, 2001; Johnson et al., 2003;
Anderson, Alexandersson & Johnson, 2010). This is
supported by data for African orchids, which show
that about 50% of species have floral traits consistent
with pollination by moths (Dressler, 1981; Cribb,
1984; Stewart, 1996; Martins & Johnson, 2007). East
Africa’s vast seasonal drylands, which include the
broader Somali–Maasai regional centre of endemism
(Bennun & Njoroge, 1999), have a large number of
plant species characterized by white or cream flowers
with long narrow corolla tubes, and evening anthesis
and scent-production, trait associations that are consistent with pollination by hawkmoths (cf. Baker,
1961; Grant, 1985, 1992; Haber & Frankie, 1989). In
this region, genera such as Crinum and Ammocharis
(Amaryllidaceae), Carissa (Apocynaceae), Turraea
(Meliaceae), Pavetta, Conostomium (Rubiaceae),
Cycnium (Orobanchaceae), Jasminium (Oleaceae),
and Gladiolus (Iridaceae) all have species with floral
traits consistent with hawkmoth pollination. Despite
these intriguing patterns, there have been no systematic studies of the occurrence and ecology of interactions between hawkmoths and flowers in a local flora
anywhere in Africa.
The general aim of this study was to document the
ecological interactions between hawkmoths and
plants in the seasonally dry tropical ecosystems of
Kenya. Specific objectives were (1) to ascertain which
plants are utilized as sources of nectar for hawkmoths, (2) to ascertain which hawkmoths are the
most frequent flower visitors, (3) to quantify temporal patterns of hawkmoth activity on flowers, (4) to
identify specific guilds of plants associated with
hawkmoths of varying tongue length, and (5) to
quantify patterns of trait covariation that characterize the floral syndrome associated with hawkmoth
pollination.
MATERIAL AND METHODS
STUDY SITES
Research for this study was conducted mainly
between 2003 and 2005 at two different sites in
Kenya, East Africa: Mpala Ranch in Laikipia County
and Kitengela in Kajiado County. The Kitengela is a
large area of land south of Nairobi National Park
encompassing a range of habitats, primarily grassland on ‘black-cotton’ or red laterite soils, with scattered tree bush-savannah and riverine woodland. The
specific study sites in this region were in Oloorsirkon
Location (01°23.5′S, 036°49.1′E) in Kajiado and a few
sites for specific plants within Nairobi National Park
(Nairobi County). Altitude is ~1650 m a.s.l. Fieldwork
at this site was carried out from late 2003 through the
main rainy season, the ‘long rains’ (March–June) in
2004.
The second study site, Mpala Ranch (0022.127′N,
036°35.309′E), was located on the plains north of Mt
Kenya in northern central Kenya within Laikipia
County. Acacia bush-woodland dominates large areas
of the red-laterite soils. Rocky outcrops, known as
kopjes, of varying size and height are scattered
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
HAWKMOTH POLLINATION IN EAST AFRICA
through the area. Altitude is ~1650–2000 m a.s.l.
Study sites and plants on Mpala were first assessed
during the short rains of 2004 (November) and the
main fieldwork was carried out during the long rains
of 2005.
DIVERSITY
AND PHENOLOGY OF PLANTS
VISITED BY HAWKMOTHS
Detailed field observations were made on focal species
that, on the basis of morphological, scent, and temporal characteristics consistent with sphingophily,
were hypothesized to be pollinated primarily by
hawkmoths (Baker, 1961; Grant, 1985, 1992). These
characteristics are long floral tubes, pale coloration,
crepuscular/nocturnal scent production, and opening
as well as anther dehiscence in the evening or being
open primarily in the evening/night. Observations
took place sporadically during the day while locating
plants and taking measurements, but detailed timed
observations were confined to the period from dusk
onwards. We did not limit our observations to the
focal species and also recorded hawkmoth visits to
other plants, including alien species that occur in the
same communities. Detailed observations were made
on a total of 25 plant species (Table 1).
PATTERNS
OF HAWKMOTH FORAGING
Hawkmoth diversity and foraging patterns were
assessed through direct observations at flowers. No
attempts were made to quantify pollen loads or the
effectiveness of hawkmoths as pollinators. However,
in cases where corolla tubes matched or slightly
exceeded moth tongue lengths, it was usual to observe
large amounts of pollen adhering to the proboscis and
body of moths. This was also evident in many of the
photographs taken at the study sites (Fig. 1). Hawkmoths were observed directly where there was sufficient light and with additional lighting when needed.
After dusk or in the dark, hawkmoths were watched
using a dimmed torch (by placing masking tape over
the glass) and/or a dimmed headlight. The time of
each hawkmoth visit was recorded along with
ambient environmental conditions (local weather and
cloud cover), number of open flowers on plants,
number of flowers visited, and the identity of the
visitor. Visitation data were recorded in 1-min intervals. Flowers were watched from c. 18:00 h until
about 20–30 min after the last hawkmoth visited at
all study sites. Dark-coloured clothing was worn
during observations and movements were limited so
as not to startle the hawkmoths. The association
between floral tube length and the time that hawkmoths spent probing individual flowers was analysed
201
using anaysis of covariance (ANCOVA) with hawkmoth species included as a fixed factor and tube
length as a covariate.
Light trapping was used to assess the broader
patterns of hawkmoth diversity at each site. Due to
unsuitable weather conditions and absence of reliable
power sources in remote sites, light-trapping was
limited and met with varying success. Prior experience
with collecting and photography of hawkmoths and
other insects in both areas allowed for easy identification of hawkmoths on the wing while feeding at
flowers. This was also simplified by the limited number
of hawkmoth species to be found foraging from floral
resources at both sites. Identifications were based on
the collection in the Department of Invertebrate
Zoology, National Museums of Kenya, and published
catalogues and revisions of the Sphingidae (Pinhey,
1962; Carcasson, 1976; Kitching & Cadiou, 2000).
FLORAL
MORPHOLOGY, ANTHESIS AND NECTAR
Measurements of floral tube lengths of freshly collected flowers were made using a ruler. Anthesis was
checked by closely inspecting the anthers, at regular
(c. 10 min) intervals from 17:00 h onwards, and
lightly brushing them with a paintbrush. Samples of
nectar in the study species were taken by carefully
detaching individual flowers in the early evening (c.
17:30–18:00 h) before pollinator activity began. Sampling of nectar was done using glass microcapillary
tubes (either 5 or100 mL). Nectar was removed from
individual flowers by carefully cutting the floral tubes
open and drawing the nectar out using capillary
action. Nectar sugar concentration was determined
using a pocket refractometer (0–50%; Bellingham and
Stanley, Turnbridge Wells, UK).
ANALYSIS
OF TRAIT ASSOCIATIONS
The relationships between log-transformed values for
corolla tube length and other traits (flower number,
nectar volume, nectar concentration) were established
using regression of actual values as well as standardized linear phylogenetically independent contrasts
(PICs). The latter were calculated using the PDAP
module (Midford, Garland & Maddison, 2005) implemented in MESQUITE (Maddison & Maddison,
2006). A phylogeny for the study taxa (Fig. S1) was
based on existing published trees and was constructed using PHYLOMATIC (Webb & Donoghue,
2005). Branch lengths were assigned according to
Pagel’s arbitrary method (Pagel, 1992), as this
resulted in homogenous variance of contrasts, as indicated by the absence of a significant linear relationship between the absolute values of the standardized
contrasts and the sum of the squares of branch
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
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D. J. MARTINS and S. D. JOHNSON
Figure 1. Plant habitat and interactions between flowers and hawkmoths: A, Agrius convolvuli visiting flowers of
Turraea mombassana; B, Nephele comma inserting its pollen-coated proboscis into the staminal tube of a flower of
Turraea mombassana; C, Nephele comma approaching Carissa edulis; D, Nephele comma probing a flower of Grewia
bicolor, a diurnal bee-pollinated plant; E, Basiothia medea foraging on Pentanisia ouranogyne, a species whose flowers
are also pollinated diurnally by butterflies. F, landscape of Laikipia District, Kenya; G, Agrius convolvuli foraging on
flowers of Gynandropsis gynandra.
䉴
lengths (Garland, Harvey & Ives, 1992; Midford et al.,
2005). Results of analyses of trait associations are
presented only for native plant species. Inclusion of
alien plant species in these analyses did not alter the
results, but are not presented here as traits of these
species would not have evolved through selection by
hawkmoths in East Africa.
ANALYSIS
OF THE
KENYAN
FLORA
The percentage of species in the flora of Kenya that
have flowers consistent with pollination by hawkmoths
(see above), and the frequency distribution
of corolla tube length among these putatively
hawkmoth-pollinated species, was calculated. This
was done by a thorough analysis of the entire flora of
Kenya using published monographs and field guides
(Cribb, 1984; Blundell, 1987; Agnew & Agnew, 1994;
Beentje, 1994; Stewart, 1996) and measurements of
specimens at the East African Herbarium located at
the National Museum of Kenya in Nairobi. All known
plant species showing traits of sphingophily within the
Kenyan flora were included in this analysis. Aspects
used in this broad analysis included floral tube/spur
length, general morphology and flower colour.
RESULTS
DIVERSITY
AND PHENOLOGY OF PLANTS
VISITED BY HAWKMOTHS
Hawkmoths were observed to visit the flowers of 25
plant species in 13 different families during the
course of this study (Table 1, Supporting Table S1).
The duration and patterns of flowering ranged from a
few days to several months (Supporting Table S1).
Flowering of hawkmoth-visited plants peaked from
the end of March/mid-April to August–September in
both sites, with a shorter, less intense flowering of
some species during the ‘short rains’ in October–
November. A number of species, including Jasminium
fluminense and Carissa edulis, also flower sporadically at other times of year.
PATTERNS
OF HAWKMOTH FORAGING
We recorded more than 700 bouts of foraging by
hawkmoths on the study species. Hawkmoth foraging
was observed to take place primarily during a short
period of c. 20 min around dusk (Fig. 2). We also
observed hawkmoths foraging at dawn on Conostomium quadangulare between 05:00 and 05:15 h at
Mpala on 16 September 2004 (N = 14 moths) and on
Lantana camara between 05:45 and 05:55 h at
Kitengela on 15 August 2005 (N = 21 moths). We did
not carry out detailed observations at dawn for the
remaining species, but did also observe dawn foraging
by an unidentified long-tongued hawkmoth on a
Crinum sp. in rainforest habitat in western Kenya.
Hawkmoths were observed foraging in all weather
conditions, except very heavy rain. As Kenya is an
equatorial country, daylength does not change during
the year, but the time of sunset shifts by a few
minutes during the year, with a corresponding shift in
the time of sunrise. Dusk and dawn foraging patterns
of hawkmoths loosely follow these shifts (Fig. 2).
The mean duration of visits to individual flowers by
various hawkmoth species showed a significant positive relationship with flower tube length (F = 11.88,
P = 0.04; Fig. 3) and did not vary among species
(F = 1.38, P = 0.285) when tube length was taken into
account. This relationship remained significant in an
analysis that considered only the association between
the tube lengths of seven plant species and mean
duration of visits by the hawkmoth Agrius convolvuli
(F = 6.15, P = 0.048).
We recorded between one and six hawkmoth species
(mean = 2.58) as visitors to each of the study species
(Supporting Table S1). There was a significant nonlinear trend (the best fitted curve was exponential
decay) for short-tubed plant species to have a higher
diversity of hawkmoth visitors than longer tubed ones
(Fig. 4A). Indeed, no more than two hawkmoth
species were observed to visit plant species with floral
tubes longer than 90 mm. The most common visitor to
these long-tubed species was the long-tongued hawkmoth Agrius convolvuli (Supporting Table S1). Plants
with flowers of medium depth (20–50 mm) were
visited by both long-tongued (Agrius convolvuli) and
short/medium-tongued hawkmoths (e.g. Nephele
comma, Hippotion celerio, Basiothia medea, and
Atemnora westermanii).
We made 400 records of foraging bouts by hawkmoths at the Kitengela ecosystem during the main
rains in 2004, 100 records during the short rains from
Mpala in 2004, 100 records from Borana in February
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
HAWKMOTH POLLINATION IN EAST AFRICA
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
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D. J. MARTINS and S. D. JOHNSON
Table 1. Hawkmoth visitors to plant species at the Kitengela and Mpala study sites
Hawkmoth species (N)
Family
Plant species
Kitengela
Mpala
Amaryllidaceae
Ammocharis tinneana
Crinum macowanii
Acokanthera schimperi
Carissa edulis
Agrius convolvuli (19)
Agrius convolvuli (7)
Sphingonaepiopsis nana (6)
Nephele comma (28)
Hippotion celerio (25)
Basiothia medea (5)
Agrius convolvuli (1)
Agrius convolvuli (2)
Asteraceae
Tithonia diversifolia
Euphorbiaceae
Croton megalocarpus
Nephele comma (3)
Basiothia medea (5)
Leucostrophus hirundo (5)
Cephonodes hylas (4)
Macroglossum trochilus (7)
Basiothia medea (3)
Apocynaceae
Croton dichogamus
Brassicaceae
Maerua decumbens
Gynadropsis gynandra
Iridaceae
Gladiolus ukambanensis
Plectranthus pubescens
Agrius convolvuli (18)
Meliacaea
Turraea mombassana
Oleaceae
Jasminium floribundum
Agrius convolvuli (20)
Atemnora westermanni (2)
Nephele comma (76)
Hippotion celerio (5)
Basiothia medea (3)
Temnora pseudopylas (2)
Nephele comma (4)
Hippotion celerio (7)
Agrius convolvuli (8)
Coelonia fulvinotata (3)
Agrius convolvuli (17)
Coelonia fulvinotata (2)
Nephele comma (19)
Temnora sp. (2)
Hippotion celerio (4)
Hippotion celerio (17)
Leucostrophus hirundo (2)
Jasminium fluminense
Orchidaceae
Aerangis brachycarpa
Rangaeris amaniensis
Rubiaceae
Pavetta abbyssinica
Pentanisia ouranogyne
Orobanchaceae
Conostomium quadrangulare
Cycnium tubulosum
Solanaceae
Verbenaceae
Cycnium ajugifolium
Datura stramonium
Lantana camara
Lippia javanica
Hippotion celerio (20)
Nephele comma (8)
Basiothia medea (6)
Agrius convolvuli (22)
Nephele comma (25)
Hippotion celerio (8)
Basiothia medea (14)
Temnora pseudopylas (7)
Temnora sp. (3)
Atemnora westermanii (5)
Basiothia medea (4)
Agrius convolvuli (2)
Nephele comma (7)
Nephele comma (85)
Hippotion celerio (11)
Temnora sp. (2)
Basiothia medea (44)
Atemnora westermanii (3)
Leucostrophus hirundo (4)
Basiothia medea (3)
Nephele comma (2)
Hippotion celerio (3)
Nephele comma (10)
Hippotion celerio (31)
Agrius convolvuli (9)
Temnora sp. (2)
Basiothia medea (7)
Daphnis nerii (6)
Hyles sp. (5)
Agrius convolvuli (1)
Basiothia medea (2)
Temnora pseudopylas (3)
Agrius convolvuli (1)
Nephele comma (4)
Hippotion celerio (2)
Basiothia medea (8)
Nephele comma (11)
Hippotion celerio (9)
Basiothia medea (12)
Hippotion celerio (17)
Nephele comma (2)
Agrius convolvuli (20)
Hippotion celerio (3)
Agrius convolvuli (40)
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HAWKMOTH POLLINATION IN EAST AFRICA
205
A)
B)
C)
D)
E)
F)
G)
H)
I)
J)
K)
I)
M)
N)
O)
P)
Q)
R)
S)
Figure 2. Foraging times of hawkmoths observed to visit flowers of dryland plant species in Kenya. Sunset is indicated
by the dashed line. See text for details of observations of dawn foraging times.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
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D. J. MARTINS and S. D. JOHNSON
Foraging time per flower (s)
6
5
4
3
2
1
0
20
40
60
80
100 120 140 160 180
Flower tube length (mm)
Figure 3. The relationship between corolla tube length
and the mean duration of visits to flowers by hawkmoth
species: Agrius convolvuli (䊊), Basiothia medea (䊐), Hippotion celerio (䉮), Nephele comma (䉭).
2005, and 117 records during the long rains at Mpala
in 2005. Up to 12 hawkmoth species were recorded at
each of the study sites, of which three (Leucostrophus
hirundo N = 11, Macroglossum trochilus N = 7,
Cephonodes hylas N = 4) are primarily diurnal and
are highly generalized foragers. The most commonly
encountered hawkmoths with short/medium length
tongues were Nephele comma (N = 284), Hippotion
celerio (N = 162), Basiothia medea (N = 114), Atemnora westermanii (N = 10), Temnora sp. (N = 9) and
Hyles sp. (N = 5). Agrius convolvuli (N = 167) was the
most common long-tongued moth observed. There is a
sharp discontinuity between the proboscis lengths
of A. convolvuli and the other hawkmoths (Table 3).
There was a marginally non-significant positive
saturating relationship between hawkmoth tongue
length and number of plant species visited (Fig. 4B).
Agrius convolvuli with the longest tongue (108 mm)
and Nephele comma (tongue length = 42 mm) exhibited the highest levels of polyphagy, each having
been recorded feeding from flowers of 11 plant
species.
Number of hawkmoth visitors
(A)
FLORAL
MORPHOLOGY, ANTHESIS
AND NECTAR PROPERTIES
Tube length (mm)
Number of plant species visited
(B)
Hawkmoth tongue length (mm)
Figure 4. A, the relationship between corolla tube length
and number of recorded hawkmoth visitors for plants
studied in Kenya. B, the relationship between hawkmoth
tongue length and number of recorded host nectar plants.
Most of the plant species that were visited by hawkmoths have corolla tubes of intermediate length,
while a few species have long corolla tubes in excess
of 10 cm in length (Table 2). Species with long
corolla tubes (> 10 cm) included Crinum macowanii,
Ammocharis tinneana, Conostomium quadrangulare,
and the two orchids Aerangis brachycarpa and Rangaeris amaniensis. A smaller number of ‘brush’
flowers were also visited by hawkmoths including
Maerua decumbens and Gynandropsis gynandra, the
latter a species that is also visited by honeybees
during the day.
The flowers visited by hawkmoths tended to open
synchronously before or at dusk. Flowers remained
open and available to hawkmoths for varying periods
of time from one evening (Conostomium quadrangluare) to 4 weeks (Rangaeris amaniensis). Most of the
flowers, other than the two orchid species, remained
open for just one and rarely two evenings. All of the
flowers that opened in the evenings were still open
and available before dawn the next day, but wilted
in the hours after sunrise. Scent, where present,
was always produced more strongly in the evening
(C. quadrangulare, Jasminium spp., P. ouranogyne,
A. brachycarpa,
R. amaniensis,
T. mombassana,
C. macowanii, A. tinneana). A few species had no
obvious or weak scent (G. gynandra, Cycnium spp.).
Nectar volumes in the flowers visited by hawkmoths ranged from 0.47 to 30.5 mL (Table 2). The
highest volumes of nectar were found in long-spurred
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
HAWKMOTH POLLINATION IN EAST AFRICA
207
Table 2. Flower corolla length, nectar volumes and nectar concentrations for plants actively visited by hawkmoths at
Kitengela and Mpala (N = 10 flowers sampled for each species)
Flower tube/spur
length (mm)
Nectar
volume (mL)
Species
Mean
SD
Mean
SD
Mean
SD
Aerangis brachycarpa
Rangaeris amaniensis
Conostomium quadrangulare
Crinum macowanii
Datura stramonium
Gladiolus ukambanensis
Ammocharis tinneana
Gynandropsis gynandra*
Cycnium tubulosum
Turraea mombassana
Jasminium fluminense
Maerua decumbens*
Pavetta abbysinica
Carissa edulis
Cycnium ajugifolium
Jasminium floribundum
Lantana camara
Acokanthera schimperi
Plectranthus pubescens
158.5
155.8
115.0
105.0
99.6
97.1
84.35
47.6
45.6
43.2
39.7
36.8
28.4
20.3
18.9
18.4
10.1
8.02
6.1
0.44
0.99
0.13
0.45
0.67
0.42
2.82
1.84
6.01
1.62
0.14
2.85
1.25
0.86
1.43
0.71
0.71
0.37
0.7
20.19
9.93
2.6
30.5
8.9
10.7
29.2
0.5
1.55
1.4
0.61
0.88
1.72
0.55
0.51
0.47
0.6
0.43
0.32
2.76
1.18
0.54
9.85
2.24
2.63
6.73
0.18
0.68
0.47
0.21
0.35
0.66
0.21
0.24
0.12
0.17
0.17
0.1
†
†
13.9
19.8
21.8
18.4
22.5
48.7
21
21.3
17.8
16.2
18.8
23.1
14.4
13.7
16.8
13.2
18.8
†
†
1.58
2.94
2.76
0.67
3.17
3.74
4.38
1.08
2.29
3.35
1.36
2.18
1.82
1.34
3.35
1.70
4.96
Nectar Conc. (%)
*No tube, brush type flower, length is that of anthers.
†Concentration varies throughout the nectar column (see Martins & Johnson, 2007).
orchids (over 20 mL in Aerangis spp. and R. amaniensis) and specialized Amaryllidaceae (c. 30 mL in
C. macowanii).
ANALYSIS
OF TRAIT ASSOCIATIONS
Plants with very long corolla tubes tended to produce
fewer flowers (Fig. 5A). This relationship was also
significant when based on independent contrasts
(Fig. 5B). There was a strong positive relationship
between corolla tube length and nectar volume, both
when using conventional regression (Fig. 5C) as well
as independent contrasts (Fig. 5D). Nectar sugar concentrations ranged from 9 to 55% (typically 10–20%,
Table 2) and did not show a significant relationship
with corolla tube length using either regression based
on conventional (P = 0.91) or contrast data (P = 0.16).
Sugar content per flower showed a strong positive
relationship with corolla tube length in the conventional regression (Fig. 5E), but this relationship was
not significant when based on independent contrasts
(Fig. 5F).
ANALYSIS
OF THE
KENYAN
FLORA
A total of 277 species of plants were found to have
traits consistent with the floral syndrome of pollina-
tion by hawkmoths. This represents about 4% of the
total known flora of Kenya (c. 6000 spp.). The distribution of tube/spur lengths among these species is
bimodal (Fig. 6), consisting of a large number of
species with tubes between 20 and 60 mm, and a
small but distinct group of apparently specialized
species with tubes/spurs longer than 100 mm.
DISCUSSION
The results of this study highlight the extraordinarily
asymmetric nature of hawkmoth pollination systems.
While hawkmoths are clearly polyphagous (Table 1),
the plants they visit are often highly specialized
(Table 2). Plants adapted for pollination by hawkmoths in Kenya tend to fall into two main guilds. The
first guild, consisting of plants with corolla tubes
20–50 mm in length, is visited mainly by a diverse
assemblage of hawkmoth species with tongues
30–50 mm in length (Table 3, Fig. 4). The second
guild, consisting of plants with corolla tubes > 90 mm
in length, is visited almost exclusively by the hawkmoth Agrius convolvuli (Fig. 4) which is the only one
of the observed hawkmoths with a tongue long
enough to reach nectar in these flowers. Only
two long-tongued hawkmoths species frequent the
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
208
D. J. MARTINS and S. D. JOHNSON
1000
(A)
0.4
100
10
1
10
100
0.0
-0.2
-0.4
-0.6
-0.8
0.0
1000
(C)
100
0.4
nectar volume contrasts
10
Nectar volume (ul)
Slope = -0.87
R2 = 0.30
P = 0.013
-1.0
1
1
0.1
Slope = 0.94
R2 = 0.70
P < 0.0001
0.01
1
10
100
0.1
0.2
0.3
0.4
0.5
0.6
(D)
0.3
0.2
0.1
Slope = 0.59
R2 = 0.51
P = 0.0005
0.0
-0.1
1000
0.0
(E)
0.3
100
0.1
0.2
0.3
0.4
0.5
0.6
(F)
0.2
sugar content contrasts
Sugar content per flower (mg)
(B)
0.2
flower number contrasts
Number of flowers
Slope = -0.82
R2 = 0.48
P = 0.001
10
1
0.1
Slope = 0.44
R2 = 0.47
P = 0.001
0.2
0.2
-0.1
Slope = 0.16
R2 = 0.11
P = 0.17
-0.2
-0.3
0.01
1
10
100
1000
Tube length (mm)
0.0
0.1
0.2
0.3
0.4
0.5
0.6
Positivized tube length contrasts
Figure 5. Relationships between flower corolla tube length and other floral traits for native plants visited by hawkmoths
in Kenya. Panels on the left are relationships based on actual value. Panels on the right are relationships based on
phylogenetically independent contrasts. A, B, tube length; C, D, nectar volume; E, F, sugar content per flower.
Figure 6. Bimodal distribution of tube lengths in the
sphingophilous flora of Kenya (N = 277 species).
drylands of Kenya, and one of these, Coelonia fulvinotata, is restricted to riverine forest habitats with a
primarily forest distribution. This means that A. convolvuli is probably responsible for the pollination of
almost all of the very long-tubed plants in non-forest
habitats in the drylands of Kenya. This ‘Agrius’ guild
includes several Crinum species, Ammocharis tinneana, Pancratium tenuifolium, Conostomium quadrangulare, Ipomoea longituba, Ruellia megachlamys,
Gladiolus candidus (formerly G. ukambanensis) and
Thunbergia guerkheana (Table 1). The effectiveness of
Agrius convolvuli as a specialized pollinator in the
drylands includes both its ability to disperse widely
as well as the abundance of larval host plants (e.g.
Ipomoea and Convolvulus spp.) at both sites which in
effect can be viewed as ‘subsidising’ the pollination
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
HAWKMOTH POLLINATION IN EAST AFRICA
209
Table 3. Proboscis lengths (mm) of common dryland hawkmoths netted feeding at flowers
Male
Female
Hawkmoth species
Mean
SD
N
Mean
SD
N
Agrius convolvuli
Hippotion celerio
Daphnis nerii
Basiothia medea
Temnora pseudopylas
Nephele comma
108.2
41.2
40.6
22.8
21.7
41.5
6.53
3.63
0.48
0.48
1.16
0.47
14
27
7
11
3
9
96.5
41.5
40
21
22.5
–
0.71
0.71
–
–
0.76
–
2
2
1
1
8
–
needs of the specialized dryland flora (Feldman,
Morris & Wilson, 2004).
The discontinuity in proboscis length between the
smaller hawkmoths and A. convolvuli and Coelonia
fulvinotata may explain why putatively hawkmothpollinated plants in Kenya show a bimodal distribution in corolla tube length (Fig. 6). This result is
similar to the bimodal patterns found by
Alexandersson & Johnson (2002) and Anderson et al.
(2010) in their studies of light-trapped hawkmoth
assemblages in South Africa, and Agosta & Janzen
(2005) in their study of the Guanacaste assemblage in
Costa Rica. The latter study also confirmed that
resource overlap by foraging hawkmoths is dependent
on tongue length, with long-tongued species able to
access nectar resources from short/shorter-tubed
flowers but not vice versa. This trend towards greater
polyphagy in longer tongued hawkmoths was apparent in our data set, but was marginally nonsignificant (Fig. 4B). Alarcon et al. (2008) suggested
that very long-tongued hawkmoths visit flowers of
fewer plant species than short-tongued ones, but this
was inferred from analysis of pollen load data, which
may not be accurate if hawkmoths fail to make
contact with anthers of flowers with tubes that are
shorter than the proboscis. It is important to note
that hawkmoth tongue lengths also reflect phylogenetic patterns (Kawahara et al., 2009) with one clade
of larger-bodied moths containing most of the longtonuged species (this group includes Agrius convolvuli, which is the main long-tongued pollinator we
observed).
Although long-tubed species show apparent specialization for pollination by A. convolvuli, this hawkmoth is highly polyphagous and was recorded as a
visitor on many of the plant species with short-tubed
flowers (Supporting Table S1). In most instances of
foraging on short-tubed species (Fig. 1A, G), A. convolvuli does not make effective contact with anthers
and stigmas, and thus probably acts mainly as a
nectar robber (see also Johnson, 1995). Contrary to
the conventional idea that Lepidoptera are only able
to feed effectively on dilute nectar (Kingsolver &
Daniel, 1979), A. convolvuli was observed to feed on
nectar that ranged in mean sugar concentration from
14% in Conostomium quadrangulare to 47% in
Gynandropsis gynandra (Table 2). Hawkmoths with
short and medium length tongues fed not only on
hawkmoth-adapted flowers, but also on many other
species, including bee-pollinated species with very
short corollas, such as Grewia bicolor (Fig. 1D).
Hawkmoths have been observed to be polyphagous in
a number of other studies (Haber & Frankie, 1989;
Agosta & Janzen, 2005) covering a range of habitats,
visiting both generalized flowers and those adapted
for pollination by other animals, such as bats (Baker,
1961, 1963, 1970; Lack, 1978; Baum, 1995; Alarcon
et al., 2008) as well as from cultivated garden flowers
in Kenya (Ng’weno, 1981) and crops such as coffee
and papaya (Martins & Johnson, 2009).
Apart from their very long corolla tubes, plants in
the A. convolvuli guild tend to have fewer flowers
(Fig. 4A, B) and produce more nectar than shortertubed plants (Table 2, Fig. 4C, D). Our interpretation
is that because A. convolvuli is highly polyphagous,
plants specialized for pollination by this moth are
required to produce large volumes of nectar in order
to induce fidelity by this insect during its short period
of foraging. The trade-off resulting from this investment in floral biomass and nectar is that fewer
flowers overall can be maintained. This supports the
idea of a flower-size number trade-off (Sargent et al.,
2007).
It is doubtful that the positive association between
flower tube length and nectar volume merely reflects
the mechanical constraints on fitting large volumes of
nectar into short corolla tubes, as even short-tubed
flowers rarely have nectar that fills more than onethird of the corolla tube. Instead, we argue that this
association arises because a plant with long-tubed
flower that filter out most hawkmoths must entice
highly polyphagous hawkmoths with a reward that is
much greater than that of sympatric plants with
short-tubed flowers that are equally accessible to
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
210
D. J. MARTINS and S. D. JOHNSON
these insects. We expect this association to apply to
both nectar volume and nectar sugar content.
However, the latter association, while also positive,
was marginally non-significant when tested using
independent contrasts (Fig. 5F).
SEASONAL
AND TEMPORAL PATTERNS OF
HAWKMOTH FORAGING
A dozen hawkmoth species, out of a total of c. 100 spp.
in Kenya, were regularly recorded on the wing during
extensive observations at the study sites (Table 1). In
southern Arizona, Alarcon et al. (2008) recorded 14
hawkmoth species in the local fauna, but just three
were regularly encountered. In the drylands of
Kenya, hawkmoths are constrained by availability
and distribution of larval foodplants as well as flowers
for the adults to feed from. The seasonal abundance of
hawkmoths observed is consistent with data for the
region from museum specimens and earlier widespread collecting (Pinhey, 1962; Carcasson, 1976), as
well as from other regional studies that focused
on collecting hawkmoths (Taylor & Brown, 1972;
Robertson, 1977; Kingston & Nummelin, 1998). This
pattern is also consistent with studies from other
parts of the tropics (Owen, 1969) and the wet–dry
seasonal regions of the neotropics where hawkmoths
have been studied (Haber & Frankie, 1989; Agosta &
Janzen, 2005).
The opportunistic feeding behaviour (polyphagy)
and rapid dispersal ability of hawkmoths are two
factors to consider when interpreting the temporal
patterns of hawkmoth foraging. Tropical hawkmoths
are large, powerful, long-lived, and also known to
mate and lay eggs repeatedly (Pinhey, 1962; Agosta &
Janzen, 2005). In the drylands of Kenya, the patchy
and unpredictable distribution of many specialized
flowers precludes extended foraging constancy. Hawkmoths forage for short specific periods of time (Fig. 2).
Observations suggest that nectar resources are
rapidly depleted by foraging hawkmoths, especially
when large numbers of moths are involved, as is
typical on the shrub Carissa edulis and the creeper
Jasminium floribundum. This opportunistic feeding
was observed to extend to introduced invasive species
such as Lantana camara and Tithonia diversifolia
(Supporting Table S1), as also observed in Madagascar by Wasserthal (1997).
Predation also seems to play a role in the restricted
temporal patterns of foraging observed in this study.
The major predators of hawkmoths feeding at flowers
in the drylands of Kenya were observed to be insectivorous bats (primarily the yellow-winged bat, Lavia
frons). These bats catch moths at flowers and as they
disperse between patches (D. J. Martins, unpublished
data). Bat activity and hawkmoth foraging seem to be
closely linked, with two separate peaks, one lagging
slightly behind the other at dusk, and probably preceding the other at dawn. We also observed that bats
are hunting moths in the middle of the night. If this
is widely observed, then predation could be another
reason for primarily dusk/after dusk foraging by
hawkmoths, as moths have widely been shown to
modify their behaviour in relation to bat predation
(Lack, 1978; Fenton & Fullard, 1981; Acharya &
McNeil, 1998).
The observation in this study of a pre-dawn feeding
pattern at both sites further reinforces the idea of
opportunistic foraging and nectar depletion. This
trend has rarely been reported before for tropical
hawkmoth pollination studies (Murcia, 1990), but it is
probably more widespread. Pre-dawn foraging follows
the same patterns as dusk/after dusk, but during this
time hawkmoths begin to feed from flowers in the
dark before dawn, and foraging ends by the time the
sky is light (c. 06:15–06:25 h in Kenya). At both sites,
fewer moths foraged at dawn than at dusk, in terms
of both abundance and species diversity, indicating
that dawn foraging is a ‘second’ lesser peak of activity
while dusk foraging remains the main time for
feeding from flowers.
CONCLUSIONS
Interactions between flowers and hawkmoths in
Kenya appear to be highly asymmetrical with both
short- and long-tongued hawkmoths exhibiting high
levels of polyphagy, while flowers, especially longtubed ones, show high levels of specialization. Polyphagous foraging by hawkmoths is of obvious benefit
in an environment which is highly seasonal and
unpredictable. The high number of East African
plants that show apparent specialization for pollination by hawkmoths is likely to reflect the sheer abundance of these insects during certain seasons. Overall,
asymmetry in these flower–hawkmoth interactions,
especially those involving short-tubed flowers and
short-tongued moths, makes it unlikely that they
have been shaped by pairwise coevolution (Janzen,
1980; Whittall & Hodges, 2007).
Despite the lack of reciprocal specialization, hawkmoths are undoubtedly responsible for the evolution
of the long-tubed flowers in this system, and this
extends to other components of the African flora, most
notably orchids (Martins & Johnson, 2007). The reliance of the specialized sphingophilous dryland flora
on a single abundant and widespread hawkmoth
species, Agrius convolvuli, is indicative of the importance of long-tongued hawkmoths as ‘keystone pollinator’ species for distinct guilds of flowering plants
(Johnson et al., 2004).
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213
HAWKMOTH POLLINATION IN EAST AFRICA
While our studies documented key aspects of these
interactions, such as floral traits, hawkmoth diversity, and foraging patterns, more research is required
to establish the extent to which these plants are
ecologically dependent on hawkmoths as pollinators.
It would also be interesting to determine the effect
that invasive plants (many of which are visited by
hawkmoths, see Supporting Table S1) are having on
native plant species, either as competitors or as facilitators for pollination.
ACKNOWLEDGEMENTS
We thank the director and staff of the Mpala Research
Centre for logistical support and assistance; the Kenya
Orchid Society for help with locating orchid populations and loaning plants for experiments and measurements; and the director and staff of the National
Museums of Kenya and East African Herbarium for
permission to work in their collections. Assistance,
useful comments, and logistical support were provided
by A. Powys, I. and A. Robertson, H. and R. Campbell,
N. Croze, E. Krystall, J. and S. E. Mamlin,
P. Kahumbu, N. Georgiadis, M. N. Mutiso, N. E. Pierce,
D. Haig, R. and M. Leakey, M. Kinnaird, C. Ngarachu,
P. Masinde, A. Kontos and S. Miller. We thank two
anonymous reviewers for making very helpful comments that improved the manuscript. This research
was supported by a fellowship to D.J.M. from the
Smithsonian Institution Women’s Committee and the
Mpala Research Centre and by the University of
KwaZulu Natal’s School of Life Sciences.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Figure S1. The phylogeny of plant species visited by hawkmoths that was used for analyses of phylogenetically
independent contrasts.
Table S1. Phenology and habit of dryland flower species visited by hawkmoths. Habit: T, tree; S, shrub; H,
herbaceous; B, bulb (herbaceous); E, epiphyte; Cr, creeper. Distribution: C, common; Sc, scattered clumps/
stands; R, rare.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 199–213