Bolantcal Journal of the Linnean Sociely (1985),91: 395-414. \Yith 8 figures
The Macaronesian bird-flower element and its
relation to bird and bee opportunists
JENS MOGENS OLESEN
Bolanical Instilute, University of Aarhus,
Nordlandsvej 68, DK-8240 Risskov, Denmark
R t w s e d Ju!v 1984, accepted f o r publicalion Nouember I984
OLESEN, J. M., 1985. The Macaronesinn bird-flower element and its relation to bird and
bee opportunists. Canarina canariensis, three Isopfexis species and Lofus berfhelotii, among other
species, have been supposed to be bird pollinated. None of their flowers reflect UV light and the
volume of nectar produced is relatively high with low sugar concentration, indicating bird
pollination. This study gives the first report of birds visiting and thus pollinating these species. Syluia
melanocephala, S. conspicillata and Phylloscopus collybifa visited I. canariensis and C . canariensis Rowers.
Isoplexis scepfrum and Digitalis obscura are regarded as transitional species anthecologically between
I. mnariensis/I. tsahelliana and European Digitalis species.
ADDITIONAL KEY WORDS:-Bird
pollination
-
Bombus
-
Canarina
-
floral biology
-
Isopfexis
Lotus.
CONTENTS
Introduction . . . . . . . . . . .
Observations and discussion . . . . . . .
Taxonomy, phytogeography, ecology and distribution
Floral biology.
. . . . . . . . .
Flower visitors or pollinators . . . . . .
General discussion and conclusion . . . . . .
Acknowledgements
. . . . . . . . .
References.
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395
396
396
398
406
411
412
413
INTRODUCTION
We have been aware for several years of a putative existence of ornithophily
in some Macaronesian species: Canarina canariensis (L.) Vatke (Campanulaceae)
(Vogel, 1954: 300, 302), Isoplexis canariensis (L.) G . Don (Scrophulariaceae)
(Vogel, 1954: 252), I. isabelliana (Webb) Masf. (Yeo, 1972), Lolus berlhelolii Masf.
(Fabaceae) (Vogel, 1954: 2 13), and Musschia wollaslonii Lowe (Campanulaceae)
(Vogel, 1954: 328). The flowers of these species possess some truly
ornithophilous characters: red-orange-yellow corollas, plenty of nectar, and (at
least in some of them) absence of scent (Stiles, 1981).
In spite of the apparent attractiveness of these Macaronesian bird flowers and
their relatively high energy rewards there seem to be no reports of any visitors
0024-4074/85/070395
+ 20 $03.00/0
395
0 1985 The Linnean Society of London
396
J. M. OLESEN
and pollinators. Vogel (1954: 213, 328) regards these bird flowers as an evidence
of an earlier presence of Nectariniidae on the Macaronesian archipelagos.
Today no flower birds are found on the islands, but several other bird species
found on the Macaronesian Islands, residents and migrants, are known to be
occasional flower visitors. For example Sylviidae (Ash, 1959; Porsch, 1924),
Paridae (Porsch, 1924) and Ploceidae (Passer domesticus (L.) on Agave americana
L. in Malaga, S Spain, personal observation) are known to include in their diet
nectar from bird-pollinated plants introduced to European gardens, such as Aloe
and Hibiscus, and from native European species, such as Prunus, Crocus and
Primula. Porsch (1924) cites observations made by Lowe in 1896, that Sylvia
atricapilla (subspecies atricapilla?) visits Hibiscus species on Tenerife, and Parus
caeruleus (subspecies tenertffae?) Abutilon species on Gran Canaria.
Extensive and unique areas of natural vegetation of Tenerife (especially),
Gran Canaria and Madeira have disappeared with ever increasing rapidity in
recent decades, but with the establishment and initiatives of different services
and institutions, the efforts for natural conservation have been greatly
intensified. The most sensitive type of vegetation on the islands is without doubt
the laurel forest (laurisilva). This broadleaved evergreen forest characterized by
Laurus azorica (Seub.) Franco is probably the oldest type of climax vegetation in
Macaronesia (Miocene or Pliocene; Bramwell, 1972, 1976; Dansereau, 1968;
Lems, 1960; Meusel, 1965; Sunding, 1970), and during the Tertiary period may
have had an enormous area of distribution in S Europe and N Africa. Its
survival in Macaronesia may be due to the buffering influence of the oceanic
climate (Aldridge, 1976; Dansereau, 1968; Humphries, 1976; Lems, 1960).
According to Parsons (1981) less than 60 km2 of the laurisilva is left on the four
western islands, maybe only 10% of its original area.
The bird-flower element belongs to the laurel forest, the tree heath (fayal
brezal), and the pine forest (pinar). Today, these types of vegetation are more
or less threatened (Voggenreiter, 1974). In recent times pine forests have been
more or less re-established (Parsons, 1981). Lotus berthelotii may already be
extinct in the wild, and is only found in gardens.
Several investigators of the Canary Islands' flora have regretted that we do
not know the reproductive systems, namely the pollinators, of these rare species
(Bramwell, 1976; Valentine, 1976). Nobody seems to believe that the species
today are pollinated by recent Macaronesian bird species (Yeo, 1972).
The findings reported here are based on field observations on Tenerife
(Canarina canariensis, Isoplexis canariensis) , herbarium material from the Botanical
Museum, Copenhagen, Denmark (C. canariensis, Isoplexis species), and living
material from the Botanic Gardens, Aarhus and Copenhagen, Denmark
(I. isabelliana, I. sceptrum, and Lotus berthelotii) .
OBSERVATIONS AND DISCUSSION
Taxonomy, phytogeography, ecology and distribution
The genus Canarina L. (Campanulaceae) comprises three species: C. canariensis
(L.) Vatke, C. abyssinica Engler, and C. eminii Ascherson ex Schweinf. (Hedberg
el al., 1961). Canarina canariensis is known from four of the Canary Islands:
Tenerife, Gran Canaria, La Palma and Gomera (Bramwell & Bramwell, 1974:
MACARONESIAN BIRD FLOWERS
397
204). The other two species are found in highland areas and mountains in
E Africa (Hedberg et al., 196 1). This so-called Macaronesian-afromontane
distribution (Hedberg el al., 1961) or Macaronesian-S and E African
distribution (Bramwell, 1976) indicates a quite different climatic and
vegetational situation in the past in N Africa.
Canarina canariensis grows in the remnants of the laurel forest, in Erica shrub, at
roadsides in the mountains, in forest margins, and in ravines in shaded places.
The species has a restricted distribution, locally common on Tenerife but rare
on the other islands (Bramwell & Bramwell, 1974). It flowers from November to
May (sometimes to June) (Ceballos & Ortuiio, 1951; Hedberg et al., 1961; and
personal observations).
Isoplexis (Lindley) Bentham (Scrophulariaceae) is a n endemic Macaronesian
genus of four species: I. canariensis (Tenerife, La Palma), I. isabelliana (Webb)
Masf., I. chalcantha Svent. & O’Shan. (both endemic to Gran Canaria and very
closely related) and I. sceptrum (L. fil.) Loudon (Madeira) (Bramwell &
Bramwell, 1974: 199; Eriksson, Hansen & Sunding, 1974: 50; Werner, 1960,
1964).
The relationships between Isoplexis, especially I. sceptrum, and Digitalis section
Frutescentes Bentham, especially D. obscura L. emend. Pau, in E and S Spain and
N Morocco, forests and maquis (Werner, 1960), have been stressed by several
authors (Meusel, 1953, 1965; Rivas Goday, 1946; Werner, 1960). Isoplexis and
D . obscura seem to be relicts of the rich Tertiary forest flora. The relations
between the two taxa encompass chemical, karyological, morphological and
perhaps anthecological ones (Bramwell el al., 1972; Delgado Benitez et al., 1969).
Descriptions of habitat types are given by Werner (1964) and Bramwell &
Bramwell (1974: 199). Isoplexis canariensis blooms during winter and spring
(personal observation), while I. sceptrum blooms in July-September (C.-0.
Ottosen, personal communication; and personal observation on a greenhouse
specimen at Aarhus).
One member of the genus Lotus L. (Fabaceae), L. berthelotii, is assumed to be
ornithophilous, but other Macaronesian species of Lotus may perhaps attract
birds too, such as L.purpureus Webb, an endemic to the Cape Verde Islands.
Lotus berthelotii is probably extinct in its natural habitat, La Florida and Baranco
de Tamadaya, Tenerife (Bramwell & Bramwell, 1974: 150). Cultivated
examples in the Botanic Garden, Copenhagen, bloom in March-July and
sometimes also in September-October. Cross-pollination is assumed to be
necessary. The Lotus clone in the Botanic Garden, Copenhagen, does set some
seeds (pods) when hand-pollinated, but the gardener has never succeeded in
raising seedlings (K. E. Auvinen, personal communication).
The genus Musschia (Campanulaceae) consists of two species, M . wollastonii
and M . aurea (L. fil.) DC., and is endemic to Madeira. Musschia wollastonii
flowers in July-September. Musschia may also be a relict bird-flower genus.
Elvers (1978) reports observations of M . aurea being visited by nectar-drinking
lizards and more rarely by the endemic Bombus maderensis Erlandsson.
AZorina vidalii (Watson) Feer (Campanulaceae) from the AGores may on closer
study show itself to be related to the Macaronesian bird-flower element. It
flowers in August-September and has a rather stiff corolla, 10-35 mm long
(Tutin el al., 1976: 93).
398
J . M. OLESEN
Figure I . UV photograph of corolla of Canarina canariensis. Filter: Kodak Wratten 18A, a UVtransmitting filter. Left petal is seen from the inside; right petal from the outside. Grey scale and
techniques according to Kevan, Mulligan & Robertson (1973).
Floral biology
General descriptions of morphology and phenology of flowers of most of the
above-mentioned species have been presented by several authors (Schmucker,
1936, Canarina; Vogel, 1954, Canarina, Isoplexis, Lotus and Musschia; Hedberg et
al., 1961, Canarina; Bryndum Christensen, Dalgaard & Hamann, 1970, Isoplexis;
Faegri & Pijl, 1971, Isoplexis; Yeo, 1972, Canarina and Isoplexis; Proctor & Yeo,
1973, Isoplexis), and will not be repeated here, but a few additional observations
of anthecological interest are given.
The stiff corollas of Canarina and Lotus have reddish colours. Canarina has
white-yellow-green flower buds, the opened flowers become red-orange and
finally dark red. Lotus has deep red flowers with a dark midline on the standard.
These colours have without doubt been the main indication in the diagnosis of
ornithophily. The flowers of Canarina and Lotus do not seem to reflect UV light
when photographed through a UV-transmitting filter (Figs 1, 2) (Kevan, 1972;
Kevan, Mulligan & Robertson, 1973). This observation is in accordance with
current belief about ornithophily.
Figure 3 shows the flower morphology of Isoplexis species and Table 1
summarizes some differences and similarities in floral characters between three
Isoplexis species.
MACARONESIAN BIRD FLOWERS
399
Figurr 2. UV photograph of flowers of IsopfexiF isabelliana ( l e f t )and Lotus berthelotii (right).
Only Isuplexis isabelliana has been tested for any U V reflection, and none was
found (Fig. 2). If the other two Zsoplexis species also lack UV reflection, the shift
in corolla colour from red to yellow, when one moves from I. canariensis to
I. isabelliana to I. sceplrum (Table l ) , makes the flowers (more) visible to bees.
Going again from the Canarian Isoplexis species to I . sceplrum in Table 1 the
increase in length and cross-sectional area of the corolla tube creates a kind of
landing platform or ‘garage’ to visiting insects (the cross-sectional area of an
individual of Bumbus canariensis PCrez (see later) is 60-80 m m 2 ) . Together with
changes in consistency of the corolla and in the orientation of the flower, this
variation in flower structure seems to document an evolutionary shift from
ornithophily towards the modern melittophilous Digitalis species. In this context
an anthecological study of Digilalis obscura would be very welcome.
Isuplexis species, Lolus berlhelolii and Canarina canariensis have been tested for
scent, but only Zsoplexis species seem to have a faint one, detectable by humans
only after enclosure of the flowers for a day or so in an airtight jar. T h e scent is
sweet and Freesia-like.
16
400
J. M. OLESEN
Figure 3. Flower morphology of Isoplexis species. A. I. canaricnsis.
B. I. isabclliana. C . I. sceptrum.
+o1
MACARONESIAN BIRD FLOWERS
Table 1. A comparison of floral characters between the three
Isoplexis species. *Uncorrected for atmospheric water, see text
Floral character
~~~~
~
~~~
I . canariensis
I . rsabriliana
I. sreptrum
red 1 -olangcI
red-orange
orange-yellow
stiR/tough
stiff/ tough
less stiffitough
-
-
~~
Colour
Consistency
Prrsenre 01'
landing platform
Area of entrance
hole t o nrrtar ( m m ' )
Orientation of
(+i
25-35
40-50
90-1 10
horizontal
slightly upright
slightly hanging
flower
Length of
corolla tube
Sren t
Sugar c o nce ti I ra Iion
(.
9 mm
c. 9 m m
c.
16mm
(+I
+
10* 25
20
22
3
19
4
(+)
of nectar [ (',,)
Percentage of
drformcd pollrn
Canarina canariensis is able to produce 0.18-0.28 g nectar per flower during a
period of 2-3 days, Schmucker (1936). No estimates of nectar volume were
made in the present study, but the figures given above seem very high. No
nectar is present in the buds. The sugar is a 25'!, w/w solution ( N = 15, range
20-30; 23"C, corrected to 20°C; full sun; Bellingham & Stanley Pocket
Refractometer; the inner part of Baranco del Infierno, S Tenerife, 9 February,
13.00 hours). Withering flowers may have concentrations above 507,.
Measurements of nectar volume and concentrations of sugar of flowers of
I. canariensis are given in Fig. 4. The volume of nectar per flower (all age classes)
is 11.8 pl ( N = 23, range 0-27.6; 14"C, cloudy; Parc Forestal, E Tenerife,
5 February, 17.00 hours). The upper and youngest flowers in each inflorescence
did not contain nectar, but only water. This phenomenon may be explained by
the climate prevailing in the habitats of I. canariensis: fog and rising clouds
caused by the trade-wind. These movements of very humid air masses may
cause water to be trapped in the flowers. The amount of water in these 'water
Rowers' was 7.0 p1 per flower ( N = 6 , range 1.2-12.3). If the 'sugar flowers' are
corrected for 7.0 pl water, the volume of nectar is only 4.8 pl. From Fig. 4 alone
i t is not possible to tell anything about the rhythm in nectar production as a
function of flower age. The concentration of sugar in 'sugar flowers' is 10% w/w
( N = 1 1 , range, 2-15; 14"C, corrected to 20°C) and the amount of sugar per
Rower is 0.66 mg. If the concentration is corrected for water added from the
exterior the concentration of sugar becomes 25O/:, w/w (Table 1).
Greenhouse specimens of I. isabelliana and I. sceptrum had 10-20 and 10-46 pl
of nectar per flower, respectively, after several days of production. The
J.
402
M. OLESEN
.....
..
!I
0
;;:::
....
0.
....
0
~
z
2
3
4
5
6
7
8
9
10
II
12
13
14
Consecutive position of flower
Figure 4. Nectar volumes (Ill) and sugar concentrations (% wjw) of individual Rowers of lsoplexis
canariensis as a function of their consecutive position on the inflorescence. The low numbers refer to
the lower positions. The 25 flowers belonged to the three inflorescences (I, 0; II, e; III,*) of the
individual under observation. The flowers nos 7 & 8, inflorescence I, had just been visited by a
Phylloscopus col(ybita.
concentration of sugar was 20% wfw (N=4, range 18-22; 26°C, corrected to
20°C; 11.00 hours) and 22% wfw (N = 20, range 15-40; 22°C, corrected to
20°C; 14.00 hours) respectively. These concentrations are closer to the corrected
percentage for /. canariensis than to the uncorrected, thus supporting the idea
that a considerable amount of water is gained by the flowers from the tradewinds.
The two outer stamens in flowers of/. sceptrum are strongly S-curved. When
their anthers open, two drops of nectar begin to increase in size and slide along
the stamens. In the hanging flowers of/. sceptrum the curved stamens seem to be
important in preventing the nectar from running out of the flowers.
The quantity of nectar produced per flower per day, percentage sugar in
nectar and sugar production per flower per day, for a greenhouse example of
L. berthelotii are given in Fig. 5. The flowers reach an age of c. I 0 days
unpollinated and with a temperature regime of max. 20-30°C and min. 6°C.
The nectar data is based on measurements of c. 20 flowers for a week; these
measurements were made at c. 10.00 hours each day. The average values were
constant from the fifth day onwards. Nectar production per flower per day is
16
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10
Age of flower (d)
I
rr
m
I![
Age class of flower
Figure 5. The productivity of nectar (in 111, N=61) and sugar (in mg, N=44) per flower per day
and percentage of sugar in the nectar (as mg/100 mg nectar, N=45) in relation to flower age class
in Lotus berthelotii under controlled greenhouse conditions. (The age classes are defined in caption to
Fig. 6.)
404
J. M. OLESEN
9.2 p1 (N=61, range 3.4-15.9). Concentration of sugar is 1201" w/w (.N=45,
range 9-20). The amount of sugar produced per flower per day is 1.24 mg
(N=44, range 0.35-2.17).
Hummingbirds and many species of bees seem to prefer nectar with relatively
high concentrations of sugar. Laboratory hummingbirds choose concentrated
sugar solutions of up to 49y0 w/w (Hainsworth & Wolf, 1976; Stiles, 1976).
Workers of Apis mellifera most frequently visit sugar concentrations in the
range 30-50y0 w/w (Corbet, 1978; Heinrich, 1975). Nectar of below 1800 sugar
w/w is non-profitable to honey bees, due to the high energy costs to evaporate
water to produce honey (see Percival, 1969).
The concentrations of sugar in nectar of many hummingbird-pollinated
flowers are relatively low, c. 20% w/w (Baker, 1975). Baker (1975) argues that
the higher viscosity of more concentrated nectar would reduce the foraging
efficiency of the birds, especially under low temperature conditions, as in
montane regions.
Bolten & Feinsinger (1978) present arguments which suggest the lower sugar
concentrations in many hummingbird flowers function primarily to exclude
bees, and not to attract birds. They find that bird flowers from tropical America
fall into two distinct groups: exclusive and accessible flowers. The first group
comprises flowers which attract birds with relatively concentrated nectar
(20-33y0) and exclude bees in their morphological structure. The second group
excludes bees on account of their relatively thin nectar (19-24%), thereby
leaving larger amounts of sugar to the birds. In this group morphology does not
hinder the access of bees.
The three genera of Macaronesian bird flowers studied fit reasonably well
into these two flower categories. The flowers of Canarina are without doubt the
most exclusive. Often the flowers hang like bells with the opening of the corolla
pointing downwards, though a relatively large portion of the flowers are turned
by the supporting plants, Rubus ulmifolius Schott. and Euphorbia canariensis L., in
different directions and may to some extent be accessible to insects. The
hypothesis of Baker (1975) of correlations between nectar viscosity and altitude
of habitat could have been tested on Canarina, but was not. It might have been
interesting to compare the concentrations of nectar in the (relict?) population of
Canarina in Baranco del Infierno, c. 200 m, with the populations in the montane
forests of Anaga Peninsula, E Tenerife, c. 900 m. Both nectar characteristics and,
at least to some extent, morphology indicate that the flower of Isoplexis is a bird
flower. Both I. canariensis and I. isabelliana have no landing platform, but
bumblebees have been observed visiting I. isabelliana in the Botanic Garden in
Copenhagen. Here they grasp and enter the flowers sideway between the upper
and lower half of the corolla. In the garden of forestry, Ribeiro Frio (860 m ) ,
Madeira, a large individual of I. sceptrum with probably more than 100
inflorescences has been observed to be visited by individuals of Bombus maderensis.
The visits were performed in the 'legitimate' way seen in Digitalis species (C.-0.
Ottosen, personal communication).
These observations confirm the earlier statements about the closer position of
I. sceptrum to the bumblebee-pollinated genus Digitalis (Table 1, Fig. 3). Lotus
has flowers truly accessible to insects, but secretes a very thin nectar, which
without doubt will exclude bees. Bumblebees have been observed approaching
Lotus pendants in the Botanical Garden, Copenhagen, but they never try to
MACARONESIAN BIRD FLOWERS
A
Figure 6. A. A triplet of flowers of Lotu berthelofii (the numbers 1-111 refer to three of the four age
classes: I, standard folded up (max. 2 days old); 11, standard unfolded (max. 6 days old); 111,
stigma visible on the tip of the keel (max. 8 days old); and I V , stigma and its pollen load visiable on
the tip of the keel (max. 10 days old). B. Hypothetical situations: a bird seeks nectar in flowers ofL.
berihclofii, the head of the bird presses the keel down, thereby pumping the pollen out.
405
406
J. M. OLESEN
land, so this hypothesis can not be explored further (K. E. Auvinen, personal
communication).
Finally it has to be stressed that the hypothesis about the two flower
categories is founded on hummingbirds and their flowers, and the situation
could be quite different for bird flowers in the Old World.
Baker & Baker (1975) have deepened our understanding of the chemical
nature of nectar. They used a so-called ‘histidine scale’ for comparative studies
of amino acid concentrations in nectar. Every nectar collection was scored
against this scale. In this study nectar samples of I. canariensis and L. berthelotii
were treated in the manner described by Baker & Baker (1975).
Isoplexis canariensis scored 3 on the scale (.N=4), and L. berthelotii scored 4
( N = 49, range 3-5). All spots were violet; yellow ones, an indication of presence
of proline/hydroxyproline, were not found in the samples. Baker & Baker (1975)
give a table relating score against histidine scale to type of pollinator. The
category ‘Old World bird’ has a mean score of 3.31. This figure fits excellently
with scores of L. berthelotii and I. canariensis. ‘Bat’, ‘Hummingbird’, ‘Generalized
fly’ and ‘Short-tongued bee’ have scores of 3.75, 4.86, 4.35 and 4.59 respectively,
the rest of the categories lie above these figures. But it has to be stressed that
there could be a rather wide range of scores intraspecifically, as with Jasminum
oficinale reported by Baker & Baker (1975).
All the species studied are protandrous. Canarina has flowers with a kind of
secondary pollen presentation comparable with what is known from Campanula.
Isoplexis species expose their pollen from anthers situated under the upper
corolla lip. Pollen grains are spheroid with a diameter of 20-24 pm. According
to data given in Table 1 the individual of I. isabelliana studied had an unusually
high fraction of deformed pollen. The cause of this high figure is unknown. Lotus
berthelotii presents its pollen by a pumping mechanism known in other species of
Lotus. A pressure on the keel sends the pollen out in big clouds (Fig. 6).
European species of Lotus exude small doses of sticky pollen when visited. There
exist no records of visiting animals, but in Fig. 6 it is demonstrated how a bird
probing for nectar might press the keel and pump pollen grains out around the
throat and forehead. The habitat of L. berthelotii suggests its pollinators could be
ground-foraging birds. This is known for some Australian ground-level
flowering Fabaceae (Baker, 1979).
Flower visitors or pollinators
During a stay on the Canary Islands in January-February 1982, some
observations of flower visitors or pollinators of I. canariensis and C. canariensis
were made at two localities.
Isoplexis canariensis: Parc Forestal, Anaga, Tenerife. An individual (1.5 m in
height with three inflorescences and the previous year’s infructescence) was kept
under observation for 2 days at the beginning of February. Other flowering
species, which might compete for the services of pollinating animals, were: Erica
arborea L., Geranium canariense Reuter, Hypericum grandifolium Choisy, Senecio
uppendiculatus (L. fil.) Sch. Bip., Sonchus acaulis Durn.-Cours. and Viburnum rigidum
Vent. (nomenclature according to Bramwell & Bramwell, 1974).
O n 5 February at 14.00 hours a Bombus canariensis was observed several times
MACARONESIAN BIRD FLOWERS
40 7
very near the Isoplexis plant and at one time it seemed to try to land on one of
the inflorescences, but was probably scared away.
At 17.00 hours on the same day a brown bird was seen visiting one of the
inflorescences for 5-7 s, probing for nectar in two flowers. It came out from the
Erica shrub and disappeared again in the same direction. It perched under one
of the inflorescences on the leafless part of the stem (observation 1). T h e flowers
visited were checked for remains of nectar, and in contrast to the rest of the
flowers contained no nectar (Fig. 4).
On 8 February at 15.00 hours a bird with a faint yellow colour on the breast,
and light dark stripes down along the flanks, c. 100 mm in length, perched on
two or three flowers, with a visiting time of 6-9 s (observation 2).
At 15.20 hours, probably the same bird came back, perching as it had 20 min
earlier, and probing two flowers. The visiting time was c. 6 s (observation 3 ) .
At 15.50 hours, a blue-ashy coloured bird with a somewhat darker cap, white
breast, a dark line through the eye and a red eye-ring, c. 150 mm in length, came
flying from the nearby trees and visited the Isoplexis plant. It probed for nectar
in three or four flowers for 12-15 s (observation 4, Fig. 7).
Figure 7 . An individual of Sylvia melanorephala leucogashe probing for nectar in the observed Isoplexis
canarirnsiJ.
408
J . M. OLESEN
At 16.00 hours the same species came back. Again it probed for nectar in
three of four flowers for c. 10 s (observation 5).
No other animals were seen visiting the Zsoplexis plant or found inside its
flowers. This could have been due to rather cloudy, rainy and cold weather.
The birds seemed to know the flower-type from previous visits. The birds in
observations 1, 2 and 3 were identified as Phylloscopus collybita canariensis
(Hartwig), and the birds in observations 4 and 5 were identified as Sylvia
melanocephala leucogastre (Ledru) following the descriptions given by Bannerman
(1963: 233 & 221, respectively).
Canarina canariensis: The innermost part of Baranco del I nfierno, Adeje, Tenerife.
This deep and narrow gorge is dominated in its inner part by trees and bushes,
especially Salix canariensis Chr. Sm. and Rubus ulmifolius.
O n 9 February at 13.00 hours one certain and one uncertain observation of
birds visiting the Canarina flowers were made. The bird was rather small, seemed
dully brown on the back, sandy or dark creamy on the breast. It perched on the
stems of Rubus ulmifolius. It was probably too heavy to perch on the Canarina
itself.
O n 10 February at 08.50 hours an observation of a bird visit was made at the
same site. This bird was more uniform brown on the back and the belly.
Suddenly it came out from the shrub, sat on a bramble branch just under a
Canarina flower and thrust its head into the bell. The head of the bird nearly
disappeared. The situation has been reconstructed in Fig. 8. The light
Figure 8. An individual of Sylvia cowfiicillafa orbitalis probing for nectar in a Canarina canaricnsis
flower. I t perched on a Rubus stem.
MACARONESIAN BIRD FLOLVERS
409
conditions in the gorge were too bad for photographing. After just one visit it
again returned into the thicket. This bird was, by the aid of the description
given by Bannerman (1963: 227), identified as the species Sylvia conspicillata
orbitalis (Whalberg).
No insects were ever seen in the flowers of C. canariensis. At least 50 flowers
were closely examined for tiny insects and other small animals hidden in the
interior of the corolla, but none was found.
The bee Bombus canariensis has only recently received recognition as a species
(Erlandsson, 1979). It is endemic to the Canarian archipelago, and i t seems to
be the only representative of the genus. The bumblebee is almost entirely black,
with only the apex of the abdomen white. However, some individuals according
to Erlandsson (1979) have a mixture of yellow and black hairs revealing the
relationships of the species to B. terrestris L., which has its nearest localities in
Algeria.
During my stay a few individuals of B. canariensis were observed and caught:
29 January, 1 1 .OO hours; one specimen caught in Sulvia canariensis L. (E of
Giiimar, Tenerife, c. 200 m); 30 January, 13.00 hours; one specimen observed in
shrub of Rubus ulmifolius (above El Rejo, Gomera, c. 700 m); 2 February, 14.00
hours; one specimen observed visiting the big capitula of Sonchus acaulis Durn.Cours.; and one specimen caught foraging in the vegetation of Spartocytisus and
Chamaecytisus, with two large deep-orange corbicular pollen loads made up of
pure Fabaceae pollen (S to Caserio Erjos, Tenerife, c. 200 m); and 5 and
8 February in the afternoon; specimens were observed several times flying up
and down the mountainside above the individual of Zsoplexis canariensis under
observation (Parc Forestal, Anaga, Tenerife, c. 900 m). The bumblebees caught
had a proboscis length (promentum+glossa) of 8 mm ( N = 3 , range 7-9), and
should in spite of the narrowness of the corolla of I. canariensis be able to reach
the nectar (Table 1). No nectar-robbing holes were observed on the flowers.
‘lhe chiffchaff subspecies Phylloscopus collybita canariensis is extremely common
in the five western islands, and is here the only resident representative of the
genus. The eastern island, Lanzarote, has its own chiffchaff, Phylloscopus collybita
rollybila exsul Hart ert. This bird has not been reported from Fuerteventura.
These two Canarian subspecies are in several characters, such as brighter colour
and smaller size, distinct from the European subspecies: Ph_ylloscopus coliybita
iberica Ticehurst, Phylloscopus collybita collybila (Vieillot), and Phylloscopus collybita
abietina (Nilsson) (Johansen, 1947). The first two of these have been found as
winter visitors in the eastern Canary Islands (Bannerman, 1963; 237).
Phylloscopus collybita iberica breeds in S European lowland forests of oak.
Phylloscopus colLvbita collybita is a NW-Central European subspecies expanding
rapidly in mixed forest areas. Finally, Phylloscopus collybita abietina is a taiga-bird
confined to NE European coniferous forests (Dybbro 1976: 248-249; Lack,
1971; 293-294). The winter quarters are, according to Lack (1971: 294),
restricted to N Africa. Phylloscopus collybita is not known to breed in N Africa.
.Johansen (1947) considered P. collybita to be a species of western palaeoarctic
origin, which rather recently in the last interglacial period has expanded its
breeding range from SW Europe to E Europe. Bannerman (1920), partly
opposing this hypothesis, regards the Canarian chiffchaffs to be European
migrants. Arguments against this view are found in Volscae (1955). According to
Johansen ( 1947) the Canarian Phylloscopus species comprise the most ancient
410
J. M. OLESEN
populations of all recent chiffchaffs. This view was further explored by Volscae
(1955), who calculated the Canarian avifauna to be highly dominated by
species of palaeoarctic origin (89%).
Phylloscopus collybita canariensis is extremely numerous in most habitats from the
Euphorbia semi-desert to the Retama, nesting even in gardens. It occupies a
range of habitats, which in Europe is shared by several Phylloscopus species and
subspecies. Phylloscopus collybita canariensis has a total body length of 105 mm
( N = 10, range 95- 120; skins from the Zoological Museum, Copenhagen), and
a bill length of 9 mm (range 9-10). Food preferences seem to be insects (HaldMortensen, 1969), but an indication of a much wider range of food items in
winter and in summer quarters is given by Pettett (1975). He reports an
observation of chiffchaffs consuming acacia gum in the Sudan. In the most
eastern Danish island, Christianss, the spring is substantially delayed in
comparison with the main and more oceanic parts of the country. Migrants of
the genera Phylloscopus and Sylvia may thus experience a shortage of animal food
in the spring on this island. Several observations made by Laursen & Holm
(1981) indicate that the birds may eat pollen and other floral parts as a dietary
supplement. Based on the observations of foraging in the flowers of Zsoplexis
canariensis and the measurements of bill length Phylloscopus collybita canariensis
should be able both to act as pollinator and to extract nectar from the flowers
(Table 1). Phylloscopus collybita canariensis is probably also able to visit Canarina
canariensis successfully.
The Canary sardinian warbler (Sylvia melanocephala leucogastre) and the Canary
spectacled warbler (S. conspicillata orbitalis) together with the dusky blackcap
( S . atricapilla obscura Tschusi) are the only breeding members of the family
Sylviidae in the Canary Islands (Bacallado, 1976). Bacallado (1976) believes the
Canarian Sylviidae to be postglacial immigrants. If the Sylviidae have
experienced successive invasions the time of their first arrival may lie far back in
time, in spite of their weak differentiation. The three species of $ylvia may
secondarily have spread to the arid parts of the islands when these belts
widened. However, according to Volsse (1955) and Bacallado ( 1976) the
Tertiary relict avifauna belonging to the laurel forest consists only of two ‘laurel
pigeon’ species today. The Pinus forest has probably existed during the whole
Pleistocene and together with this vegetation type we find the first massive
appearance of several bird species.
Both the sardinian and the spectacled warbler are found all over the
archipelago (Bacallado, 1976). Bannerman ( 1963: 224) writes: “In Tenerife the
Sardinian Warbler ascends to a greater altitude . . . there is little doubt that it
nests in the tree-heath zone where it is probably more plentiful than anywhere
else in the archipelago”. It may also be observed in the barrancos. Sylvia
conspicillata is also a very common bird, especially in S Tenerife. It is mostly
observed in the semi-desert belt along the whole maritime zone, and in the
barrancos. It seems to be absent from the forests. It is found in connection with
many different plant species such as those of Euphorbia. The one observed on
10 February, probably a female, was diving in and out of the bramble shrub, in
accordance with one of its many common names ‘zarzalero’, the one in the
brambles. The total body length of the sardinian warbler is c. 140 mm ( N = 3,
range 135-140), and the length of bill c. 10 mm ( N = 2); the analogous figures for
the spectacled warbler are 120 mm (N=8, range 110-125), and 9 mm ( N = 8 ,
MACARONESIAN BIRD FLOWERS
41 1
range 8-9). According to Jordano (1982) Jjlvia melanocephala in Spain eats Rubus
fruits. The diet was composed of animal and vegetable matter in equal amounts.
In stomachs of Sylvia melanocephala, Herrera (1981) found fruit remains and seeds
in 83% and 28O; of the stomachs, respectively. Nine different plant species were
represented. Sylvia melanocephala is a typical bird species of the Mediterranean
region. Sylvia conspicillata was rarely observed eating Rubus fruits (Jordano,
1982). According to Hald-Mortensen (1969) its preferred food seems to be
insects. Sylvia atricapilla probably also prefers a mixed diet.
The data on habitat preferences and bill length support the conclusion that
Sylvia melanocephala may be an important pollinator of Isoplexis and probably also
of Canarina. On the other hand, Sylvia conspicillata, due to its more narrow
habitat choice, is only a possible pollinator of Canarina in its southern localities
on Tenerife.
In Ash (1959) an old phenomenon often observed has found its solution.
Migrating birds from S and NW Europe have frequently been found with a
substance adhering to their bills. Ash (1959) estimates that no more than 1-2%
of the spring migrants carry this substance, which he identifies as Citrus pollen.
Among the bird species were Sylvia atricapilla and Phylloscopus collybita.
I n order further to reveal any possible flower-visiting habits by Canarian
birds the bills and feathers of head and neck of all specimens of Canarian
Sylviidae, Phylloscopus and several other genera in the skin collections of the
Zoological Museum, Copenhagen, were brushed for any residual pollen grains.
The material from the birds was brushed onto a glass slide mounted with a
‘Scotch’ double-sided tape. The method was adopted and modified from
Iwarsson (1979), who examined the skins of African Nectariniidae. I found no
pollen grains of any kind. T h e reason may be due to a non-existence of any
flower-visiting habits, to a meticulousness of the collectors in cleaning the skins,
or due to the birds themselves cleaning their bill and forehead. In view of the
study of Iwarsson (1979) on sunbirds, which are regular flower birds, and in fact
are dependent on the existence of bird flowers, where he found less than 10
grains per preparation, the results of my study may not seem surprising. In spite
of the absence of grains in the skins, there is plenty of ornithological
documentation of a tendency to visit flowers in several groups of passerines in
summer and perhaps especially in winter quarters.
GENERAL DISCUSSION AND CONCLUSION
Conclusions drawn from data on nectar, corolla colours, scent and other
morphological characteristics confirm the supposed ornithophilous nature of
Isoplexis species, Lotus berthelotii, and Canarina canariensis. These species have their
origin in the Tertiary Period, while flower-visiting birds do not appear as fossils
until the Pleistocene, but undoubtedly originated considerably earlier.
Therefore, the story of Old World bird-flower coevolution probably begins at
some time in the early to mid-Tertiary. Without doubt the Macaronesian birdflower element belongs to a richer bird-flower flora once distributed in the
humid forests in the Mediterranean and N Africa. Recent African taxa may be
remnants of the same flora, such as, the E African species of Canarina and Erica.
Some modern S African species of Erica have bird flowers.
This study gives examples of three different modes of Old World bird
412
J. M. OLESEN
pollination: Ground foraging, Lotus; perching and nectar drinking on the same
plant, Zsoplexis; and perching and nectar drinking on different plants, Rubus and
Canarina. These plants might have been pollinated by different sunbirds in the
past.
With changes in climate and vegetation in S Europe and N Africa new plant
species appeared: the bee-pollinated Digitalis and Lotus species. They have
different corolla colours, lower nectar volume per flower, and higher sugar
concentrations than their bird-pollinated relatives. The relation Canarina-Campanula might be the third example. The concentrations of sugar, as in
Digitalis, lie between 21 and 40% (Percival & Morgan, 1965) and in European
Lotus between 30 and 50% (Percival, 1969). The concentration of sugar in
Macaronesian species of Lotus other than L. berthelotii is not known.
Macaronesia has, compared with the Mediterranean region, a relatively poor
Hymenopteran fauna. The sea has acted as a dispersal barrier. The importance
of bee pollination on the Macaronesian Islands is not known, but is probably
low.
The Macaronesian bird-flower element has both in the past and in the
present relied on birds, whether sunbirds or other groups. If sunbirds have been
present in the past, they probably disappeared when the arid zones widened and
ultimately resulted in a shortage of their food plants.
Some time in the past the two species of Sylvia, Phylloscopus collybita, Bombus
canariensis, and probably other animal groups too, have included nectar from
these bird flowers in their diet. These animals harvest a wide variety of food
items with a low predictability in time. They have thus been named
opportunists in this context (McKey, 1975). This plastic way of foraging might
have been favoured and intensified after their colonization of the islands due to
a lack of congeneric competition. The idea of niche widening on islands relative
to nearby continents has been a matter of dispute (McArthur & Wilson, 1967;
Williamson, 1981). Since red flowers generally seem to attract opportunistic and
pollinating birds, the supposed extinction of L. berthelotii in nature might be
explained by herbivores and/or man.
Of all the European species of Bombus, it was a Bombus close to the Bombus
terrestris-type which reached Macaronesia. Bombus terrestris and a few other
European and American Bombus species are, compared with most bumblebee
species: more often nectar robbers; use more non-flower food sources (e.g. honey
dew, juice from ripen fruits and anemophilous pollen); have a broad-spectred
use of food plants; possess stronger mandibles and shorter probosces; are more
abundant at a habitat; have wider geographical and altitudinal ranges; emerge
earlier from hibernation; are more long-distance dispersers; and may be
aggressive. Together, these characters constitute a kind of opportunist
syndrome. Bombus canariensis was able to reach the Canaries and to obtain food
from a wide variety of plants from different vegetation types and altitudinal
zones.
ACKNOWLEDGEMENTS
I am very grateful to Dr Peter F. Yeo for his helpful suggestions and
comments. I thank the directors and curators of the Botanic Gardens,
Copenhagen and Aarhus, the Botanical Museum, Copenhagen, and the
MACARONESIAN BIRD FLOWERS
413
Zoological Museum, Copenhagen, for use of facilities. M r K. E. Auvinen and Dr
C.-0. Ottosen, Copenhagen, Dr P. Svec, Charles University, Praha, and Dr
M. Fraissinet, Istituto e Museo di Zoologia, Napoli, are gratefully acknowledged
for their information, as is the important assistance of A.-M. Jensen and
0. Vorre.
REFERENCES
ALDRIDGE, A. E., 1976. Evolution within a single genus: Sonchus in Macaronesia. In G. Kunkel (Ed.),
Bio<geo<grapband Ecology in the Canary Islands: 279-291. The Hague: Junk.
ASH, J . S., 1959. Pollen contamination of birds. British Birds, 52: 424-426.
BACALLADO, J . J., 1976. Notas sobre de la distribuqion y evoluqion de la avifauna canaria. In G. Kunkel
(Ed.), Biogeography and Ecology in the Canary Islands: 4 13-43 I . The Hague: Junk.
RAKER, H. G., 1975. Sugar concentrations in nectars from hummingbird flowers. Biotropica, 7: 37-41.
BAKER, H. G., 1979. Anthecology: Old Testament, New Testament, Apocrypha. N e w zealand Journal of
Botany, 17: 431-440.
BAKER, H. G. & BAKER, I., 1975. Studies of nectar-constitutions and pollinator-plant coevolution. In L. E.
Gilbert & P. H. Raven (Eds), Coevolution oJAnimals and Plants: 10Ck139. Austin: University of Texas Press.
BANNERMAN, D. A,, 1920. List of the birds of the Canary Islands, with detailed reference to the migratory
species and the accidental visitors, VII (Summary and general conclusions). Ibis, 2: 519-569.
BANNERMAN, D. A., 1963. Birds of the Atlantic Islands, I . Edinburgh: Oliver & Boyd.
BOL'I'EN, A. B. & FEINSINGER, P., 1978. Why do hummingbird flowers secrete dilute nectar? Biotropica,
10: 307-309.
BRAMWELL, D., 1972. Endemism in the flora of the Canary Islands. In D. H. Valentine (Ed.), Taxonomy,
Phytogeograpb and Euolution: 141-159. London: Academic Press.
BRAMWELL, D., 1976. The endemic flora of the Canary Islands; distribution, relationships and
phytogeography. In G. Kunkel (Ed.), Biogeograply and Ecology in the Canary Islands: 207-240. The Hague:
Junk.
BRAMWELL, D. & BRAMWELL, Z., 1974. W i l d j o w e r s of the C a n a v Islands. London: Stanley Thornes.
BRAMWELL, D., HUMPHRIES, C. J., MURRAY, B. G. & OWENS, S. J., 1972. Chromosome studies in
the flora of Macaronesia. Botaniska Notiser, 125: 139-152.
BRYNDUM CHRISTENSEN, T., DALGAARD, V. & HAMANN, O., 1970. Oversigt over Madeirasjora.
Copenhagen: Institute of Systematic Botany.
CEBALLOS, L. & O R T U R O , F., 1951. Estudio sobre la vegetation y l a j o r a forestal de las Canarias Occidentales.
Madrid: Ministerio de Agricultura, Instituto Forestal de investigaqiones y experiencias.
CORBET, S . A,, 1978. A bee's view of nectar. Bee World, 59: 25-32.
DANSEREAU, P., 1968. Macaronesian Studies. 11. Structure and functions of the Laurel Forest in the
Canaries. Collectanea Botanica, 7: 227-280.
DELGADO BENITEZ, J., VELAZQUEZ, J. M., BRETON, J. L. & GONZALEZ GONZALEZ, A., 1969.
Glucosidos y agluconas de las Scrophularias. Anales de quimica, 65: 8 17-824.
DYBBRO, T., 1976. D e danske ynglefugles udbredelse. Copenhagen: Dansk Ornithologisk Forening.
ELVERS, I., 1978. The Madeiran lizard-flower connection observed in a natural habitat. Botaniska Notiser,
131: 159-160.
ERIKSSON, O., HANSEN, A. & SUNDING, P., 1974. Flora of Macaronesia. Check-list of vascularplants 1974.
Umei: Department of Biology.
ERLANDSSON, S . , 1979. Bombus canariensis Ptrez, 1895 n.stat. and B . maderensis n.sp. from the Macaronesian
Islands. Entomologica Scandinavica, 10: 187-192.
FAEGRI, K. & PIJL, L. VAN DER, 1971. The Principles ofPoNination Ecology, 2nd edition. Oxford: Pergamon
Press.
HAINSWORTH, F. R. & WOLF, L. L., 1976. Nectar characteristics and food selection by hummingbirds.
Oecologia, 25: I0 1 I 13.
HALD-MORTENSEN, P., 1969. Fugle-Aves. In M. Gissel Nielsen, L. B. Holm-Nielsen & S. Jeppesen (Eds),
Studierejse Tenerife 1968: 161-187. Arhus: Den naturhistorisk-geografiske Faggruppe.
HEDBERG, 0..JONSELL, B., JUNELL, L., LUNDQVIST, N. & OLSSON, O., 1961. Monograph of the
genus Canarina L. (Campanulaceae). Svensk Botanisk Tidrkrift, 55: 17-62.
HEINRICH, B., 1975. Energetics of pollination. Annual Review of EcologV and Systematics, 6: 139-170.
HERRERA, C. M., 1981. Fruit variation and competition for dispersers in natural populations of Smilax
aspera. Oikos, 36: 5 1-58.
HUMPHRIES, C. J., 1976. Endemism and evolution in Macaronesia. In G. Kunkel (Ed.), Biogeograpb and
Ecolog~in the Canary Islands: 171-199. The Hague: Junk.
IWARSSON, M., 1979. Pollen from bills of African sunbirds (Nectariniidae). Botaniska Notiser, 132: 349-355.
JOHANSEN, H., 1947. Gransangerens geografiske variation. Dansk Ornithologisk Forenings Tidsskriji, 41:
198-2 15.
-
414
J. M. OLESEN
JORDANO, P., 1982. Migrant birds are the main seed dispersers of blackberries in Southern Spain. Oikos, 38:
I 83- 193.
KEVAN, P. G., 1972. Floral colors in the high arctic with reference to insect-flower relations and pollination.
Canadian Journal of Botany, 50: 2289-2316.
KEVAN, P. G., MULLIGAN, G. A. & ROBERTSON, A. R., 1973. A gray-scale for measuring reflectance
and color in the insect and human visual spectra. Ecology, 54: 924-926.
LACK, D., 1971. Ecological isolation in birdr. Oxford: Blackwell.
LAURSEN, K. & HOLM, E., 1981. Fugls fede pa Christianse. Kaskelot, 53: 5 8 4 3 .
LEMS, K., 1960. Botanical notes on the Canary Islands. 11. The evolution of plant forms in the islands:
Aeonium. Ecology, 41: 1-17.
McARTHUR, R. & WILSON, E. O., 1967. The Theory of Island Biogeography. Princeton: University Press.
McKEY, D., 1975. The ecology of coevolved seed dispersal systems. In L. E. Gilbert & P. H. Raven (Eds),
Coevolution of Animals and Plants: 154-191. Austin: University of Texas Press.
MEUSEL, H., 1953. Uber Wuchsformen, Verbreitung und Phylogenie einiger mediterran-mitteleuropaischer
Angiospermen-Gattungen. Flora, 139: 333-393.
MEUSEL, H., 1965. Die Reliktvegetation der Kanarischen Inseln in ihren Beziehungen zur sud- und
mitteleuropaischen Flora. Gesammelte Vortrage iiber Moderne Probleme der Abstammungslehre, I : I 17-1 36.
PARSONS, J. J., 1981. Human influences on the pine and laurel forests of the Canary Islands. Geographical
Reuiew, 71: 253-27 I .
PERCIVAL, M., 1969. Floral Biology. Oxford: Pergamon Press.
PERCIVAL, M. & MORGAN, P., 1965. Observations on the floral biology of Digitalis species. .New
Phytologist, 64: 1-22.
PEYI’ETT, A,, 1975. Chiffchaff feeding on acacia gum. British Birds, 68: 4 5 4 7 .
PORSCH, O., 1924. Vogclblumenstudien, I. Jahrburh der wissenschajlirhen Botanik, 63: 553-706.
PROCTOR, M. & YEO, P., 1973. The Pollination of Flowers. London: Collins.
RIVAS GODAY, S., 1946. Sobre la Habitagion de la “Digitalispurpurea L. (sensu lato)”. Anales del Instituto Josi
Celestino Mutis de Farmacognosia, 5: 123-153.
SCHMUCKER, T., 1936. Uber die Bliiten von Canarina Campanula. Berichte der Deutwhen Botanischen GesellschaJ,
54: 230-239.
WILES, F. G., 1976. Taste preferences, color preferences, and flower choice in hummingbirds. Condor, 78:
10-26.
WILES, F. G., 1981. Geographical aspects of bird-flower coevolution, with particular reference to Central
America. Annals of the Missouri Botanical Garden, 68: 323-351.
SUNDING, P., 1970. Elementer i Kanarieyenes flora, og teorier ti1 forklaring av floraens opprinnelse. Elyttia,
28: 229-259.
‘I’UTIN,‘I. G., HEYWOOD, W. H., BURGES, N. A., MOORE, D. M., VALENTINE, D. H., \$’ALTERS,
S. M. & WEBB, D. A., 1976. Flora Europaea, 4: 93. Cambridge: University Press.
VALENTINE, D. H., 1976. Conclusion. In G. Kunkel (Ed.), Biopography
.
~ and
. Ecology in the Canary Islands. The
Hague: Junk.
VOGEL, S., 1954. Bliitenbiologische Typen als Elemente der Sippengliederung. Botanische Studien (Jena), I :
1-338.
VOGGENREITER, V., 1974. Geobotanische Untersuchungen an der natiirlichen Vegetation der Kanarinsel
Tenerife als Grundlage fur den Naturschutz. Dissertationes Botanicae, 26: 1-7 18.
VOLSBE, H., 1955. The breeding birds of the Canary Islands. 11. Origin and history of the Canarian
avifauna. Videnskabelige Meddelelser f r a Dansk .Vaturhistorisk Forming i Kebenhaan, 117: 1 17-1 78.
WERNER, K., 1960. Zur Nomenklatur und Taxonomie von Digitalis L. Eotanische Jahrbucher fir $wtematisrhr
Botanik (Martin-Luther-Universitat, Halle- Wittenberg), 79: 2 18-254.
WERNER, K., 1964. Die Verbreitung der DigitahArten. Wissensrhaffliche Zeitsrhrft der Martin-LutherUniwrsitat, Halle- Wittenberg, 13: 453486.
WILLIAMSON, M., 1981. Island Populations. Oxford: University Press.
YEO, P. F., 1972. Miscellaneous notes on pollination and pollinators. Journal of .Natural History, 6: 667-686.