Journal of Natural History

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Miscellaneous notes on pollination and

P.F. Yeo

To cite this article: P.F. Yeo (1972) Miscellaneous notes on pollination and pollinators, Journal of Natural History, 6:6, 667-686, DOI: 10.1080/00222937200770621 To link to this article: https://doi.org/10.1080/00222937200770621

Published online: 17 Feb 2007.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tnah20 J. nat. Hist., 1972, 6 : 667-686

Miscellaneous notes on pollination and pollinators

P. F. YEO University Botanic Garden, Cambridge

Introduction On the grounds that I was a botanist with an interest in insects I was asked many years ago to participate in the writing of a book on pollination. The book is due to appear soon (Proctor and Yeo, in the press). My contribution to it is largely based on previous publications and I have not done any experi- mental work on the subject. However, I have made some observations from time to time and some of these seem to be worth publishing, though most are not suitable for inclusion in the forthcoming book. These, together with some thoughts stimulated by the literature and my continuous contact with British and exotic in the Cambridge Botanic Garden, form the very mixed bag of notes presented here.

Terminology Guide-marks The phrase 'nectar guide ', which derives from the German Saftmaal (now Saftmal), a term coined by Sprengel (1793, p. 15), is familiar to all who have studied floral biology. However, some nectarless flowers have patterns like nectar guides and the term is then inappropriate. Such flowers are fl'equent in Leguminosae--subfamily Lotoideae--where lines or blotches appear to indicate the entry to flowers which are visited by insects for pollen. Further, it seems likely that some floral markings may be specifically ' pollen guides ' (or ' Pollenmale '--Vogel, 1963, p. 733). I have therefore'adopted the non- committal phrase 'guide-mark '. Lex (1954) has found that scent sources in flowers may also have the form of patterns which have a guiding function, and has used the terms Duftmal (' scent guide ') and Farbmal (' colour guide '). These could be replaced respectively, by ' olfactary guide-marks ' and ' visual guide-marks '. Frequently the scent is produced by the coloured guide-marks.

Window-panes A frequent occurrence in insect-trapping flowers (e.g. , Ascle- piadaceae and Aristolochiaceae) is a zone of more or less colourless translucent tissue bounded by dark-pigmented areas in the chamber where the insects are temporarily imprisoned. This zone evidently has the function of attracting trapped insects towards it. McCann (1943), Van der Pijl (1953) and Faegri & Van der Pijl (1966) have used the phrase 'light-window' for these zones. However, since the function of a window is normally to let in light the expression is somewhat tautologous. A window may be either open or shut, and as we are here dealing with a closed translucent area I propose the use of the phrase 'window-pane '. Bright openings which insects can pass through are also frequent in insect-trapping flowers, often taking the form of lantern-like

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Published online 17 Feb 2007 668 t ). F. ¥eo structures at the entrance (Vogel 1954); the phrase 'window-pane' is self- evidently not applicable to these, for which the phrase 'window opening' has been used by Faegri & Van der Pijl (1966, pp. 71, 88).

Functional morphology of flowers Secondary presentation and protection of pollen The Papilionate flower of Leguminosae, subfamily Lotoideae, has presum- ably evolved from an approximately actinomorphic Caesalpinioid flower, first by developing declinate stamens and pistil, and second by the modification of the two lowest petals to form a keel embracing these organs. This stage of evolution is in fact reached within the Caesalpinioideae (as in Cereis); in the Lotoideae there seems to be no change of principle in the action of the flower, as compared with Cercis, but numerous refinements occur, some involving permanent retention of the anthers within the keel. Declination of stamens and pistil is necessarily associated with an oblique or nearly horizontal floral axis. It occurs chiefly in flowers pollinated by Lepidoptera, which may feed on the wing, and by bees, for which the stamens act as the alighting place instead of the petals. Declination in Lepidoptera- flowers (e.g. Crinum--Voget 1954, p. 97.) may be well-suited to the light brushing of the under-surfaces of a hovering insect which necessarily has only one feeding posture. In bee flowers (for example, Cassia Caesalpinioideae) it must certainly make the flowers less suitable to all Diptera but the most highly flower-adapted, as one does not usually see these insects perching on a collection of horizontally protruding stamens. It would also probably make the collection of pollen by these insects, and possibly also by the more primitive bees, more difficult. Indeed, it could conceivably have begun as a means of protecting pollen from being eaten by any insects. However, most bee- pollinated flowers have compromized on pollen-protection, making their pollen available to bees, if not to other insects, and relying for pollination on grains that have not been collected up into the insects' corbicula. The ' Papilionate 't flower is, in fact, characterized by the protection of the stamens by the petals, and by the return of the petals to a function of supporting the by their being directed forwards. Once the stamens have become fully protected, a mechanism has to be provided to release the pollen when an insect visits the flower; this consists basically of obliging the insect to push its head into the flower and to depress the wing-petals with its legs, so drawing the keel downwards and in some cases opening the upper edge of the keel. The details of this mechanism were carefully investigated in various genera by Mfiller (1873, 1883). The pushing of the head into the flower is done chiefly in order to get at the nectar, but in some cases it also seems to be a necessary part of the procedure for releasing the pollen, and the insertion of the extended proboscis even into nectarless Papil- ionate flowers is a habit of Bombus lucorum (Brian 1957), but there is no suggesUon in the behaviour of these insects that they are actually testing for the presence of nectar. In such flowers (e.g. Ononis, Lupinus, Sarothamnus) the insect visits are purely for pollen. Only bees seem to be really well adapted

~From Papilionaceae, the name of the Lotoideae at familial rank. Miscellaneous notes on pollination and pollinators 669 to pushing aside barriers of the kind described and such obstacles, which evidently render the flowers more specific to these insects, are found widely in other families with different floral mechanisms, such as Ranunculaceae (Aconitum, Delphinium), Boraginaceae (Symphytum) and Scrophulariaceae (Antirrhinum, Linaria). Thus the raison d'etre of the Papilionate flower appears to be bee-pollination, though in some cases the mechanism has atro- phied even though bees seem to be the pollinators (Amorpha fruticosa), and there has, of course, been adaptive radiation in this great group towards use of other pollen vectors which renders the mechanism irrelevant (e.g. birds in Erythrina ). In many Lotoideae the stamens never protrude from the flower, the pollen being extruded from the tip of the keel by a piston mechanism. Mfiller (1873, 1883) demonstrated a great and, to my mind at present, unaccountable diversity in these extrusion mechanisms. While this diversity is puzzling, it seems safe to conclude that selection acts strongly in favour of such arrange- ments in preference to the protrusion of the anthers themselves. In the flowers with extrusion mechansims the pollen is released into the keel and the anthers themselves shrivel up before the flower opens (fig. 1).

stam~ tube

FIG. 1. cornieulatus. (A) Side view of flower with one wing petal, one keel petal and half the upper petal (standard) removed ( × 2½). Pollen is shed into the tip of the keel before the flower opens, and growth thereupon ceases in five of the stamens; the other five continue to grow, keeping pace with the expansion of the flower, while the tips of their filaments swell (B) to form a piston. The piston causes extrusion of pollen during insect visits ( × 3).

Other flowers with a basically Papilionate type of mechanism occur in Polygala (Polygalaceae), Hyptis & Coleus (Labiatae) and Collinsia (Scrophu- lariaceae) (Delpino 1871). Whereas the Lotoideae deposit pollen on the under- sides of their pollinators (sternotribic) most Labiatae, in which bee-pollination is also prevalent, deposit pollen on the backs of their visitors (nototribic), and here pollen-protection devices are less well developed. I have seen bees of the, Andrena taking pollen by clawing and biting it from the anthers of Lamiunv album, and Dr. M. C. F. Proctor has photographed Syrphid Diptera sucking 670 P.F. Yeo pollen directly from the anthers of the same ; the pollination mechanism, however, is designed for the brushing of the backs of Bombus while the insect's head is deeply inserted into the flower. In spite of such cases, it does seem possible that Diptera might find pollen robbery easier with sternotribic than with nototribic flowers, so that protective devices have become more common in the former. Another factor could be a difference of opportunity for a mechanism to evolve; in sternotribic flowers the weight of the insect on the lower petals virtually creates a mechanism itself, which can then be refined, whereas stamens placed above the visiting insect are not necessarily displaced by the visitor. Protection is, however, well developed in the nototribic genus Salvia, as in such species as S. pratensis. Here the anthers are tucked away in the compressed, inverted keel-like upper lip of the corolla, and are lowered by a lever mechanism when a bee tries to enter the flower. Perhaps the scarcity of the type of flower exemplified by Salvia pratensis is compensated for by those nototribic flowers in which powdery pollen simply falls from above. The release of the pollen is here effeeted by the bee's forcing open a laterally compres- sed flower, a type well developed in Serophulariaeeae, Tribe Rhinantheae. Here protection is as good as in Lotoideae, while delivery of pollen is gravi- tational (fig. 2).

(B)

FzO. 2. Pedicularis sylvatica. (A) SagittM section of flower ( x 2); (B) View of flower from below, to show the lateral compression of the upper lip (the oblique lower lip is a special feature of Pedicularis flowers) ( × 1~:).

Pollen deposition before the flower opens, as in Lotoideae, occurs in several other families. After its deposition by the anthers, some other organ has to do the job of pollen presentation, hence the expression ' secondary presentation ' (Faegri & Van der Pijl, 1966, p. 17). Secondary presentation is associated with extrusion mechanisms in Compositae (fig. 3), Phyteuma (- Campanuloideae), Campanulaeeae-Lobelioideae, Goodeniaceae, Serophularia- ceae (Pediculari8--Sprague 1962), Fumariaeeae (Cor~/dalis), Polygalaceae (Polygala). It occurs without associated extrusion mechanisms in Campanu- laeeae-Campanuloideae (, Codonopsis, Jasione etc.--figs. 4 and 5) and Proteaceae; in these pollen is deposited near the exposed tip of the style before the stigmas expand and become receptive. The significance of the Miscellaneous notes on pollination and pollinators 671

(A) (B)

FIG. 3. Senecio squalidus. (A) Young floret. The five anthers form a cylindrical tube into which pollen is shed. The growth of the style pushes the pollen out at the top. (B) Older floret. The two arms of the style have emerged from the tube and diverged; the stigmatic surfaces at their tip are now receptive ( x 9).

f' ~ \\\\ // :~ "~

FIG. 4. Campanula rotundifolia. (A) Flower shortly before opening, with the corolla shown in section; anthers dehiscing and depositing pollen on the hairy part of the style. (B) The same, just after opening; the corolla and style have enlarged and the pollen is available for removal by insects; the stamen filaments have scarcely enlarged and the empty anthers remain in the lower part of the bell. (C) Later stage, with pollen removed and the three lobes of the recurved to expose the receptive surface ( x 3~). 672 P.F. Yeo arrangement in such cases does not seem to be clear, but it may differ in the different groups of plants. Carolin (1960) has suggested that in the Order Campanales (sensu Hutchinson) secondary presentation without an extrusion mechanism may have evolved as one mechanism among others for placing pollen and stigma at the same place in the flower at different times. After this arrangement had evolved, selection could have favoured the modification of various structures for the protection of the pollen, and for its extrusion only when deposition on an insect is more or less assured.

FIG. 5. . Flower in natural posture with parts of the and part of the corolla removed. A large blob of nectar surrounds the grooved base of the style, being held in position by the expanded bases of the stamens. Pollen presentation is as in Campanula (fig. 4) ( × 2).

Seed-type versus pollination-type The adaptive features of flowers relate not only to pollination but to pro- tection, seed production and dispersal. Some species produce large numbers of small seeds, and others small numbers of large seeds. The balance between seed-size and seed-number is presumably determined by natural selection and must relate to the habitat and mode of life of the species (an assertion broadly supported by Salisbury 1942). In the Labiatae and Boraginaceae the maximum number of seeds is four per flower. If, therefore, the environment dictates the production of large numbers of small seeds the must produce large Miscellaneous notes on pollination and pollinators 673 numbers of flowers which will generally be small in all parts and not only in their seeds. In these circumstances the pollination type may be influenced by seed type owing to the inflexibility of ovarian structure, for only certain floral types will be possible if the consists of numerous small flowers. However, this interaction will affect the 'Gestalttyp' more than the 'Stil' (Vogel 1954), because a given ' Gestalttyp' may be capable of adaptation to more than one pollinator type: thus the small tubular flowers of Mentha attract a profusion of Diptera, whereas the similarly small flowers of Thymus and of Marrubium vulgare seem to be more attractive to Apis and Bombus. Even so adaptation to some pollinator types will probably be incompatible with some seed types in the Labiatae and Boraginaceae. The occurrence of this type of interaction has also been inferred in the Compositae by Burtt (1961, p. 218). In another family with a fixed small number of seeds per flower, the Ger- aniaceae, dense massing of very small flowers is almost unknown, and here nearly all species appear to be adapted to pollination by bees of various sizes, long-tongued flies and Lepidoptera, and they produce small numbers of large seeds.

Robert Graham and the trapping of flies by Aristolochia Knoll's researches on Arum nigrum Schott (Araceae) and other Arum species (1926) showed that the insects entered the prisons of these involuntarily, being unable to retain a grip on the surface of the spathe and the spadix appendage, each cell of which is produced into a downwardly projecting conical papilla lubricated with an oily secretion. As an insect tightens its claws on one of these papillae they are simply forced off the tip. (For an accessible summaryin English see Dormer (1960)). Exactly the same mechanism in Ceropegia woodii Schlecht. (Asclepiadaceae) was described in the same year by Leopoldine Miiller (1926), and it was also found in Aristolochia lindneri A. Berger (Aristolochiaceae) by Cammerloher (1933). Such a papillose epidermis had been noted many times previously though the fact of its being lubricated was not usually recorded. Thus it was found in Aristolochia grandiflora Swartz by Cammerloher (1923), in Arum maeulatum L. by Church (1908), in Helieodiceros museivorus (L.f.) Engl. (Araceae) by Arcangeli (1890) and in Arisarum proboscideum (L.) Savi (Araceae) by Arcangeli (1891). The function of this papillose epithelium was clearly understood by Arcangeli, while the presence of a greasy secretion of the spadix of Arum italicum Mill. was reported by Church (1908) who, however, believed that this was the form in which the scent was produced. In view of this history of the subject it is interesting to find that such a mechanism was postulated, apparently without its physical basis having been detected, by the Edinburgh botanist Robert Graham (1786--1845) in 1839. In this year there appeared in Curtis's Botanical Magazine VoI. 65 a coloured plate (t. 3640) of Aristolochia saecata Wall. with a text by Graham, in which he infers the existence of " a particular condition of the surface in the upper part of the tube, from secretion or other cause, which prevents adhesion of the feet of the insects, though they are able to walk along it when horizontal " Graham's judicious wording thus exactly covers the facts. 674 P.F. Yeo

Stages of Anthesis in Arum maculatum L. During the period 2-13 May 1966 the inflorescences of this species were frequently inspected in the Cambridge Botanic Garden. It was found that spathes began to open in the morning or the first part of the afternoon. Heating of the spadix in newly opened inflorescences was noted from 16.30 G.M.T. onwards (observations ceased at about 18.15 hours) and was accompanied by a powerful emission of the well-known disagreeable smell. During this period open inflorescenees in which the tip of the spathe was slightly withered contained insects, some of which were seen escaping, while the fresh inflores- cences contained no insects except on one occasion when a few were seen in the chambers and two or three were seen to fall in. In the mornings inflores- eences which had contained insects the previous afternoons were found to be empty, while those that had heated spadices the previous afternoons now had cold spadices and insects in the chamber. Thus, it seemed clear that the pollination activity covered two days, each inflorescence trapping flies in its first stages one afternoon and evening and releasing them in its final stage in the same period on the following day. There were considerable temperature fluctuations during the period of observation, and although the time at which heating of the spadix began was not accurately determined, it appeared that it was not substantially delayed during cold weather. This suggests that opening is not regulated purely by a temperature-controlled growth process. This is in agreement with the results of Schmucker, quoted by Prime (1960, pp. 166-167). The temperature fluctuations under which my observations were made were evidently not as severe as those under which Prime (1960, p. 174) observed interference with the normal timing of floral activity. On 7 May in the morning, which was cold, some infloreseences were still smelling, though no longer heated, and one or two insects were seen to fall into the chamber from the spathe. On the warm afternoon of 13 May at 18.00 hours some insects had been trapped by the spathes of some of the plants with heated spadices in a luxuriant clump in a shady place, but spathes sheltered by Arum where the plants grew most thickly were empty. In two or three cases flies crawled on the spathe, and once on the spadix appendage, without apparent difficulty, but they fell sudenly from the lower third of the spathe. On the same day about 30 insects were released by my breaking open a non-heated inflorescence; although there was an active inflorescence 0.25 m away, at most one insect was attracted to this, the others dispersing. These observations are consistent with those of Knoll (1926), who states that the first stage of flowering takes place in the afternoon. They also agree essentially with those of Prime (1960, pp. 166, 168-169) and of Church (1908) in Oxford, who says that " the inflorescences expand late in the morning, 10-12 noon, or even late in the afternoon ", while " the temperature [of the spadix] rises to a maximum towards evening (5 p.m.) " The vast majority of the insects seen in my observations were Psychodidae, as is usually the case with A. maeulatum and A. italicum.

Presence of window-panes in Aristoloehia clematitis L. The perianth in this well-known European species appears to be a rather uniform yellowish-green eolour. However, if the perianth-tube is cut trans- versely near the top of the prison and the inner surface of the prison is viewed Miscellaneous notes on pollination and pollinators 675 through the cut hole, a definite set of window-panes can be seen round the reproductive organs; they appear almost white instead of yellow-green, they are much more translucent than the rest of the chamber and are separated from one another by weak longitudinal veins. This observation was made in the University Botanic Garden, Cambridge, on 22 July 1965. Although the species is not native to Britain it is capable of attracting insects here, for on the above date various small Diptera and a minute beetle were found when flowers were broken open. Window-panes in fly-trapping flowers are normally set off by a blackish or dark purple surround, rather than green.

The pollinators of certain flowers Calycanthus fertilis (Magnoliaceae) The pollination of Calyeanthus occidentalis Hook. & Arn. (Calycanthaceae) by the beetle Colopterus truncatus (Randall) (family Nitidulidae) in California is described by Grant (1950), who quotes a record of another Nitidulid, Soronia grisea L., from a flower of the same plant in cultivation in Berlin. C. truneatus is brown, about 3 mm long, and has a flat body; it has been collected on various wild and cultivated fruits, while its relatives are known to live under bark and feed on sap (Grant 1950). In the Cambridge Botanic Garden the flowers of Calycanthus at a certain stage regularly contain small, flattened, brown beetles, 3-4 mm in length. Such beetles were noted in a flower of C. fertilis Walt. on 2 June 1966; when the flower was disturbed the beetles came out and fell or flew away. It appeared that the food bodies of this flower had been eaten. Again, on 18 July 1968, 15 beetles were obtained from two flowers of C. occidentalis, and these were passed to Mr. C. E. Tottcnham, of the Cambridge Zoology Museum, who kindly identified them as probably Epuraea unicolor Oliver (the expression of doubt being due to the taxonomic difficulty of the group, which also belongs to the Nitidulidae). Mr. Tottenham tells me that the species of Epuraea are mostly associated with sap, etc., but many are often found on flowers. Epuraea appears adjacent to Soronia in the systematically arranged Check List of British Insects by Kloet & Hincks (1945). Thus Calycanthus in Europe attracts insects exactly comparable with its pollinator in California.

Convergence in Fritillaria and Codonopsis What seems to be a notable case of convergence is seen in the flowers of some Fritillaria species (Liliaceae) and some Codonopsis species (Campanu- laceae). Many species of Fritillaria have a pendent bell-like perianth (formed by six free but connivent segments) coloured green or brown, or patterned with both these colours. The nectaries are shallow pits near the base of each perianth segment. On one or two occasions I have seen at Cambridge queen wasps (Vespula germanica or V. vulgaris) in these flowers taking the nectar; to do this they stand on the perianth segments and touch the stamens and stigmas with their backs. I understand such visits have been seen also in England by Rear-Admiral Paul Furse. Several species of Codonopsis also have pendent green or green and brown bell-shaped flowers, and on 19 July 1963 in the garden of Sir Cedric Morris at Hadleigh, Suffolk, I saw the green and 676 P.F. Yeo

faintly purple-tinged flowers of C. pilosula (Franch.) Nannf. being freely visited by Vespula workers (apparently V. sylvestris (Scop.) and V. rufa (L.)). The nectar is found abundantly in grooves at the base of the bell of these flowers and the wasps take it by standing on the corolla, becoming dusted with pollen on the dorsum of the thorax in the process. The flowers were very inconspicuous to the human eye among the yellowing leaves which the plants bore. Thus these two types of wasp-attracting flower are similar in shape, in colour and in the position of nectary, and they clearly operate in a similar way. The Fritillaria species are found in the Mediterranean Region and West Asia, the Codonopsis species in the Sino-Himalayan Region and East Asia.

Is Fritillaria imperialis bird-pollinated? I can still remember my suprise when, as a student, I first became aware of the existence of the Crown Imperiah It seemed an extraordinary object and I groped in my mind for some significance which its structure might hold, though in vain, for I was not then pollination-oriented. Later I came to take it for granted, and scarcely thought about its pollination until seeing Vogel's comments (1954, p. 94) supporting an earlier suggestion by Porsch that it is bird-pollinated t. The reasons for supposing Fritillaria imperialis L. to be bird-pollinated are its habit, with a stout bare scape below the flowers giving access to them for a perching bird, the large reddish perianth of firm texture, the very large quantity of dilute nectar (8.2 % sugar according to Jaeger ( 1957 )) and, ac cording to Vogel (1954) the projecting androecium and style. It may be added that the distinctive form of the plant, with the whorl of flowers at the top of the bare scape and crowned with green leafy , may also be related to pollin- ation by animals with clear long-distance vision. If this flower is indeed bird-pollinated, then it has one anomalous feature, namely a strong and disagreeable scent, for ornithophilous flowers are usually scentless. The interior of the flower is a remarkable sight: six ahnost colourless trans- lucent nectarial pits near the bases of the perianth segments, each holding a large pendulous drop of nectar and a pattern of well-defined blackish brown veins converging and thickening to form a dark ring round each nectary. These features do indeed suggest that the pollinator is a bird, but field obser- vations are required.

Putative ornithophilous flowers of Macaronesia A bell-like flower of similar size and colour to that of F. imperialis occurs also in Canarina canariensis (L.) Vatke (Campanulaceae). Inside the corolla a strong network of brownish veins coalescing at the base around a central

~Dr. M. C. F. Proctor has kindly drawn my attention to the following, which is part of a note to Canto IV of Erasmus Darwin's The Botanic Garden, Part I, The Economy of Vegatlon (it appears as a note to the line ' Fair Cyprepedia . . . ' numbered 505 in the 2nd edition of 1791 and 535 in the 1825 edition): " A bird of our own country called a willow-wren (Motaeilla) runs up the stem of the crown- imperial (Frittillaria coronalis) [sic] and sips the pendulous drops within its petals, This species of Motacilla is called by Ray Regulus non cristatus. White's Hist. of Selborne ". The scientific name of the Willow Wren (or Willow Warbler) is Phylloscopus trochilus (L.). Miscellaneous notes on pollination and pollinators 677 pale area, and a great blob of nectar, held in position by the bases of six stamen- filaments, strongly recall the Crown Imperial flower (fig. 5). This species differs from the latter, however, in being scentless, and in being more or less flagelliflorous, with the flowers solitary on the ends of pendent leafy shoots. Like the Crown Imperial, Canarina eanariensis is considered by Vogel (1954, p. 302) to be ornithophilous. Its adaptive convergence upon a species of Fritillaria is interesting in view of the convergence of Codonopsis and other species of Fritillaria in their adaptations to wasp-pollination (Section on Fritilla.;'ia imperialis). Another plant with a flower similar in colour, though not in form, to the two already mentioned, is Isoplexis eanariensis (L.) Loud. This is closely related to, and similar to, Digitalis but the lower lip of the corolla is reduced and recurved; the corolla (in the stock grown at Cambridge,) is a similar shade of dull orange to that of Canarina eanariensis, and the style and stamen filaments are dark brown and appear to provide guide-marks (fig.6). A fairly large drop of nectar can be seen by looking into the mouth of the corolla. These features suggest that the flower is ornithophilous.

(A) (B) FIG. 6. Isoplexis eanariensis. (A) Side view of flower. (B) Face view of flower; two anthers are dehisced and shrunken, while the other two are still undehisccd. The stout style and stamen-filaments are blackish maroon in colour and the corolla light orange ( × 2).

In addition to these two Canary Island plants the genus Musschia (Caml panulaceae), endemic to Madeira, also appears to be ornithophilous (Voge- l954, p. 328), yet there seem to be no reports of birds visiting their flowers. The only records of birds taking nectar in these islands refer to Blackcaps (Sylvia atricapilla (L.)) visiting entomophilous or exotic ornithophilous flowers. The Blackcap is essentially an insectivorous bird, but is well known to take nectar occasionally, especially in the Mediterranean Region (Porsch 1924).

Oncoeyclus irises In addition to the insect-trapping flowers which lure flies and beetles by scents which probably resemble those of their egg-laying substrates, and then imprison them for a period, there are other flowers which lure such insects by similar means, possibly with an added emphasis on visual attraction, but do not imprison them. Most notable among these are the Stapeliads (Ascle- piadaceae), but a number of orchid genera have the same system, e.g. Bulbo- phyllum (Ridley 1890) and Masdevallia (Dodson 1962).

~This corresponds with I. isabelliana (Webb) MasL, a variant which apparently does not deserve separation as a species from I. canarie~sis. 678 P.F. Yeo

Frequently such plants do not appear to provide food for the insects they attract. All these plants exhibit the ' Myophil style' of pollination (Vogel 1954) and one of the characters of this ' style ' is the possession of vibratile organs, which is most marked in Ceropegia and Bulbophyllum. These are considered to provide stimuli acting on the insects' ready perception of move- ment (Vogel 1961). In subsect. Oncocyclus (Siemss.) Benth. we find species with various of the visual characters of myophil flowers. Thus Baker is dull yellow with red-brown spots over most of the area of the perianth, but the entrance to each flower-tube is marked by an intense blood-red spot. Various species show dark purplish colouring on the falls intensifying to almost black at the entrance to the flower tubes, and in these flowers long coarse bristles are often present ( Hoffm., I. susiana L., I. bismarekiana Dammann). Such colours and textures are frequent in the perianths of Stapeliads, the perianth limbs of Aristolochia species, the spathes and spadices of some Aroids, and indeed in the perianths of some fly-pollinated members of the iridaceous genus Tigridia (Molseed 1970), and they strongly suggest that some of these irises are myophilous. In this connection a possibly significant observation was made on a cultivated plant of L. in March 1967. In this plant the falls are greyish white with dark purplish brown striations; the entry to the flower-tube (formed by the haft of the fall and the style) is very dark. with long hairs in the opening and a dark velvety patch just in front of it. The large, erect standards, paler in colour than the falls, were observed to waggle vigorously with very slight movements of the pot containing the plant. This suggests that the standards may act as vibratile organs (normally res- ponding to air movements) with a similar function to the vibratile organs of other myophil flowers. (The scent of I. susiana is plummy, similar to, but weaker than, that of Muscari neglectum Guss.) Another Oncoeyclus Iris, I. paradoxa Baker, has small dark velvety falls, sometimes with lighter transverse barring, which even suggests the possibility that it might be pollinated by pseudocopulation. There can be little doubt that there are interesting discoveries in polli- nation biology to be made in the semi-arid Middle Eastern areas where these plants occur, comparable to what has already been found in Australia, southern Africa, North Africa and western North America.

Insect behaviour Comparisons between predation and pollination Individual flower-constancy and specificity of pollinating insects are well- known in the interaction between plants and insects in pollination. The advantages to a pollinator are summarized by Levin (1971) as follows " Floral constancy permits it to minimize search time and energy expenditure per unit food gathered. Flower specificity permits it to reduce interspecific competition for pollen ". Levin gives the advantages for the plant as an increase in relia- bility of pollination, reducing gametic wastage which might limit seed-set, and a decrease in the incidence of hybridization. He also quotes references sup- porting the conclusion that both flower-constancy and pollinator-specificity are most pronounced in areas of high food-plant density, and that they decrease Miscellaneous notes on pollination and pollinators 679 as densiby declines. He continues " At low plant density, a pollinator is apt to feed on any suitable plant. In this regard, its foraging behaviour is similar to the predatory behaviour of some vertebrates " (see Levin 1971, p. 99, for references). It seems worth looking into aspects of this comparison. In order to explain the foraging behaviour observed in a predatory animal (the Great Tit, Paras major) Tinbergen (1960) postulated that ' specific search- ing images ' are set up for common species but not for rare ones. It was found that uncommon prey were taken less frequently than would be expected from their frequency in the feeding area, whereas common ones were taken more frequently than expected. In other words the predators were showing a degree of prey-constancy related to the density of the prey. The selective effect of the existence of specific searching images has been termed apostatic by Clarke (1962, 1969), since it favours polymorphism in the prey by improving the survival of uncommon morphs arising in the popu- lation. As the advantage of such divergent phenotypes varies inversely with their frequency, polymorphism is maintained. Clarke suggests that apostatic polymorphisms will be most likely to arise in species which are not excessively rare, nor excessively common, and are eaten only occasionally (but then possibly in considerable numbers) by their major predators. A mode of life not favourable to the development of effective crypsis may also help. Clarke states that there is an enormous number of non-mimetic polymorphisms in the animal kingdom. His own study of polymorphism in the snail Cepaea nemoralis suggested that this was a case of apostatic polymorphism. Clarke further suggests that apostatic selection could favour divergence between two species which share the same predator. Initial divergence will be enhanced, under appropriate conditions, so that the same specific searching image will not do for both species of prey. Tinbergen (1960) found that extremely common prey, unlike moderately common ones, were taken less often than expected. He attributed this to a preference for a mixed diet on the part of the predators. Clarke points out that when two such species occur together, they benefit from the predator's preference for a mixed diet if they come to resemble each other. Allen and Clarke (1968) carried out an experiment on Turdus merula, the Blackbird, by putting out edible pellets identical except in colour, which was either brown or green. With nine green to one brown pellet and 14 visits to the area by birds, green pellets only were taken on 12 visits and brown only on two; both colours were not taken on any visit. The experiment shows an extreme readiness to develop ' constancy ', for there was no advantage in being constant from the point of view of handling the food (locomotor facili- tation), but only from the point of view of searching and finding (optic-mental facilitation). Even the latter is, no doubt, highly significant from the point of view of the food-gatherer. It is certainly something experienced by the field naturalist in his search for ' prey '. Although some of the prey species involved in the above-described situations may be cryptically coIoured, the selective forces described are ones which come into effect after the predator has recognized a potential prey-object. It is for this reason that these animals show parallels with aposematic mimicry, where the effectiveness of mimicry in palatable species, whether monomorphic or polymorphic, likewise varies inversely with the density of the mimic. 680 P.F. Yeo

Since many pollinating insects develop flower-constancy it would seem that the concept of the specific searching image can be applied here too. However, as the pollinators are benefactors of the plants, the results in terms of variation will differ. Polymorphism within species will be discouraged, but divergence between species will be promoted, as in the insect prey of birds, though for different reasons. Plants that characteristically occur with low density will be at a disadvantage as they may fail to induce a specific searching image in potential pollinators. The result may be convergence by a low-density form on a high-density form, for the rare plant may solve its problem by mimicking a common one with which it grows. It has been suggested that this may account for the resemblance between Euphrasia micrantha and Calluna vulgaris (Yeo 1968); this would be a case of Batesian mimicry with Calluna as a model. A similar mimicry of two different plants by related species of Erysimum is reported from North America (Macior 1971). A Muellerian mimicry has been suggested to account for the red colouring of hummingbird-pollinated flowers in North America (Grant 1966, Grant & Grant 1968), and for disc-like yellow and stellate white flowers in Europe (Proctor, in Proctor and ¥eo, in the press, p. 375). Probably the circumstances of these cases are such that a high degree of or individual constancy cannot be achieved, and it then pollinator-specificity becomes more important to attract the right general type of pollinator than to attract one that has just visited another flower of the same species. The latter condition would tend to be assured anyway if the density of the plant is high. In both the bird-pollinated flowers considered by the Grants, and the insect- pollinated ones mentioned by Proctor, it is common to find several species occuring together at high density, and this may be a factor making the estab- lishment of constancy difficult. In addition, the insect-pollinated flowers concerned are species adapted for unspecialized visitors in which flower- constant behaviour is not very rigid. A complication with insect-pollinated flowers is that there is a long-range response and a close-range response. The long-range is usually to colour alone, while at close range shape, colour-patterns and scent are perceived. Hummingbirds might behave similarly in respect of visual stimuli perceptible at long and short range, respectively, but a mimetic convergence need not necessarily involve the attributes of both long-range and short-range significance. Plants with a high degree of pollinator-specificity are mostly trap-flowers and orchids (notably pseudocopulatory species). They mimic breeding substrata or mating partners, by producing appropriate sign-stimuli, and in theory could get themselves into trouble by being too abundant and interfering too much with the reproductive processes of their pollinators, in the same way that Batesian mimics lose their advantage if they become too abundant. It seems rather unlikely that this would happen, except very locally, whereas there is evidence for it among mimetic butterflies, some having become mimetically polymorphic on more than one distasteful model species (Wickler 1968, pp. 22-33).

Recognition of flowers just visited It is reported by Van der Pijl (1954, 1960) that bees of the genus Xylocopa leave odour signals in flowers, and that " Bombus also shows signs of using this mechanism, often refusing many individual flowers ". Such apparent Miscellaneous notes on pollination and pollinators 683 selection of individual flowers can often be seen but a particularly clear case was recorded on 31 May 1967 in a greenhouse at Cambridge Botanic Garden. The greenhouse doors were open and a worker Bombus agrorum, which had not been present a few moments previously, was noticed on a group of potted plants of Geranium palmatum Cav. (G. anemonifolium L'H@it). Each of these plants produces from the basal rosette a small number of stout divergent flowering branches, which are cymosely branched and bear large pink flowers about 3 cm in diameter; nectar is concealed in the calyx and is reached by five narrow slits between the petal bases. The bee worked fairly systematically over the branches, so that it was easy for me to know which flowers it had visited. When the bee reached the extremity of a branch it flew up slightly and then went to flowers that it had visited before, approaching the centre of each but never really alighting; this continued until it reached a flower it had not visited before, when it alighted and again took nectar. It seemed perfectly clear that the bee could tell, during these close approaches, which flowers it had visited before. By the procedure described it moved from one area to another of the primary branches, and from one primary branch to another, so visiting all the flowers on two interlacing plants; it then very rapidly tested again almost every flower on these two plants, swept away from them and then returned to another group of the same species of plant about 3 m away from the first, and started to work these in a similar way.

Response to a visual food signal by Vespula That Vespula requires nectar for the feeding of its brood was established by Brian & Brian (3952); it is a persistent visitor to certain flowers which seem to be specially adapted to it and demonstrate a definite pollination syndrome which includes greenish and brownish flower-colourings. The significance of this is not known, nor is the relative importance of vision and scent in the finding and recognition of flowers by Vespula. However, wasps feed a great deal on ripe fruit and on jam, and their readiness to enter houses when fruit is being stewed or jam made suggests that scent plays a large part in directing their foraging activities, and this is supported by their swinging approach flight which is typical of a scent-directed flight (Knoll 3922), though in the case of Vespula and many other wasps it may also serve for predator-avoidance. The following observations are of interest in showing an apparent visual approach to food. On 2 September 1967 I was one of three people who took tea together in the garden of a hotel in Norfolk; the tables had white-painted metal gauze tops, and only ours was occupied. As soon as plates were brought Vespula spp. crowded round, crawled on plates and cups and touched buttered scones. The jam was brought, I believe, just afterwards, but thinking this was attracting the wasFs, I placed it on the lawn 30 m from the table and placed a paper napkin over it which, of course, was not an airtight covering. Jam was obtained by taking the scones to the pot. No was p was seen near the jam the whole time we were in the garden, but the wasps continued their activities at the table for a short while until I lashed out at them, after which they only occasionally appeared. None seemed to obtain food until the end of the meal when they ate jam from the used knife-blades. Thus it seemed very evident that it was the visual stimulus of the persons sitting round the table and the plates, etc., being laid that attracted the wasps, and not any 682 P.F. Yeo smell from the jam, though this, it turned out, was the only food available that they were actually interested in. No doubt the wasps had acquired con- ditioning to this visual stimulus during the preceding weeks, apparently having found the visual signal a satisfactory guide to food and so abandoned olfactory searching in this context.

The purple flower in the umbel of Daucus A curious feature of the umbels of some plants of Daucus carota L. (Umbel- liferae) is a single blackish purple floret at the centre. When collecting insects I have sometimes, on seeing one of these umbels out of the corner of my eye, momentarily supposed that it was occupied by an insect. Detto (1905) has suggested that the significance of the dark flower lies in the impression it gives of the presence of an insect. His theory was that it might discourage grazing animals fi'om damaging the umbels. He found that honey-bees (Apis mellifera) and bumblebees (Bombus spp.) usually turn away from flowers already occupied by insects or foreign bodies, and so made the alternative suggestion that it keeps these insects away. Brian (1957), working with bumblebees, found that a bee on one of a group of artificial flowers attracted passing bees which usually alighted on the same flower. If, however, several flowers were occupied the attracted passers-by usually alighted on an unoccupied flower of the group. (Perhaps one bee indicates a good flower, several indicate a good crop.) Thus at least under some circumstances, the presence of one insect can attract others, and although Apis, and Bombus may not be primary pollinators of Daucus, Apis at least, is a highly effective pollinator of the carrot (Bohart & Nye 1960), and Bombus might be expected to cause some pollination, so there would not be much advantage in keeping it away. The other most effective pollinators of the carrot (in Utah) are certain Diptera and short-tongued Hymenoptera (Bohart & Nye 1960) and it is the behaviour of these types of insect that needs to be studied in this connection. Perhaps these too are induced to alight by a dark spot signifying an insect already present.

Damage to flowers by non-pollinators Avian nectar-robbery in the British Isles Nectar-robbery from Gooseberry (Ribes uva crispa L.) and American Currant (R. sanguineum Pursh) by Blue Tits (Parus caeruleus L., Paridae) is recorded in Ireland by Swynnerton (1916). The birds pecked holes in the sides of the receptacle-tubes of the flowers, apparently to obtain the nectar. Great numbers of holes were pecked and many of the visits of the birds to the flowers involved probing those already punctured. In 1963 I saw blossoms of Prunus avium L. (t~osaeeae) and other Prunus species showing damage which I suspected was caused by Tits (Parus spp.) which I had casually noticed feeding in the trees in the University Botanic Garden, Cambridge. The following year, on 13 April, in a Cambridge suburban street, I actually saw a Blue Tit (P. caeruleus L.) attacking the blossoms of an Almond Tree (Prunis dulcis (Mill.) D. A. Webb,=P. amygdalus Batsch). The bird was pecking at the receptacles of the flowers, sometimes tearing off part of the flower. On the ground below the tree there were numerous flowers and fragments, each with a hole pecked in the side of the receptacle, which was the same kind of damage as had been seen the previous year. I collected Miscellaneous notes on pollination and pollinators 683 some flowers from the ground and have preserved them in my herbarium. The observations strongly suggest that the bird was feeding on the nectar of the flowers.

Flower-peeking by house sparrows The subject of flower-pecking by Passer domesticus L. (Ploceidae), has been discussed by Summers-Smith (1963, pp. 38-39). He describes it as flower- tearing and suspects that the birds eat the petals and get some nourishment or supply of moisture from them, but that this is to some extent a spare-time activity. The casual nature of the activity is perhaps the reason for the fact that damage is much worse at the back than at the front of my terrace-house in Cambridge, and that new plantings of Crocus ([ridaceae) in the Cambridge Botanic Garden have escaped damge for the first few years, but subsequently have been consistently devastated. The plants listed by Summers-Smith as suffering damage from sparrows are Crocus, Ranunculus ficaria L. (Ranun- culaceae), Primula vulgaris Huds., P.×polyantha Mill. ('primula'), P. 'Wanda' (Primulaceae) and Taraxacum officinale Weber (Compositae). In my garden the first two of these Primulas are attacked, also various Crocuses, Iris reticulata Bieb. (), Galanthus nivalis L. (Amaryllidaceae), Saxi- fraga × apiculata Engler (Saxffragaceae) and Anemone blanda Schott & Kotschy (Ranunculaceae). All these plants are normally attacked in bud, although the perianths of fully open Crocuses are also shredded, and the impression I get is that the birds have eaten the young anthers and stigmas from these buds. As these organs are particularly nutritious they may well be the objects of the attacks. Summers-Smith emphasizes the reported prevailing preference for yellow flowers. This may be subject to local variation, for all kinds of Crocus are eaten indiscriminately in my own garden, while in the Cambridge Botanic Garden there is a border containing a patch of the purple C. tomasinianus Herb., of which no flower is ever allowed by the birds to expand, and a patch of a pale yellow cultivar of C. chrysanthus Herb. twenty yards away, which is scarcely or not at all touched by them.

Camouflaged flowers It is common for floral organs of visual attraction to be more brightly coloured on the inner, adaxial surface than on the outer. This differential pigmentatation is probably, at least in some cases, related to pollination, having the effect of discouraging pollinators from approaching the wrong side of the flower. It may also be of value in preventing insects from trying to enter the flower at the wrong time, such as just before the flower opens, or during the day in a nocturnal flower. Where a whitish cast is present in a coloured flower, as on the backs of the petals of Geranium robertianum L. (Geraniaceae) the function may be to enhance the effect of the pigment when viewed from in front, in the same way that the internal starch layer enhances the effect of the superficial pigment in l:lanunculus (Parkin 1928, 1931, 1935). This function is compatible with the suggested function of directing insects, and both could be operative in the same flower. There are some flowers, however, which are strikingly marked externally in a way that seems to have no possible relationship to pollination. For example, Crocus imperati Ten.

J.N.H. 2Y 684 P.F. Yeo

and its allies (C. minimus DC., C. corsicus Maw) have on the outer surface of the outer perianth segments a pattern of bold blackish violet feathering on a greyish, buff or even nut-brown ground. Such patterning occurs also in the other main subdivision of the genus Crocus (Nudiflori, as opposed to Involu- crati), as in C. laevigatus Bory & Chaub., C. versicolor Ker-Gawl. and forms of C. biflorus Mill. The patterning is reminiscent of the cryptic colouring on the breast of the Bittern (Botaurus stellaris (L.), Ardeidae) and other birds of marshy habitats, and this, combined with the great difference of the external ground colour of the flower from the internal, strongly suggests that it repre- sents cryptic coloration for concealment in a habitat of dead grass in early spring. In most habitats where they occur, crocuses must be about the earliest plants to flower in spring, and as they often grow in great quantity, their blooms could well be a tempting food for grazing animals (reptiles, birds, mammals). Other plants with similar patterning of similarly shaped flowers are Romulea crocea Boiss. & Heldr. (Iridaceae) with brown stripes, another early flowering Mediterranean species, and some Gentiana species (Gentianaceae) particularly some Sino-Himalayan ones, which are blue with greenish longitu- dinal stripes. Whether the environment of these gentians is such that the corollas would need protection from grazing animals I do not know. If the principle of camouflage against grazing mammals is acceptable, it might be extended to crocuses with greyish peppering externally (e.g.C. korolkowii Maw & Regel) and tulips with greenish and brownish exteriors such as Tulipa tarda Stapf, T. primulina Baker and T. polychroma Stapf, (Liliaceae); for these the usual background would have to be more or less open soil. Cryptic coloration of plants against grazing mammals perhaps reaches its peak in the well-known xerophytic Lithops (Aizoaceae), or 'flowering stones' of southern Africa, in which the two fleshy leaves at ground level, which constitute the aerial vegetative parts of the plant, are apparently coloured to look like stones, each species having a more or less characteristic pattern and colour, usually related to the colouring of its particular habitat. Schwantes (1957, pp. 368, 369) reports that the theory of mimicry for these plants has been very strongly condemned by a whole range of authors, one of the arguments being that animals find and eat large quantities of these plants. However, one has only to consider what would happen when a hypothetical species of grass-green Lithops produced mutants with some degree of cryptic colouring. Obviously the green individuals would be eaten first and the camou- flaged ones would be expected to have more chance of leaving progeny. The process, once started, would soon lead to such perfection of concealment as we see today. Whether one calls this coloration adaptive or not, there is no reason to doubt that its presence is related to the presence of grazing animals in the habitats of Lithops, and that it is a result of the action of natural selection. A system which works well enough for a time may disappear simply because an improved system has come on the scene. An instance of the same kind of argument as that used against the theory of cryptic coloration in Lithops is quoted by Prime (1960, p. 175-176). Schmucker cut off various parts of the inflorescence of Arum maculo2um L. beforepolli- nation, and observed the seed-set. The average number of berries per fruiting plant was reduced from 15 to 5 by the removal of spathe, spadix and Miscellaneous notes on pollination and pollinators 685

sterile bristle-like flowers, but only to 10 by the removal of both spathe and spadix, and to 14 by the removal of the spadix only. Schumucker is said to have concluded that the whole apparatus is not of very great value to the plant. Prime criticized this on the ground that the experiment was done in an area where the plant was abundant, so that many of the pollinating insects carrying pollen would have been available. It may also be criticized on the ground that it ignores the consequences of even a slight differential fertility.

Acknowledgments [ am grateful to Dr. M. C. F. Proctor and Messrs. William Collins for permission to reproduce figs. 1-4, to Dr Proctor for reading the whole manu- script and Professor Bryan C. Clarke for reading 'Comparisons between predation and pollination' and to the Rev. C. E. Tottenham for identifying the insects mentioned in ' Calycanthus fertilis (Magnoliaceae) '

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