Pollination of the southwestern Opuntias

This paper presents an overview of pollination systems inOpuntia sens. lat. in the southwestern United States. The floral syndrome of large, colorful, bowl-shaped, diurnal flowers is present in all of the prickly-pear species and most of the cholla (Cylindropuntia) species in this area. Pollination by medium-sized and large bees is established for some of the species with this floral syndrome and is predicted for the others. The same floral syndrome is widespread inOpuntia in other geographical areas.—Deviations from this floral syndrome occur in certain species of southwestern chollas, one of which has nocturnal disc-shaped flowers, and in several tropical American species groups or segregate genera with red hummingbird flowers. But such cases are relatively infrequent. Divergence between species with respect to floral syndrome and pollination system is not a common feature in the evolutionary pattern ofOpuntia. Pollination of North American Cacti, IV.—Previons parts of this series:Grant & Grant 1979a,Grant & al. 1979,Grant & Grant 1979b.     

From pollination byLepidoptera to selfing: The case ofDianthus glacialis (Caryophyllaceae)

Pollination of the alpine herbDianthus glacialis was studied in a population in the Swiss Alps in 1991 and 1992. Only one insect species,Zygaena exulans (Lepidoptera), was observed to visit the flowers ofD. glacialis. Pollen loads onZ. exulans indicate that it is an effective pollinator ofD. glacialis. In 1991,Z. exulans frequently visited flowers ofD. glacialis. However, in 1992 almost no visits could be observed. Despite the occurrence of pollinators and the conspicuous flowers ofD. glacialis, there are strong indications that this plant is mainly selfing: (1) anthesis of individual flowers is short (c. one and a half days), (2) protandry, although pronounced in otherDianthus spp., is absent, (3) nectar production is low, (4) odour production is weak, (5) seed production by spontaneous selfing is high, (6) seed set in emasculated flowers is extremely low and (7) the seed/ovule ratio is distinctly higher inD. glacialis than in outcrossing plants.—Selfing inD. glacialis could have evolved under a shortage of pollinators during the glaciation periods. Present levels of cross-pollination byZ. exulans have apparently not been sufficient to reverse the pollination mechanism ofD. glacialis from selfing to outcrossing.     

Pollination ofOpunta basilaris andO. littoralis

The flowers ofOpuntia basilaris andO. littoralis in southern California are visited commonly by beetles(Carpophilus, Trichochrous) and bees (especially anthophorids, megachilids, and halictids), but are pollinated mainly by the bees. This agrees with observations presented in the previous papers in this series for other cactus species in Arizona and Texas. The available evidence indicates that the large, diurnal, cup-shaped flowers in cacti of the American Southwest are primarily bee-pollinated. Our earlier view that theseOpuntia flowers are also pollinated to a significant extent bynitidulid andmelyrid beetles must be modified now in the light of further evidence. Some pollination probably is carried out by small beetles, but it probably represents only a small proportion of the total pollination.Pollination of North American Cacti, III.—See alsoGrant & Grant (1979) andGrant & al. (1979).     

Bat pollination ofEncholirium glaziovii,a terrestrial bromeliad

The many-flowered, brush-like spikes ofEncholirium glaziovii, a ground-dwelling pitcairnioid bromeliad of the campo rupestre formation of southeastern Brazil, was observed being pollinated by the glossophagine bat,Lonchophylla bokermanni, in the Serra do Cipó (Minas Gerais). Nectar feeding was while hovering, and the pollen was preferentially transferred by the bat's snout. The floral pattern is chiropterophilous; unlike known tillandsioid bat flowers, stamens and style are protrusive beyond a small, persistent perigon, and anthesis, apparently protogynous, extends over several nights, with gradual onset and cease. Although various other flower-visitingChiroptera are known to occur in the area and are not mechanically precluded from exploitingEncholirium glaziovii, no one seems to compete withLonchophylla bokermanni. This species, a trap-liner, habitually forages in open habitats, a possible reason for its exclusiveness.—Flower details of two other species ofEncholirium from the same locality including one with the bat pollination syndrome, are given.     

Breeding systems and pollination inVigna minima (Leguminosae,Papilionoideae)

Four types of floral breeding systems—(i) chasmogamy, (ii) aerial pseudocleistogamy, (iii) subterranean pseudocleistogamy and (iv) obligate subterranean true cleistogamy—are observed in the populations ofVigna minima inhabiting the Western Ghats (India). Five categories of phenotypes are recognized based on the number and kinds of floral breeding systems found in a given individual. The frequencies of different categories of phenotypes not only show intra- and interpopulation variation, but also fluctuate from generation to generation suggesting differences in the genetic structure of populations. This polymorphism in the breeding system of a single species is unique and may be adaptive. Obligate subterranean true cleistogamy and amphicarpy appear to be adaptations to jungle fires and soil erosion.—The flowers are of the flag-blossom type and insect visitors act as tripping agents. The tripping mechanism together with the polymorphic floral breeding system result in a balanced mixture of selfing and outcrossing. Such a recombination system may enhance the fitness ofV. minima which is essentially a colonizing species.     

Pollination ofOpuntia lindheimeri and related species

The large, yellow, bowl-shaped flowers ofOpuntia lindheimeri, O. discata, O. phaeacantha major, andO. compressa in Texas are visited by various species of beetles and bees. The beetles and small bees (Perdita, Dialictus) are pollen thieves. The pollinators are the medium-sized and larger bees (Melissodes, Diadasia, Lithurge, Megachile, Agapostemon, etc.). Different species of theOpuntia lindheimeri group have the same pollination system and there is no evidence of any floral isolation between them. The pollination system of these species ofOpuntia in Texas is essentially the same as that ofEchinocereus fasciculatus andFerocactus wislizeni in Arizona.Pollination of North American Cacti, II.—SeeGrant & Grant (1979).     

The reproductive biology ofJaborosa integrifolia (Solanaceae): Why its fruits are so rare?

Jaborosa integrifolia exhibits stigma-height polymorphism. There are individuals with flowers where anthers and stigma are at the same height but the rule is variable herkogamy, the most common type (75%) being that with an exerted stigma. Self- and cross-tubes did not differ in their capability to reach the ovary (t = –0.67,P < 0.53); they had a high growth rate (6.95 ± 2.28 mm h^–1). There is not autogamy but mostly self-incompatibility. Fruits from controlled cross-pollination showed the highest seed set and seed viability. The nectar sugar is characterized by a similar amount of glucose and fructose, and by the absence of sucrose. Although nectar secretion was continuous throughout the life of the flower, most nectar was secreted during the first 24 h after flower opening. Nectar production costs appear to be lower than in other species since nectar secretion is neither inhibited after a removal (i.e. a pollinator visit) nor reabsorbed as the flower ages. Sphingids visit the flowers mainly after midnight. They insert their proboscis down to the base of the corolla tube to reach the nectar. The upper limit to fruit production is set by pollinator visits. Fruits produced from open-pollinated flowers are often predated by numerous larvae (mainly lepidopteran ones). Considering that this species is mostly self-incompatible and pollination is limited, that each plant displays only a low number of flowers throughout the flowering season, and that there is a high rate of fruit predation, it is not surprising that fruits ofJ. integrifolia are so rare.     

Notes on the pollination mechanisms ofMoraea inclinata andM. brevistyla (Iridaceae)

Individual flowers ofMoraea inclinata are nectariferous and last about six hours. They appear to be pollinated largely by bees in the familyHalictidae (Lasioglossum spp.,Nomia spp.,Zonalictus) and to a lesser extent by bees in the familyAnthophoridae (Amegilla). The mechanism of bee-pollination inM. inclinata is the Iris type; i.e., each flower consists of three pollination units (an outer tepal, a partly exserted anther, and the opposed style branch which terminates in a pair of petal-like crests). Bees rarely visit more than one pollination unit per flower. Transferral of pollen to the bee is passive and nototribic although all bees collected on the flowers were female and 55% of the bees carried pollen loads with 2–5 pollen taxa in their scopae.Moraea brevistyla flowers are nectariferous but lack scent and last two days. They are visited infrequently by bees and only one femaleLasioglossum spec. carried the pollen ofM. brevistyla. Unlike flowers ofM. inclinata those ofM. brevistyla deposit pollen only on the head and thorax. Bee-mediated autogamy in both species is avoided due to the erratic foraging patterns of the bees and the flexibility of each stigma lobe as the bee backs out of the flower. Approximately 2–4 flowers in the inflorescences of both species (6–8 flowers/infloresence) develop into capsules.     

Pollination by passerine birds: why are the nectars so dilute?

Bird-pollinated flowers are known to secrete relatively dilute nectars (with concentrations averaging 20–25% w/w). Many southern African plants that are pollinated by passerine birds produce nectars with little or no sucrose. Moreover, these hexose nectars are extremely dilute (10–15%). This suggests a link between sugar composition and nectar concentration. Nectar originates from sucrose-rich phloem sap, and the proportion of monosaccharides depends on the presence and activity of invertase in the nectary. Hydrolysis of sucrose increases nectar osmolality and the resulting water influx can potentially convert a 30% sucrose nectar into a 20% hexose nectar, with a 1.56 times increase in volume. Hydrolysis may also increase the gradient for sucrose transport and thus the rate of sugar secretion. When sucrose content and refractometer data were compared, some significant correlations were seen, but the occurrence of sucrose-rich or hexose-rich nectars can also be explained on phylogenetic grounds (e.g. Erythrina and Protea). Hexose nectars may be abundant enough to drip from open flowers, but evaporation leads to much variability in nectar concentration and increases the choices available to pollinators.     

Ornithophilie auf den Canarischen Inseln

(1) On the Canary Islands and Madeira typical bird-flowers occur in at least twelve species of six genera, although true flower-birds are absent. This inconsistency is in part elucidated by field observations on exotic and wild plants of Tenerife. —(2) In the Botanical Garden of Orotava it could be observed that various ornithophilous plants, which were introduced there, were visited by indigenous birds for nectar and in one case (Orthostemon) for food tissue. Of the three bird species involved, an endemic race of Chiffchaff (Phylloscopus collybita) and resident Blackcaps (Sylvia atricapilla) exploit, and pollinate, flowers legitimously, while the Wild Canary (Serinus canaria) is predominantly a destructive nectar robber. —(3) The insular Chiffchaff also proved to be a regular pollinator in the wild, at least ofCanarina canariensis andIsoplexis canariensis, two ornithophilous paleoendemics. Ornithophily, thus, is naturally practised on the island, though by birds basically insectivorous. —(4) A list of Macaronesian plants bearing the more or less complete ornithophilous syndrome is presented, including newly recognizedTeucrium heterophyllum andScrophularia calliantha. —(5) On biogeographical and faunistic grounds it is presumed that the modern visitors of Canarian bird flowers are secondary rather than the original partners of the continental tertiary flora in which these plants originated. Palearctic immigrants, when becoming resident on the islands during and since the Pleistocene, adopted facultative nectar feeding, entering an orphaned food niche. Casual flower visits in Europe suggest a certain predisposition of the Chiffchaff and the Blackcap for the exploitation of flowers. — (6) The ability of unspecialized birds to acquire nectardrinking spontaneously and to pass this habit on to their offspring, is demonstrated by a population of Tree Sparrows (Passer montanus) which have visited ornithophilousKniphofia (Liliaceae) in Berlin for several years.

     

Floral scent and intrafloral scent differentiation inMoneses andPyrola (Pyrolaceae)

Floral scent was collected by headspace methods from intact flowers, petals, and stamens of four species ofPyrolaceae. The scent samples were analyzed by coupled gas chromatography-mass spectrometry (GC-MS). The floral scent inPyrola spp. is differentiated into a characteristic petal scent—phenyl propanoids and a characteristic stamen scent—methoxy benzenes. InMoneses the scent is characterized by isoprenoids and benzenoids, with a larger proportion of benzenoids in the stamens compared to the petals. Specific anther scents may promote foraging efficiency in buzz-pollinated species and enhance flower fidelity. Variation in floral scent composition is consistent with the taxonomic relationships among the genera and species examined.     

Notes onDiphucephala affinis (Coleoptera:Scarabaeidae) associated with flowers ofHibbertia andAcacia in Western Australia

Notes are provided on the association of the beetleDiphucephala affinis (Scarabaeidae) with yellow flowers ofHibbertia hypericoides, H. huegelii (Dilleniaceae),Acacia pulchella, andA. stenoptera (Mimosaceae). Observations were undertaken during September 9–19, 1979 at S. Perth, Western Australia. They indicated thatD. affinis is not a pollinator ofHibbertia as suggested in the literature, but may play a small role in the pollination of someAcacia species.     

Competition between the oligolectic beePtilothrix plumata (Anthophoridae) and the flower closing beetlePristimerus calcaratus (Curculionidae) for floral resources ofPavonia cancellata (Malvaceae)

The flowers ofPavonia cancellata, a creeping ruderal half-shrub of northeastern Brazil, open synchronously at 6:00 h with all anthers already dehisced. The oligolectic beePtilothrix plumata was the most effective pollinator. During 90—180 min, female bees make up to 40 brief pollen collection trips to provision their brood cells. The pollen of about 40 flowers ofP. cancellata is needed to feed one bee larva. The most frequent flower visitors, however, are the specialized curculionid beetlesPristimerus calcaratus, which do not crosspollinate the flowers. They perforate the epidermis with their mouthparts, provoking dehydration, and then actively close the loose petals with their legs. Two hours after opening, half of the flowers had already been closed by the beetles. We interpret the fast, uninterrupted pollen foraging ofPtilothrix plumata bees as a strategy adapted to synchronous pollen presentation ofPavonia and to competition withPristimerus calcaratus: the female bees have to provision their brood cells before the beetles succeed in closing the flowers.     

Molecular phylogeny ofForsythia (Oleaceae) based on chloroplast DNA variation

Phylogenetic relationships of ten wild species and several cultivars ofForsythia were reconstructed based on the chloroplast (cp) DNA variation. A total of 216 cpDNA variants, 44 of which were potentially phylogenetically informative, was detected using 24 restriction endonucleases. Phylogenetic analysis usingFontanesia andAbeliophyllum as outgroups revealed four well defined species groups in the genus: 1)F. suspensa, 2)F. europaea — F. giraldiana, 3)F. ovata — F. japonica — F. viridissima, and 4)F. koreana — F. manshurica — F. saxatilis. The amount of support for each monophyletic group was evaluated by various methods including character number, decay analysis, parsimony bootstrapping, Neighbour-Joining (NJ) — bootstrapping, NJ-jackknifing, and the topology-dependent permutation tail probability (T-PTP) test. The data do not support the hybrid origin ofF. intermedia fromF. suspensa andF. viridissima. The disjunctly distributed European species,F. europaea, was identified as a sister species of the ChineseF. giraldiana and it was probably derived through recent long distance dispersal.     

Taxonomic status of the species of the green algal genusNeochloris

Komárek has recently reviewed the various species assigned to the green algal genusNeochloris Starr (Chlorococcales, Chlorococcaceae) and removed those with uninucleate vegetative cells to a new genus,Ettlia. Watanabe & Floyd, unaware ofKomárek's work, also reviewed the species ofNeochloris and distributed them among three genera—Neochloris, Chlorococcopsis gen. nov., andParietochloris gen. nov.—on the basis of details of the covering of the zoospore and the arrangement of the basal bodies of the flagellar apparatus. This paper reconciles these two treatments and makes additional recommendations at the ranks of genus, family, order, and class.     

Stamen movements in flowers ofOpuntia (Cactaceae) favour oligolectic pollinators

Opuntia brunneogemmia andO. viridirubra occur sympatrically in the Serra do Sudeste, Rio Grande do Sul, Brazil. Their flowers have 450–600 thigmonastic stamens and provide large amounts of pollen and nectar for bees. Bees of 41 species were registered at the flowers ofO. brunneogemmia and 30 at the flowers ofO. viridirubra. Females of three oligolectic species are the only effective pollinators:Ptilothrix fructifera (Anthophoridae),Lithurgus rufiventris (Megachilidae), andCephalocolletes rugata (Colletidae). During their visits inOpuntia-flowers, bees touch the filaments and stimulate the movement of the stamens to the centre of the flower. At the end of this movement, the anthers are densely packed around the style. As a consequence the pollen is presented in an easily accessible upper layer of anthers and various, nearly inaccessible lower layers. The lower layers contain about 80% of the pollen reward. Only females of the three oligolectic pollinators exploit the pollen from the lower layers and reach the nectar furrow. Therefore, through their stamen movements,Opuntia flowers hide most of their pollen from flower visitors but favour effectively pollinating, oligolectic bees.     

Honeyeater (Meliphagidae) pollination and the floral biology of PolynesianHeliconia (Heliconiaceae)

The primary pollinator of Polynesian heliconias,Heliconia laufao andH. paka, is the Wattled Honeyeater,Foulehaio carunculata. This report is the first documentation of pollination by honeyeaters in the genusHeliconia and the first record ofF. carunculata as a pollinator of a plant species. The Polynesian heliconias bear inflorescences that produce 2–4 hermaphroditic flowers per day for a period of 2–3 months. Each flower secretes abundant nectar (125–184 l) with low sugar concentration (15–18% sucrose-equivalents, weight per weight basis) which is available at anthesis just before dawn. Ninety percent of flower visits occur between anthesis and mid-morning. The honeyeaters perch on inflorescence bracts, and probing of the flower results in pollen deposition on the head and bill from where pollen is transferred between flowers. No statements on compatibility can be made forHeliconia paka; however,Heliconia laufao appears to be self-compatible. Calculations of energetic values of nectar of the Polynesian heliconias and Daily Energy Expenditures ofF. carunculata suggest that populations ofH. laufao andH. paka serve as rich energy resources for their pollinators.     

Pollination biology of annual and perennialLeonotis species (Lamiaceae)

The pollination syndromes ofLeonotis (Pers.)R. Br. are discussed. Ornithophily accounts for most of the nutlets set in perennialLeonotis species but in the annual species [L. nepetifolia (L.)R. Br.] autogamy prevails.Leonotis species are predominantly pollinated by a variety of sunbirds, although bees are also involved. Nectar is sucrose-dominant in perennial species but hexose-dominant in the annual.     

Nectar by day and night:Siphocampylus sulfureus (Lobeliaceae) pollinated by hummingbirds and bats

Most species of the neotropical genusSiphocampylus are believed to be bird-pollinated. The pollination biology ofSiphocampylus sulfureus was studied in a montane region in SE Brazil. This species has features intermediate between ornithophilous and chiropterophilous syndromes: it presents a striking combination of yellowish flowers with strong odour (chiropterophilous features), and diurnal anthesis and sucrose-dominated nectar (ornithophilous features). Major pollinators were hummingbirds by day, and a phyllostomid bat by night.Siphocampylus sulfureus may be viewed as a recent derivate from the presumed ornithophilous stock within sect.Macrosiphon, and thus benefits from the activity of both diurnal and nocturnal vertebrate pollinators.Dedicated to DrIlse Silberbauer-Gottsberger and Prof. DrGerhard Gottsberger for their pioneer contribution to floral biology in Brazil.     

The pollination spectrum in the southwestern American cactus flora

The cacti of the American Southwest, defined as the region from southern California to Texas, are surveyed for types of pollination systems and their frequencies. Four types of pollination systems are known to occur in the southwestern cactus flora: bee, hummingbird, hawkmoth, and bat pollination. Two other modes are suspected but not documented: miscellaneous smallinsect pollination and autogamy.—Bee flowers comprise a wide and nearly continuous series of size classes from very small to very large. The large bee flowers, with perianths 5.5 to 12.5 cm in diameter, form a prominent but arbitrarily delimited subcategory in the bee pollination system. Promiscuous flowers and autogamous flowers, if they occur, are included with the medium-sized and small bee flowers in our present classification, due to lack of information, and will have to be separated out when our knowledge is more complete. The overwhelming majority of species in the southwestern cactus flora are bee flowers. Between 39 and 44% of the species are large bee flowers. Another 50 to 56% of the species are classified as medium-sized and small bee flowers; while some of these may turn out to be promiscuous flowers and autogamous flowers, most of them are undoubtedly bee flowers.—Hummingbird, hawkmoth, and bat pollination are conspicuous but statistically minor components of the pollination spectrum, occurring in only one or a few species (see Table 2). Hummingbird pollination has arisen from bee pollination in the Southwest. The species or species groups with hawkmoth and bat pollination, on the other hand, are basically tropical groups which developed their advanced pollination systems in the tropics.Pollination of North American Cacti, V. See alsoGrant & Grant (1979a),Grant & al. (1979),Grant & Grant (1979b),Grant &Hurd (1979).