Anthophilous Insects Research Articles

Reproductive biology of the Red List speciesPolemonium caeruleum(Polemoniaceae)

The majority of flowering plants, including many rare and threatened species, are pollinated by animals, but little is known of pollination and breeding systems of many endangered species. Polemonium caeruleum (Polemoniaceae) is a red-listed species and is regarded as dichogamous, self-compatible and bee pollinated. However, some studies show that it is visited by a vast assemblage of anthophilous insects from many taxonomic orders and that breeding systems vary greatly between closely related taxa of this genus. Over a period of 3 years we investigated breeding system, dichogamy, nectar secretion and composition, insect visitations and pollen loads in flowers of P. caeruleum in north-eastern Poland to determine whether the reproductive biology of the plant explains its rarity. Contrary to published data, our study plants were self-incompatible and showed a high degree of outcrossing. Our experimental work confirmed the occurrence of protandry in this species, revealed that nectar is sucrose-dominant and proline-rich and, for the first time for Polemoniaceae, that nectar secretion and nectar sugar concentration in flowers of P. caeruleum is female-biased. Although flowers were visited by at least 39 species of insects from five taxonomic orders, overall the plant exhibited many characters associated with bee pollination, and analysis of insect performance showed that bumblebees and honeybees are the key pollinators; occasionally hoverflies and butterflies may also be involved. We conclude that, in terms of pollination system, P. caeruleum demonstrates high apparent generalization, but low realized generalization, and is a functional specialist, as most pollinators belong to a single functional group (guild). Its conservation status, at least in our study population, cannot be explained in terms of the biological properties of its breeding or pollination systems; rather, the present decline of the species is caused by habitat loss. However, if this process and bumblebee decline in Europe continue, P. caeruleum populations may diminish in numbers and density and, owing to the self-incompatibility of the species, quickly become severely pollen-limited, thereby accelerating further local extinctions. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 92–107.

Myophily in the critically endangered umbelliferous plant Ostericum palustre Besser (Apiaceae)

Globally, many plant species face human-induced habitat loss and an associated reduction in population size and vitality. Their survival is often possible only when appropriate conservation measures are taken that address the biology and ecology of these species, including their reproduction, often the most vulnerable stage in the life history of the organism. Unfortunately, little is known about these aspects of the biology of many listed plant species. For 3 years, we studied the pollination biology of the critically endangered plant species Ostericum palustre Besser (Apiaceae), one that is listed in the Bern Convention and Annex II of the EU Flora–Fauna Directive. Flowers of this taxon were visited by over 81 species of anthophilous insects derived from 5 taxonomic orders, indicating the presence of a generalised pollination system. However, detailed analyses of the frequency of insect visits, pollen loads and insect behaviour on inflorescences suggest that the plant is chiefly pollinated by large Dipterans, predominantly large Syrphid flies and Muscoid flies, that together are often responsible for over 90 % of total pollinations. Occasionally, wasps (Vespidae) may also be involved in the pollination of this species. With respect to the pollination system of O. palustre, our results indicate that this is a classic example of myophily, and generally, this species can be regarded as a functional specialist, but like many other members of Apiaceae, it is a typical “bet-hedger”. This strategy may probably increase the plant’s reproductive success in a range of habitat conditions, suggesting that the pollination system is unlikely to be the cause of rarity in this species.

Honey bee contribution to canola pollination in Southern Brazil

Although canola, (Brassica napus L.), is considered a self-pollinating crop, researchers have indicated that crop productivity increases as a result of honey bee Apis mellifera L. pollination. Given this crop's growing importance in Rio Grande do Sul State, Brazil, this work evaluated the increase in pod and seed productivity with respect to interactions with anthophilous insects and manual pollination tests. The visiting frequency of A. mellifera was correlated with the crop's blooming progression, and productivity comparisons were made between plants visited by insects, manually pollinated plants (geitonogamy and xenogamy) and plants without pollination induction. Pod set and seed production per plant were determined for each treatment. Among the 8,624 recorded flower-visiting insects, Hymenoptera representatives were the most prevalent (92.3%), among which 99.8% were A. mellifera. The correlation between these bees and blooming progression was positive (r = 0.87; p = 0.002). Pollination induction increased seed productivity from 28.4% (autogamy) to 50.4% with insect visitations, as well as to 48.7 (geitonogamy) and to 55.1% (xenogamy) through manual pollination.

Mechanical vs. Beetle-mediated Self-pollination inGossypium Tomentosum(Malvaceae), an Endangered Shrub

Experimental hand pollinations of the endangered, Hawaiian, endemic, Gossypium tomentosum Nutt. Ex. (Malvaceae) showed that it was self-compatible, but self-pollination resulted in reduced reproductive output. Field observations and pollen tube analyses using fluorescence microscopy showed that mechanical self-pollination in this species included a mechanism known as bending stigmas. A receptive stigma bent backwards and contacted dehiscent anthers in 7% of flowers found on 17 G. tomentosum plants. The yellow flowers were nectarless and were not visited by most anthophilous insects in situ except for the introduced, nitidulid beetle, Aethina concolor Macleay. Collections and insect GI-tract dissections showed that A. concolor carried and ate the pollen of the host flower. Field observations recorded regular contact between beetles and stigma lobes as these insects exited the flowers effecting self-pollination. Behavioral experiments showed that the beetles responded positively to a yellow visual cue. Under some circumstances, an introduced pollen vector may help maintain a low level of reproductive success in an insular endemic.

Evaluation of chrysanthemum flower model trap to attract two Frankliniella thrips (Thysanoptera: Thripidae)

Frankliniella occidentalis Pergande and F. intonsa Trybom (Thysanoptera: Thripidae) are anthophilous insect pests of many crops worldwide. We evaluated a flower model trap mimicking the chrysanthemum flower as a new method to attract the thrips in the laboratory and a strawberry greenhouse. Both choice and no-choice tests in the laboratory showed that the chrysanthemum flower model trap attracted significantly more adult F. occidentalis and F. intonsa compared to yellow sticky trap. Up to 4.1 times more of F. occidentalis and 5.4 times more of F. intonsa were caught in the flower model trap in the strawberry greenhouse. The flower model trap would be a good addition to the integrated thrips management, although at present it is more expensive than the yellow sticky trap.

Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth

Flower colour is an important signal used by flowering plants to attract pollinators. Many anthophilous insects have an innate colour preference that is displayed during their first foraging bouts and which could help them locate their first nectar reward. Nevertheless, learning capabilities allow insects to switch their colour preferences with experience and thus, to track variation in floral nectar availability. Manduca sexta, a crepuscular hawkmoth widely studied as a model system for sensory physiology and behaviour, visits mostly white, night-blooming flowers lacking UV reflectance throughout its range in the Americas. Nevertheless, the spectral sensitivity of the feeding behaviour of naïve moths shows a narrow peak around 450 nm wavelengths, suggesting an innate preference for the colour blue. Under more natural conditions (i.e. broader wavelength reflectance) than in previous studies, we used dual choice experiments with blue- and white-coloured feeders to investigate the innate preference of naïve moths and trained different groups to each colour to evaluate their learning capabilities. We confirmed the innate preference of M. sexta for blue and found that these moths were able to switch colour preferences after training experience. These results unequivocally demonstrate that M. sexta moths innately prefer blue when presented against white flower models and offer novel experimental evidence supporting the hypothesis that learning capabilities could be involved in their foraging preferences, including their widely observed attraction to white flowers in nature.

Diversidade de insetos antófilos em áreas com reflorestamento de eucalipto, município de Triunfo, Rio Grande do Sul, Brasil

O efeito da fragmentação de habitats tem sido avaliado medindo-se a riqueza e diversidade de determinados grupos funcionais, especialmente insetos visitantes florais. Esses organismos possibilitam conectividade funcional entre plantações e áreas protegidas e a restauração de ambientes alterados. Este estudo objetivou analisar a diversidade de insetos antófilos ao longo de transectos estabelecidos entre mata ciliar e reflorestamento de eucaliptos e exclusivamente entre talhões de eucaliptos, no sul do Brasil. Os insetos coligidos pertencem às ordens Hymenoptera, Lepidoptera, Diptera, Coleoptera e Hemiptera. Comparativamente a outros estudos, a abundância de insetos foi baixa. Vinte e oito espécies foram encontradas em ambos ambientes, enquanto 138 foram exclusivas em um ambiente (61 em mata ciliar/eucaliptos e 77 em eucaliptos/eucaliptos). Os insetos visitaram flores de 31 espécies vegetais, representantes de 20 famílias. Nos dois ambientes foram encontradas poucas espécies dominantes e um grande número representadas por um único indivíduo. A alta diversidade foi similar nos dois ambientes de estudo (H' = 4,084 e H' = 4,018). Entre os insetos, as abelhas mostraram a maior diversidade nos ambientes mata ciliar/eucaliptos (H' = 3,211) e eucaliptos/eucaliptos (H' = 2,8). Considerando-se a similaridade na estrutura da comunidade entre os ambientes, a fauna de insetos antófilos difere quanto à composição de espécies e número de indivíduos das espécies amostradas.

Observations of putative pollinators of Hemipilia flabellata Bur. et Franch. (Orchidaceae) in north-west Yunnan Province, China

Interactions between Hemipilia flabellata and anthophilous insects were studied in north-western Yunnan, China during June–July of 1996 and 1997. Twenty-seven species of insects were seen visiting the flowers of this species, although only male and female individuals of the bee Anthophora mangkamensis Wu were observed carrying the pollinaria. The frequency of visits by A. mangkamensis to this orchid was rather low. Pollinating bees normally sampled only the lowermost flowers in an inflorescence, staying for 1–3 seconds. This species is also characterized by low pollination, low fruit set (1–22%) and a very striking decrease in fruit production from bottom to top of the inflorescence. All of these indicate that the orchid may rely on deception to attract visitors. Ajuga forrestii Diels (Labiatae) appears to be the main or exclusive subsidiary nectar source for A. mangkamensis during the flowering period ofH. flabellata. It appears that H. flabellata utilizes a food deceit pollination strategy for pollination. The orchid benefits from the great variation of flowers in colour and shape. Phenological, functional-morphometric and distribution data indicate that A. mangkamensis is an optimal pollinator of H. flabellata and thus the anthecological adaptation of the orchid to the pollen vector may be unique.

Observations of putative pollinators of Hemipilia flabellata Bur. et Franch.(Orchidaceae) in north-west Yunnan Province, China

Interactions between Hemipilia flabellata and anthophilous insects were studied in northwestern Yunnan, China during June‐July of 1996 and 1997. Twenty-seven species of insects were seen visiting the flowers of this species, although only male and female individuals of the bee Anthophora mangkamensis Wu were observed carrying the pollinaria. The frequency of visits by A. mangkamensis to this orchid was rather low. Pollinating bees normally sampled only the lowermost flowers in an inflorescence, staying for 1‐3 seconds. This species is also characterized by low pollination, low fruit set (1‐22%) and a very striking decrease in fruit production from bottom to top of the inflorescence. All of these indicate that the orchid may rely on deception to attract visitors. Ajuga forrestii Diels (Labiatae) appears to be the main or exclusive subsidiary nectar source for A. mangkamensis during the flowering period of H. flabellata. It appears that H. flabellata utilizes a food deceit pollination strategy for pollination. The orchid benefits from the great variation of flowers in colour and shape. Phenological, functional-morphometric and distribution data indicate that A. mangkamensis is an optimal pollinator of H. flabellata and thus the anthecological adaptation of the orchid to the pollen vector may be unique.

Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems?

Abstract Native vegetation near Hobart in Tasmania was investigated to determine whether it was being invaded by the recently introduced large earth bumblebee, Bombus terrestris (Linnaeus, 1758). This species was found to be established in high numbers in a variety of vegetation types from coastal heath, through sclerophyll forest, and subalpine shrubberies up to an altitude of 1100 m. Hence, it has the potential to spread through much of Tasmania and temperate, mesic regions of mainland Australia. It is highly polylectic, foraging on at least 66 native plant species from 21 families. While the most heavily visited species produced abundant nectar, the lack of pre‐dation on this species also allowed it to forage economically on small flowers in clusters. This foraging profile overlapped with those of all anthophilous insect families, all bee subgenera, and all species of nectarivorous birds which were encountered. Therefore, B. terrestris has the potential to compete with most native anthophiles and commercial honeybees. As it forages from some plant taxa which are not visited by the European honeybee, Apis mellifera Linnaeus, 1758, this species is impacting on plant‐pollinator relationships which have previously been free from the effects of exotic bees.

SPATIAL FLOWER PARAMETERS AND INSECT SPATIAL VISION

ABSTRACTThe present article reviews recent and older literature on the spatial parameters that flowers display, as well as on the capacities of anthophilous insects to perceive and use these parameters for optimizing their foraging success. Although co‐evolution of plants and pollinators has frequently been discussed with respect to floral colours and insect colour vision, it has rarely been assessed with respect to insect spatial vision and spatial floral cues, such as shape, pattern, size, contrast, symmetry, spatial frequency, contour density and orientation of contours. This review is an attempt to fill this gap. From experimental findings and observations on both flowers and insects, we arrive at the conclusion that all of the spatial and spatio‐temporal parameters that flowers offer are relevant to the foraging task and are tuned to the insect's visual capacities and visually guided behaviour. We try, in addition, to indicate that temporal cues are closely related to spatial cues, and must therefore be included when flower–pollinator interactions are examined. We include results that show that colour vision and spatial vision have diverged over the course of evolution, particularly regarding the processing of spatio‐temporal information, but that colour vision plays a role in the processing of spatial cues that are independent of temporal parameters. By presenting this review we hope to contribute to closer collaboration among scientists working in the vast fields of botany, ecology, evolution, ethology and sensory physiology.

Timing in the evolution of derived floral characters: upper cretaceous (turonian) taxa with tricolpate and tricolpate-derived pollen

Various hypotheses that seek to explain the rich species diversity of angiosperms relative to other seed plants are briefly mentioned or reviewed. Of these, the subset that relates angiosperm diversity in some way to the relationship between angiosperms and insects, particularly anthophilous insects, is here the object of attention. Specifically, I address and reject the possibility that the relationship between angiosperm diversification and insects, particularly those demonstrating a preference for flowers with derived floral characteristics associated with insect pollination, may be ruled out because of asynchronous patterns of diversification in the fossil record. New data on floral structure from the Turonian of the Atlantic Coastal Plain reveal a surprising diversity of floral characters in taxa bearing tricolpate and tricolporate-derived pollen. The characters and taxa that appear in these Turonian sediments suggest that rather specific modes of insect pollination, perhaps involving highly derived insect pollinators, already existed at 90 Ma. Given the observed rate of diversification of angiosperms during that time and the pattern of evolution in insects, including what can be inferred about the history of the Apidae, these new floral data suggest that hypotheses relating angiosperm diversity to highly specific pollinators are still valid in the context of fossil evidence. Even so, consistency with fossil evidence is not necessarily proof of these relationships. In any case, there may well be multiple causes of relatively high angiosperm species diversity and understanding the relative importance of each of these requires neontological as well as paleontological investigations. One promising approach is to work within the context of phylogenetic patterns with more fossil data.

Flowers and their insect visitors in the arid winter rainfall region of southern Africa: Observations on permanent plots. Composition of the anthophilous insect fauna

The composition of the anthophilous insect fauna of a plant community in the north-western Cape, South Africa, has been investigated. During a 3-year survey more than 300 species belonging to four orders and 41 families have been identified as day-active floral visitors. The vast majority are solitary bees (136 spp.), but masarine wasps (14 spp.), bombyliid flies (53 spp.), and monkey beetles (20 spp.) are also well represented. The anthophilous insect fauna of Goegab appears to be far more diverse than those of desert scrub communities in California and Chile, but equally diverse as that of a Californian Chaparral site. Compared to the latter, Goegab seems to be particularly rich in bee flies, Masarinae and possibly Eumenidae, but poorer in bees and butterflies.

Flowers and their insect visitors in the arid winter rainfall region of southern Africa: observations on permanent plots. Insect visitation behaviour

Aspects of the relationships between the plants and the flower-visiting insects of the north-western Cape, South Africa, based upon a 3-year study on permanent plots, are examined. The vast majority of plant species of the study area show entomophilous pollination syndromes. Particularly noteworthy is the preponderance of large open brightly coloured blossoms, especially of Asteraceae and Mesembryanthemaceae, most of which show allophilous to melittophilous pollination syndromes. Flower-visiting records are given for more than 300 day-active insect species belonging to four orders and 41 families. From the flower-visiting records and the analysis of pollen loads of selected bee specimens it is concluded that the anthophilous insect fauna is dominated by generalist foragers. Most flower/insect associations are not exclusive and frequently overlap.

Insects and plants in the pollination ecology of the boreal zone

AbstractPollination systems in the boreal zone range from generalist to specialist, both entomologically and botanically. The relative importance of wind pollination, insect pollination, sexual separation between and within plants, and between flowers, hermaphroditism of flowers, and various breeding systems are related to plant growth form and habitat. The diversity and specializations of anthophilous insects parallel those in other biogeographic zones, but seem less developed. We suggest that this reflects the combined effects of evolutionary youth, severity of climate, restriction of symbiont ranges within those of their hosts, and the naturally frequent perturbations by fire or insect outbreaks in the zone, requiring faunal and floral vagility and constraining specialization in mutualism. Modern perturbations by logging and pesticides seem to be well buffered because of the relative openness of the ecosystem (compared to others), although damage has been documented. Insect pollination is as much a keystone process in the boreal forest as elsewhere, despite the immediate counter‐impression given by the dominance of wind‐pollinated conifers. Nevertheless, there are few studies, botanical or entomological in situ. The boreal system offers important opportunities in general and applied research in pollination ecology and synecology generally.

Observations on anthophilous Muscidae and other Diptera (Insecta) in Abisko National Park, Sweden

Muscidae are the dominant anthophilous insects in arctic and subarctic environments. In Abisko National Park, North Sweden, five genera were found to visit blossoms regularly for feeding. Species of Thricops and Phaonia fed extensively on pollen and nectar, and some specialized modes of gathering pollen are described. Morphological adaptations, abundance, activity, periodicity, and flower fidelity are discussed. Muscidae are the leading group of pollinators of open blossoms in arctic and subarctic ecosystems. Brief notes are given on other flower-visiting Diptera.

To make a meadow it takes a clover and a bee: the entomophilous flora of N.W. Europe and its insects

An analysis of the anthophilous fauna of N.W. Europe is presented, stressing the role plants play for insects. The study is based on some 29,000 relations between about 2,600 insect species and 1,300 plant species (569 genera). The data are derived from our database (“CrypTra”) of biotic relations between Cryptobiota and Tracheophyta, that is based on published sources. It is suggested that a ratio of 2 to 5 anthophilous insect species per entomophilous plant species is the rule in N.W. Europe, where other types of zoophily are virtually absent. A small minority of the plant species/generaplay a disproportionally important role as hosts to flower visitors; many of these so-called cornucopian taxa belong to the commonest entomophilous plants in the region, and occur also in moderately disturbed habitats. There is a significant positive correlation between the commonness of a plant species and the fraction this plant represents of the trophic resources exploited by an insect species. There is, on the other hand, a significant negative correlation between the number of insect species visiting a given plant species, and the number of plant species visited by a given insect species. These two elements together demonstrate that the anthophilous fauna and the entomophilous flora of N.W. Europe as a whole form a loose system, not predominantly characterised by specialisation. In accordance with this, factor analysis suggests that there is no ground to recognise more than three visitor types, viz., the allotropous, hemitropous, and eutropous visitors as defined by Loew. A minorityof the plant taxa - essentially the cornucopian ones - can with some difficulty be associated with these three types of visitors, and a very few narrowly specialised plant taxa can be associated with more specific visitor groups. However, the large majority of plants cannot be fitted in any typology. These results have practical implications for the nature management of the anthophilous fauna, in that the important role of the cornucopian floral element is underlined. The fact that the majority of the cornucopian species are perennial, or evenwoody, places constraints to agricultural practices intended to foster beneficial anthophilous insects.

Observations on the pollination of Pelargonium tricolor, section Campylia (Geraniaceae)

A group of four species of Pelargonium L’Herit. in the section Campylia (Sweet) DC. have embossed ‘warty areas’ at the bases of the posterior petals of the zygomorphic flowers. In Pelargonium tricolor Curt, these embossed areas are most distinctive. The significance of these embossed areas in the attraction of insect pollinators is discussed. From repeated observations of P. tricolor it is concluded that these areas are false nectaries and that they are effective in attracting dipteran pollinators. Megapalpus capensis Wiedemann (Diptera: Bombyliidae), in particular, exhibits strong association with these false nectaries. It is further predicted that the embossed areas on the petals of the remaining three species in the group, namely P. capillare (Cav.) Willd., P. ocellatum J.J.A. van der Walt and P. incarnatum (L’Herit.) Moench have similar value for attracting anthophilous insects.

Fossil evidence for the evolution of biotic pollination

The Cretaceous-Paleogene history of plants and insects reveals a discernible pattern in the evolution of floral character complexes and insects. Earliest Cretaceous flowers were small apetalous magnoliids with few parts. They co-occurred with a greater variety of anthophilous insects than has previously been supposed, and the idea that Coleoptera were the principal early insect pollinators is in need of review. By the mid-Cretaceous rosid flowers are known with well-developed corollas and the Rosidae are diverse by the late Cretaceous. The more derived asterid floral types are not firmly established until the Tertiary. Nectaries are present in many of the late Cretaceous rosids and may signal the beginning of the most significant evolutionary interaction between H ym enoptera and angiosperms. Advanced floral types in M aastrichtian and early Tertiary deposits are consistent with the appearance of meliponine Apideae (Stingless honeybees) in the late Cretaceous.

Deceit pollination of Orchis spitzelii (Orchidaceae) on the Island of Gotland in the Baltic: a suboptimal system

Interactions between anthophilous insects and Orchis spitzelii were studied on the island of Gotland, in the Baltic Sea of southern Sweden. The plant is nectar ‐ less and thus deceives its nectar‐seeking pollinators. No specific nectar‐plant model exists for mimetic resemblance, but the orchid produces an exuberant floral display. Pollinators comprise mainly bumble‐bee queens (Bombus spp.) that transport 90% of the pollinaria. The remaining pollinators are cuckoo bumble‐bee females (Psithyrus spp.). Pollinating bees make exploratory visits primarily to only a few of the lowermost flowers in inflorescences. Many‐flowered individuals are more attractive and have a higher fitness in terms of fruit set. Bees quickly learn to avoid the non‐rewarding orchid. Arctostaphylos uva‐ursi (Ericacae) and Rubus saxatilis (Rosaceae) are the most important subsidiary nectar plants for the bees during the flowering of O. spitzelii. Phenological, morphological and functional data indicate that the anth‐ecological adaptation to the main pollen vectors is suboptimal. Moreover, experiments indicate that O. spitzelii is an obligate outcrosser and lacks an effective isolating mechanism against the abundant and concurrently blooming Orchis mascula. It is therefore proposed that O. spitzelii has spread to Gotland in recent time.