Is Cycas revoluta (Cycadaceae) wind- or insect-pollinated?

Among the Cycadales (Cycadaceae and Zamiaceae), the Zamiaceae are known to be insect-pollinated. In contrast, the Cycadaceae are still considered wind-pollinated, although some doubt has been cast on several species, including Cycas revoluta. Using a large population of C. revoluta on Yonaguni Island (Okinawa, Japan), we performed exclusion experiments, documented insects from male and female cones, and analyzed the morphology of the apical part of the ovule to determine the pollination method of this species. Insect exclusion resulted in a notable reduction in seed set, except in a few individuals growing near male cones. The amount of airborne pollen was abundant within a 2-m radius of male cones but decreased markedly beyond this distance. Pollen grains of C. revoluta were found on the body of Carpophilus chalybeus (Nitidulidae, Coleoptera), one of a few species of insects collected from both male cones and female cones far from males. We conclude that C. revoluta relies on both wind (anemophily) and insect pollination (entomophily), although such anemophily is restricted to female trees growing within a 2-m radius of male trees. The nitidulids are not host specific to this cycad and primarily feed on plant tissue but serve as pollinators during pollen release. Cycas revoluta appears to be in an initial mode of animal pollination, as opposed to the host-specific insect pollination observed in most Zamiaceae.     

INSECT POLLINATION IN THE CYCAD ZAMIA PUMILA (ZAMIACEAE)

A wind and insect exclusion pollination experiment was conducted in a wild population of the cycad Zamia pumila L. in Florida. Cones from which insects but not wind were excluded produced no viable seeds, while cones from which wind but not insects were excluded produced abundant viable seeds. Two beetle species have been identified which may be effecting pollination. Adults and larvae of both beetles are found abundantly on the male cones, and adults of both species and larvae of one species are found occasionally on female cones. Z. pumila produces sugar and amino acid-rich micropyle droplets which may serve as pollinator rewards. Mimicry of resource-rich male cones by female cones and the use of cones as refuges between mating and feeding bouts may account for beetle movement from male to female cones.     

Geographical matching of volatile signals and pollinator olfactory responses in a cycad brood-site mutualism

Brood-site mutualisms represent extreme levels of reciprocal specialization between plants and insect pollinators, raising questions about whether these mutualisms are mediated by volatile signals and whether these signals and insect responses to them covary geographically in a manner expected from coevolution. Cycads are an ancient plant lineage in which almost all extant species are pollinated through brood-site mutualisms with insects. We investigated whether volatile emissions and insect olfactory responses are matched across the distribution range of the African cycad Encephalartos villosus. This cycad species is pollinated by the same beetle species across its distribution, but cone volatile emissions are dominated by alkenes in northern populations, and by monoterpenes and a pyrazine compound in southern populations. In reciprocal choice experiments, insects chose the scent of cones from the local region over that of cones from the other region. Antennae of beetles from northern populations responded mainly to alkenes, while those of beetles from southern populations responded mainly to pyrazine. In bioassay experiments, beetles were most strongly attracted to alkenes in northern populations and to the pyrazine compound in southern populations. Geographical matching of cone volatiles and pollinator olfactory preference is consistent with coevolution in this specialized mutualism.     

Pollination of the cycad <Emphasis Type="Italic">Zamia incognita</Emphasis> A. Lindstr. &amp; Idárraga by <Emphasis Type="Italic">Pharaxonotha</Emphasis> beetles in the Magdalena Medio Valley,Colombia: a mutualism dependent on a specific pollinator and its significance for conservation

The genus Zamia (Zamiaceae: Cycadales) exhibits its greatest diversity in Colombia and is highly threatened by habitat loss, extraction for ornamental plant trade, and mining, among other factors. One of the most important considerations for the effective conservation of Zamia is its highly specialized reproductive biology. Despite the importance of pollination for the populations’ viability, no studies have examined the pollination process of cycads in Colombia. Herein, we describe the pollination process of Zamia incognita A. Lindstr. & Idárraga, in a natural population. Exclusion experiments were performed by selectively excluding wind, beetles, both, or neither, which demonstrated that Pharaxonotha beetles are effective pollinators of Zamia incognita and that wind does not play any role as pollen vector. By following beetles marked with fluorescent dyes and directly observing beetle movements on and into female cones and micropyles, we confirmed that Pharaxonotha sp. is the effective pollinator of Z. incognita. The beetles traveled a maximum dispersal distance from a male to female cone of nearly 22 m and a minimum distance of 5 m. We found Pharaxonotha beetles in male cones, where they complete their life cycle. Cones produce heat in a circadian pattern associated with the elongation of the cones and pollen shedding. The increase in cones’ temperature appears to play an important role in beetle attraction. We suggest that pollination droplets on the micropyles would be a reward to pollinators. We also discuss the relationship of this Zamia species with other insects, which have important consequences for the conservation of web interactions.     

Plant-mediated indirect effects of carpenterworms on the insect communities attracted to fermented tree sap

Carpenterworm (Lepidoptera, Cossidae) larvae bore into trunks of the oak Quercus acutissima, thereby promoting sap exudation, and prey on insects attracted to tree sap. We examined the interactions between carpenterworms and sap-attracted insects to elucidate community-level consequences of carpenterworms and to estimate the relative magnitudes of their direct and indirect effects on community structure. Species richness, total abundance, and Simpson’s index of diversity (1/D) in tree sap communities were all significantly higher in carpenterworm-associated patches (sap-exuding patches that contained either larvae or larval nests) than in patches without evidence of carpenterworms. Abundance was also significantly higher in carpenterworm-associated patches for 10 out of 14 taxonomic groups, and this difference was much greater in the following groups that are sensitive to resource increases: drosophilid flies (Drosophilidae), sap beetles (Nitidulidae), and rove beetles (Staphylinidae). These results indicate that carpenterworms increase community size indirectly by increasing resource abundance, which is supported by the results of structural equation modeling (SEM). SEM also revealed that the direct effect of carpenterworms on species richness was weaker than their indirect effect, suggesting that predation by carpenterworms does not determine community structure. Similarly, carpenterworms can increase the abundance of some taxa by increasing resource abundance, and the predation pressure from carpenterworms on most taxa may be minor. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

An Appraisal of Range and Evolutionary Significance of Flower-Beetle Association,with Special Reference to Sap Beetles (Coleoptera: Nitidulidae)

A range of beetle species are associated with plants and many of them reside primarily in flowers; of these Nitidulidae possess a large share. Beetles which thrive upon angiosperms exhibited a rapid rate of speciation as compared to others with different feeding habits. Hence, beetles and angiosperms have co-evolved and influenced each others’ evolution for better survival. Some flower-visiting beetles have developed special features for floral diet and other purposes like pollination, shelter, reproduction, etc. Likewise, certain flowers also have adapted structurally and physiologically to attract beetles for pollination which include pollen, nectar, floral heat etc. Although beetles are found to be amongst the pioneer flower visitors, they are not as efficient pollinator as bee and butterfly. However, they have been found to be chief pollinators for a few plant families like Magnoliaceae, Annonaceae and Palmae. Several sap beetles have been encountered in floral parts in West Bengal, Assam, Uttar Pradesh, Karnataka and Tripura. Nature of relationships of those beetles with inflorescence and flowers were examined. None of them is yet found to be a true pollinator.     

Autodissemination of Beauveria bassiana by Sap Beetles (Coleoptera: Nitidulidae) to Overwintering Sites

An autoinoculative device was used to test the ability of sap beetles (Coleoptera: Nitidulidae) to carry a specific strain of Beauveria bassiana (Balsamo) Vuillemin to overwintering sites in a multiyear field study. The device was baited with the pheromone and coattractants for the dusky sap beetle (Carpophilus lugubris Murray) and placed in the field in the fall of each year. The introduced strain occurred at high frequency among the B. bassiana isolated in the fall of all four years tested (100% of all isolates from 21 of 22 collection dates). The introduced strain of B. bassiana was isolated at high frequency from all the B. bassiana-contaminated sap beetles recovered from the overwintering traps (100% of all isolates from 13 of 23 trap/beetle species combinations) and was highest after the longest fall exposure. The introduced strain was primarily isolated from C. lugubris and C. antiquus, but species distribution was also dependent on the overwintering trap design used. Few non-sap beetles species of insects were recovered from the artificial overwintering sites. Although B. bassiana was isolated from free flying sap beetles caught in traps in the spring of each year, none were infected with the introduced strain. The autoinoculating device provides selective contamination of sap beetles in overwintering sites when used in the fall. It may be useful in providing some control of sap beetles or other insects where limited numbers of mass overwintering sites (such as tree holes) occur.     

苏铁类植物传粉生物学研究进展(综述)

苏铁类植物是现存最古老的种子植物,研究其传粉特点,对于研究种子植物的起源与演化、植物与动物的协同进化以及苏铁类植物的繁殖机制、濒危机制有重要意义。本文从苏铁雌雄株开花物候学、传粉媒介及传粉机制等方面,对苏铁类植物传粉生物学相关研究进行综述,并提出今后该类植物传粉生物学研究的建议：对更多苏铁属种类未知的传粉机制进行研究;更广泛地应用排除法研究苏铁类特别是苏铁属植物的传粉媒介,进一步探讨传粉昆虫与苏铁类的共生关系问题。     

Rain forest provides pollinating beetles for atemoya crops

Small beetles, usually species of Nitidulidae, are the natural pollinators of atemoya (Annona squamosa L. x A. cherimola Mill. hybrids; custard apple) flowers but commercial atemoya growers often need to carry out labor-intensive hand pollination to produce enough high-quality fruit. Because Australian rain forest has plant species in the same family as atemoya (Annonaceae) and because many rain forest plants are beetle pollinated, we set out to discover whether tropical rain forest in far north Queensland harbors beetles that could provide this ecosystem service for atemoya crops. Orchards were chosen along a gradient of increasing distance from tropical rain forest (0.1-24 km). We sampled 100 flowers from each of nine atemoya orchards and determined the identity and abundance of insects within each flower. To assess the amount of pollination due to insects, we bagged six flowers per tree and left another six flowers per tree accessible to insects on 10 trees at an orchard near rain forest. Results indicated that atemoya orchards < or = 0.5 km from rain forest were predominantly visited by five previously unrecognized native beetle pollinators that are likely to originate in tropical rain forest. These native beetles occurred reliably enough in crops near rain forest to have a positive effect on the quantity of fruit produced but their contribution was not great enough to satisfy commercial production needs. Management changes, aimed at increasing native beetle abundance in crops, are required before these beetles could eliminate the need for growers to hand pollinate atemoya flowers. Appreciation of the value of this resource is necessary if we are to develop landscapes that both conserve native biodiversity and support agricultural production.     

Pollination of Australian Macrozamia cycads (Zamiaceae): effectiveness and behavior of specialist vectors in a dependent mutualism

Complementary field and laboratory tests confirmed and quantified the pollination abilities of Tranes sp. weevils and Cycadothrips chadwicki thrips, specialist insects of their respective cycad hosts, Macrozamia machinii and M. lucida. No agamospermous seeds were produced when both wind and insects were excluded from female cones; and the exclusion of wind-vectored pollen alone did not eliminate seed set, because insects were able to reach the cone. Based on enclosure pollination tests, each weevil pollinates an average 26.2 ovules per cone and each thrips 2.4 ovules per cone. These pollinators visited similar numbers of ovules per cone in fluorescent dye tests that traced insect movement through cones. Fluorescent dye granules deposited by Cycadothrips were concentrated around the micropyle of each visited ovule, the site of pollen droplet release, where pollen must be deposited to achieve pollination. In contrast, Tranes weevils left dye scattered on different areas of each visited ovule, indicating that chance plays a greater role in this system. Each weevil and 25 thrips delivered 6.2 and 5.2 pollen grains, respectively, on average, to each visited ovule per cone, based on examination of dissected pollen canals. In sum, the pollination potential of 25 Cycadothrips approximates that of one Tranes weevil.     

印度加尔各答市区外围一地的露尾甲物种组成、多度和季节性发生(英文)

【目的】印度大部分露尾甲在腐烂的水果和蔬菜上大量发生,其种群在一年中表现出明显的季节性波动。据推测,露尾甲种群很大程度上依赖于温度、湿度和降雨之类的环境因子。【方法】本研究调查了2013-2015年印度加尔各答市区外围一地Garia的露尾甲物种组成、季节性发生和种群结构,记录了其活跃时期、季节性多度和影响其发生的因素。【结果】调查期间在调查地共发现数目不等的6个物种。其中最常见露尾甲为Urophorus humeralis,它是个体数量最多的物种且在一年中几乎所有月份均有发生;其他常见物种为Epuraea ocularis和E. luteola。不同物种在食物发酵的连续阶段进入诱捕器中。最初12 h被捕获的是Epuraea 属的种类,而在诱捕器中食物严重腐烂的后续阶段发现最多的是U. humeralis。在合适范围的气温(22~29℃)和相对湿度(82.5%~86%)下,物种丰富度最高,表明这些环境变量对露尾甲种群具有重要影响。【结论】加尔各答主要水果和蔬菜在季风后季节种植,在季风后季节取食这些作物的露尾甲发生量(物种丰富度和多度)最高。这一研究结果可能有助于制定针对这些甲虫的有效田间治理策略。     

Critical factors in the limited occurrence of the Japanese tree sap mite <Emphasis Type="Italic">Hericia sanukiensis</Emphasis> (Acari: Astigmata: Algophagidae) inhabiting the sap of the oak <Emphasis Type="Italic">Quercus acutissima</Emphasis>

Hericia sanukiensis (Astigmata: Algophagidae) is a semi-aquatic mite inhabiting fermented sap flux of the Japanese sawtooth oak (Quercus acutissima) and utilizes Nitidulidae (Coleoptera) as the dispersal (phoretic) carrier. Although nitidulid beetles are commonly found in sap flux, the occurrence of H. sanukiensis has been extremely limited to a few trees in Shikoku Island, Kagawa Prefecture, Japan. To elucidate the critical factors limiting the occurrence of this species, we compared several physical and biological characteristics of sap-exudation points, including the structure and temperature of tree trunks, period and abundance of sap exudation, and seasonal occurrence and dispersal behavior of nitidulid beetles between environments with and without mites. During the two consecutive years of field research, we found that only sap-exudation points with obvious tree holes (ringent area >10 cm², depth >10 cm) had sustained mite populations throughout the observation period. In contrast, for the sap-exudation points lacking tree holes, H. sanukiensis temporally (from spring to autumn) colonized only when the sap production was considerably high. Thus, we suggest that the settlement of H. sanukiensis populations requires tree holes as an overwintering habitat. Nitidulid beetles also concentrated in areas with high sap production and did not disperse from such habitats during the sap flow season. This indicates that H. sanukiensis mites may only disperse and colonize new habitats at very limited opportunities, such as drastic habitat deterioration, which may promote the movement of their carrier. Taken together, these findings may explain the limited occurrence of this mite species.     

A novel pollination mode,saprocantharophily, in Duguetia cadaverica (Annonaceae): A stinkhorn (Phallales) flower mimic

Duguetia cadaverica (Annonaceae), a small understory tree of humid primary forest from the Guianas to Pará state, Brazil, unites several unusual blossom and floral characters such as flagelliflory and putrid-smelling flowers, respectively. The few pollination studies conducted in the large genus Duguetia have shown that species are usually cantharophilous, pollinated by either small (mostly Nitidulidae) or large specialized dynastid (Scarabaeidae) beetles. Foul-smelling flowers are a novelty within the genus, and to better understand their significance, we undertook a study of the reproductive biology and flower scent chemistry of D. cadaverica. In a primary forest of French Guiana, we observed and measured morphology and phenology of trees and flowers; additionally, flower pollination chamber temperature was measured and insect visitors to flowers observed. Flower scent was collected in situ and later analyzed in the laboratory by GC–MS. Flowers are visited by small beetles of a single Pycnocnemus species (Nitidulidae), which are the only insects observed to enter the pollination chamber. Moreover, flowers evince a rhythm in sexual stage, scent emission and temperature, which finds correspondence in behavioral characters of the putative nitidulid pollinator, such as timing of entry and exit from the pollination chamber. Floral scent analysis revealed an unusual, previously undescribed combination of chemical odor classes. The earthy, rank flower scent contained 18 compounds, among them fatty acid derivatives, terpenoids and N- and S-bearing compounds. The most abundant volatiles were 1-octen-3-ol, 3-octanone, and (E)-2-octenol, which are characteristic earthy odors of fungi; additionally, there were sulfides and 4-methylpentanoic acid, which are molecules associated with carcass and cheese odors, respectively.     

Suitability of commercially available insect traps and pheromones for monitoring dusky sap beetles (Coleoptera: Nitidulidae) and related insects in Bt sweet corn

Two trap types and pheromone sources for the dusky sap beetle, Carpophilus lugubris Murray (Coleoptera: Nitidulidae), were compared in Bacillus thuringiensis (Bt) and non-Bt sweet corn fields over a 3-yr period. Overall, commercial traps and pheromones were equally effective as experimental traps and pheromones used previously for capturing C. lugubris and other sap beetle species. The commercial trap often caught significantly more Glischrochilus quadrisignatus Say than the experimental trap that had been used in previous studies. Bt corn significantly reduced caterpillar damage to ears compared with the non-Bt isoline and did not adversely affect levels of Orius sp., the most common insect predator. Sap beetle damage was the most common insect damage to Bt sweet corn ears. Sap beetles were detected by traps at population levels below that which are likely to cause economic concern, indicating commercially available traps and pheromone lures for monitoring sap beetles should be suitable for detecting them under commercial growing conditions.     

Cycad mutualist offers more than pollen transport

Specialist insects share obligate mutualisms with some contemporary cycad species whereby the insect's pollination services are rewarded with a nursery in which the insect's larvae consume the postdispersal male cone. I prevented visits of the pollinator moth Anatrachyntis sp. to male Cycas micronesica (Cycadaceae) cones to show that consumption of the cone tissue by the mutualist hastened initiation of the plant's subsequent reproductive event. This is the first documented case where removal of a postdispersal cycad pollination organ speeds up subsequent reproductive events, and the current paradigm that the offering of cone tissue as a nursery is a sacrifice by the plant in return for the pollination services is therefore inaccurate. In C. micronesica, the herbivory stage of pollination mutualism confers a cryptic benefit of cone tissue disposal, which translates into an increase in ultimate lifetime reproductive effort. The plant population relies on the pollinator for moving gametes, as well as for increasing the number of male coning events. The dual benefits afforded to the plant by associating with this pollinator shows that mutualism can operate simultaneously on very different traits.     

Investment in visual system predicted by floral associations in sap beetles (Coleoptera: Nitidulidae)

Patterns in morphological variation are a central theme of evolution. Uncovering links between morphological character evolution and natural history, specifically feeding behaviour, is important to understanding biological diversity. Species within the sap beetles (Nitidulidae) exhibit a tremendous diversity of feeding behaviours. This immense diversity of feeding can be seen both between major lineages and very closely related taxa. Feeding behaviour diversity may drive morphological variation in several character systems (e.g., eyes). For example, in a shift from feeding on rotting fruit to flower-visiting (anthophily), selective pressures on the visual system may vary and ultimately lead to differences in eye morphology. We tested for potential morphological shifts in relative eye size among adult beetles. We specifically tested for significant relationships between relative eye size and the following factors flower-visiting and sex. We also tested for the influence of phylogeny on the evolution of relative eye size, implementing tests of trait correlation across a topology. We found greater relative eye size in taxa exhibiting anthophilous behaviour, regardless of phylogenetic relatedness or feeding behaviour of sister taxa. We were unable to recover a relationship between relative eye size and sex. Thus, feeding behaviour is currently the strongest predictor of eye size in sap beetles.     

Is there a floral parasite mutualism in cycad pollination? the pollination biology of Encephalartos villosus (Zamiaceae)

Observations and experiments were carried out over 5 yr to distinguish between wind and insect pollination in the cycad Encephalartos villosus Lemaire (Zamiaceae). They were also designed to determine whether a pollination mutualism exists between E. villosus and Antliarhinus zamiae (Thunberg) (Coleoptera: Brentidae), an obligate ovule parasite that routinely parasitizes a large proportion of the ovules. The percentage of fertilized ovules dropped slightly when wind was excluded from the megastrobilus. However, when insects were excluded by either net bags or insecticide there was a substantial decrease in the proportion of fertilized ovules. Five beetle species belonging to four families were found on the strobili at the time of pollination. Using data on the effectiveness of pollen transfer to the receptive ovule, as well as data on abundance and pollen loads, a pollinator importance value (PIV) was determined for each beetle species and a pollinator importance index (PII) was determined for each population. PII values showed that an undescribed weevil (Porthetes sp., Curculionidae) was consistently the most important pollinator. A. zamiae and an undescribed beetle species within the Xenoscelinae (Languriidae) played a minor role in pollination, and their contributions varied from year to year and between populations. Two additional beetle species, Metacucujus goodei Endrödy-Younga (Boganiidae) and a second species of Xenoscelinae, had very low PII values and probably had little or no effect on pollination. Low PIV scores for A. zamiae were a result of its low numbers on the microstrobilus and the tendency of the beetles to remain on the outside of the megastrobilus. In the interaction between E. villosus and A. zamiae, the cycad does not appear to benefit significantly from a pollination service and I interpret this to mean that the relationship is antagonistic rather than mutualistic. There is, however, a possible mutualism between Porthetes sp. and E. villosus.     

Ambrosiodmus rubricollis (Eichhoff) (Coleoptera; Curculionidae; Scolytinae) associated with young Tasmanian blue gum trees

Eucalypts are among the most widely planted forest trees in the world, and outside their native Australian range, the main arthropod pests are sap‐sucking insects, defoliators, gall‐making insects and xylophagous beetles. We report on a new association between a polyphagous wood‐boring beetle and Tasmanian blue gum (Eucalyptus globulus Labill.) in Central Portugal. Unidentified wood‐boring insects were found attacking two three‐year‐old E. globulus trees showing signs of decline among otherwise healthy trees in a commercial plantation, in June 2018. Declining trees presented dead twigs and branches, and recently developed epicormic sprouts evident on the trunks. Insects emerging from logs were identified as Ambrosiodmus rubricollis (Eichhoff), a species native to eastern and southern Asia, with the taxonomic identification validated by molecular analysis. To our knowledge, this is the first record of A. rubricollis associated with a eucalypt species worldwide. It is not clear whether the beetles played any significant role on the decline of the trees, but Ambrosiodmus may be potential pests for several tree and shrub species in Europe, as these beetles can transport pathogenic fungi.     

Evidence for beetle pollination in the African grassland sugarbushes (Protea: Proteaceae)

Most lineages in the African genus Protea consist of species with large unscented flowers pollinated principally by birds, and several of these lineages also show evidence of shifts to rodent pollination, associated with concealed yeasty-scented flowerheads. In this study we investigated the hypothesis that brightly coloured and fruity-scented flowerheads of four Protea species (P. caffra, P. simplex, P. dracomontana and P. welwitschii) represent a novel shift from bird to insect pollination in a grassland lineage in the genus. These species are visited by a wide range of insects, but cetoniine beetles were found to be the most important pollinators because of their abundance, size and relatively pure pollen loads. Three of the four putatively insect-pollinated Protea species have flowers presented at ground level, and experiments showed that cetoniine beetles preferred inflorescences at ground level to those artificially elevated to the height of shrubs and small trees. Relative to insects, birds were infrequent visitors to all of the study species. The nectar of all the study species contained xylose, as documented previously in bird- and rodent-pollinated Protea species, suggesting that this is a phylogenetically conserved trait. However, the very low concentration of nectar (ca. 8%), short nectar-stigma distance and the fruity scent of florets appear to be traits that are associated with specialisation for pollination by cetoniine beetles.     

Life history of the newly discovered Japanese tree sap mite, Hericia sanukiensis (Acari, Astigmata, Algophagidae)

Hericia sanukiensis (Acari, Algophagidae) is a species of tree sap mite which has been newly discovered in the sap flux of oak trees (Quercus acutissima). In this study, we have clarified the life history of H. sanukiensis at the onset of sap exudation in spring, overwintering deutonymphs molt to tritonymphs as their molting is exacerbated by the sugar contained in the tree sap, and develop to adulthood and reproduce. The mite colony develops as long as the sap continues to exude during the spring and summer. In this period, most of the protonymphs develop into tritonymphs directly bypassing the deutonymphal stage completely. Facultative deutonymphs which arise in the summer season are phoretic morphs. They attach to coleopteran insects, especially of the family Nitidulidae, as carriers by which to disperse. In autumn (when sap exudation terminates), most of the protonymphs molt to non-phoretic deutonymphs. In winter (without sap exudation), the mite colony is composed only of non-phoretic deutonymphs.