Hoverflies can sense the risk of being trapped by carnivorous plants: An empirical study using Sphaerophoria menthastri and Drosera toyoakensis

Carnivorous plants are major predators of small insects in some habitats. Because traps of carnivorous plants are serious threats for small insects, it is probable to evolve a mechanism to sense a cue of carnivorous plants and avoid being trapped. However, such a sensing behavior of small insects has never been described. Here we report that a hoverfly species Sphaerophoria menthastri, a major pollinator species of carnivorous sundew Drosera toyoakensis, exhibits a behavior to sense a cue of trap leaves and avoids landing there. In a quadrat (5?m?×?5?m) where D. toyoakensis and other non-carnivorous plant species co-occur, we observed behaviors of hoverflies approaching D. toyoakensis and other plants. The numbers of approaches to trap leaves, flowers of D. toyoakensis, flowers of non-carnivorous Lysimachia fortunei and leaves of Poaceae and Cyperaceae were 9, 60, 52 and 54, respectively, and the numbers of landings to those four organs were 2, 55, 49 and 49, respectively. When S. menthastri approached trap leaves, almost all individuals successfully avoided landing there by 1 or 2 hesitation behaviors. These findings suggest that S. menthastri can sense the cue of trap leaves during an approach.     

A sensitive flower: mechanical stimulation induces rapid flower closure in Drosera spp. (Droseraceae)

Some plants rapidly close their leaves in response to mechanical stimulation, but no case is known in which mechanical stimulation causes rapid petal closure. In this study, we found that Drosera tokaiensis closes petals within 2–10 min after experimental stimulation of the calyx, closed flowers or scapes with a pair of tweezers. Although petal closure was induced more rapidly by touching a position closer to a flower, it was not induced by stimulating stamens and pistils. The habit of petal closure varies among species of Drosera: after experimental stimulations of the calyx or scapes, D. tokaiensis and D. spatulata often closed petals but D. rotundifolia and D. toyoakensis did not close them. The petal closure may function as defense against a specialist florivore.     

The significance of opportunistic predators for the sympatric carnivorous plant species Drosera intermedia and Drosera rotundifolia

Summary Earlier feeding experiments with Drosera in the field using adult Drosophila melanogaster as prey had shown that D. intermedia reacts three times as strong with respect to biomass production as the sympatric species D. rotundifolia. The present study shows that in D. rotundifolia only 29% of added flies remain on the leaves for more than 24 h, but 95% in D. intermedia. Opportunistic predators, mostly ants, are likely to be responsible for this difference. Ants were often observed robbing food from the leaves of D. rotundifolia, and showed a much higher activity in the microhabitat of this species. In both species of Drosera larger individuals were better than smaller ones in retaining added flies. The activity of ants significantly increased with air temperature and the duration of sunshine. The advantage of plundering seems to be more important for the ants than the danger of being caught. The prey collected from Drosera may be an important source of food for bog-dwelling ants.     

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.     

Flexibility of Pollinator-Flower Relationship in Isodon umbrosus and I. effusus (Lamiaceae) and its Relation to Fruit-set and Seed-set

Isodon umbrosus was pollinated by two bumblebee pollinators, Bombus honshuensis and B. diversus. B. diversus was a secondary pollinator when both pollinators were present, but in the absence of B. honshuensis, B. diversus pollinated I. umbrosus, and the resulting seed production was comparable to when visited by the two bumblebee species together. Not only the high visitation frequency of B. diversus but also the low ratio of seed to ovules (= average seed set × fruit set) of I. umbrosus compensated for the low pollination efficiency of B. diversus. Since, the low pollination efficiency of B. diversus, based on the finding that the low average seed set of I. umbrosus did not require a definite morphological match between flowers and pollinators, and did not require very frequent visitations to each flower. In other words, Isodon umbrosus could briefly maintain constant seed production under the condition of the low ratio of seeds to ovules (the low seed set and the low fruit set) and a large number of flowers without B. honshuensis as legitimate pollinator. On the other hand, I. effusus was exclusively pollinated by B. diversus and produced almost the same volume of seeds as I. umbrosus. Isodon effusus had fewer flowers than I. umbrosus, but this smaller number of flowers was compensated for by the high ratio of seeds to ovules in I. effusus, which was maintained by frequent visitations of the morphologically matched pollinator, B. diversus. Received 17 September 1999/ Accepted in revised form 10 February 2000     

Size,structure and nitrogen content of seeds of Fabaceae in relation to nodulation

Looking for clues to explain the low rate and unpredictability of the pollination of allogamous, epiphytic orchids in the context of the success of the orchid family in general, we compared the pollination of two miniature twig epiphytes in Mexico: Notylia barkeri, a ‘weedy’, rewarding species, and Erycina crista‐galli, a rare, deceptive species. We measured the effects of the spatial organization of the flowers and various parameters of visibility and height above the ground in relation to the spatial organization of the seed capsules (which retrospectively measures the activity of the pollinators). The spatial presentation of the flowers of E. crista‐galli explained only 5% of the distribution of the seed capsules. For N. barkeri, with compound flowers, the spatial presentation, considering individual flowers or inflorescences, explained 12% and 45% of the distribution of the seed capsules, respectively, and all other interactions between the variables were insignificant. Both the deceptive and reward strategies resulted in the production of large numbers of seeds despite a low pollination percentage (1–5%). Notylia barkeri produced 11.8 (2005–6) and 53.7 (2007–8) times more seeds in total than E. crista‐galli. Furthermore, unlike E. crista‐galli, N. barkeri responded to loss of individuals after high winds with an increased production of flowers per plant. We suggest that orchids have evolved to specialize in chance, and instead of maximizing pollinator attraction, they maximize the seed production resulting from every casual encounter. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165 , 251–266.     

Determinants of seed production in Geranium maculatum

Summary We experimentally examined factors limiting seed production in two populations of the perennial woodland herb Geranium maculatum in central Illinois, USA. To test the pollinator-limitation hypothesis, we compared the seed production of plants whose flowers were supplementarily pollinated with outcross pollen to that of control plants receiving natural pollination only. To test if fruit production by early flowers suppresses fruit and seed formation by late flowers, a third group of plants was prevented from producing seed from the first 50% of the flowers to open (stigmas were excised at flower opening). Finally, to test if seed maturation and flower initiation are correlated with photosynthetic capacity, we performed a defoliation experiment in which either the stem leaves within the inflorescence, the stem leaves below the inflorescence, or the rosette leaves were removed during late flowering. Plants that reccived supplemental pollination produced 1.5–1.6 times more seeds than control plants. We found no difference between hand-pollinated plants and controls in mortality, flowering frequency or number of flowers produced in the year following the experiment. In both control and hand-pollinated plants, the fruit set and total seed production of early flowers were more than twice as high as those of late flowers. In one of the two populations, plants whose early flowers were prevented from setting seed produced significantly more seeds from their late flowers than did control plants. Seed predation was low and did not differ between early and late flowers. Leaf removal did not affect seed number or size in the year of defoliation, nor did it reduce survival or flower production in the subsequent year. This suggests that the plants were able to compensate for a partial defoliation by using stored resources or by increasing photosynthetic rates in the remaining leaves. Taken together, the results demonstrate that both pollinator activity and resource levels influence patterns of seed production in G. maculatum. While seed production was pollinatorlimited in both populations, a seasonal decline in resource availability was apparently responsible for the low seed production by late flowers.     

Effectiveness of ants as pollinators of<Emphasis Type="Italic"> Lobularia maritima</Emphasis>: effects on main sequential fitness components of the host plant

The effectiveness of ants as pollinators of Lobularia maritima (Cruciferae) was experimentally analyzed by assessing (1) their quantitative importance at flowers; (2) their effect on host plant seed production; (3) their effect on the performance of host plant progeny, estimated as seed germination, seedling emergence, seedling survival to flowering, and (4) the overall effect of ants on a cumulative, more realistic measure of plant fitness related to the recruitment probability. Flowers of L. maritima were visited during the 2 years of study (1996 and 1997) by more than 50 pollinator species belonging to about 30 families of disparate taxonomic affiliation, notably ants and flies. There was significant seasonal variability in insect abundance and type. Ants, especially Camponotus micans (Formicidae), visited the flowers of L. maritima in summer, representing 81.2% of the visits during this season. This ant species acted as a pollinator of L. maritima, with flowers visited exclusively by ants producing significantly more seeds than flowers from which all pollinators were excluded, whereas flowers visited by only winged insects did not differ from self-pollination. Ant-pollinated flowers produced seeds with a germination rate comparable to the other treatments. Moreover, seedlings from these seeds emerged as fast, and survived at the same rate as controls. Consequently, both ants and winged insects had similar overall effects on host plant recruitment probability (0.6 and 0.7% of initial ovules produced flowering offspring, respectively), a result similar to that of open-pollinated flowers (1.0%). This study demonstrated that the overall effectiveness of the ant C. micans as a summer pollinator of L. maritima was as high as that of other winged insects, contributing not only to the seed production of this crucifer but also to the recruitment of new flowering offspring. Received: 17 February 1999 / Accepted: 26 August 1999     

POLLINATOR EFFECTIVENESS AND SEED SET IN POPULATIONS OF AGALINIS STRICTIFOLIA (SCROPHULARIACEAE)

Examining variation in pollinator effectiveness and seed production resulting from single pollinator visits can provide a deeper understanding of how pollinators may influence reproduction in plant populations. When comparing populations, differences in the number of seeds produced from single pollinator visits to flowers may not always be attributable to differences in pollen deposition, but rather to differences in plant fecundity or resource availability. Pollinator effectiveness and seed production were studied for two populations over a 4-year period and were measured using single bee visit manipulations of flowers. No significant difference in pollinator effectiveness (pollen deposited on stigmas) was observed between the two populations. However, a significant difference between the two populations was observed in the number of seeds produced per flower. The Wellhouse population produced approximately three times as many seeds/flower from a single pollinator visit as did the Firefly Meadow population. Within each population, pollinators (Bombus pennsylvanicus and Apis mellifera) did not differ in the number of pollen grains deposited on stigmas or seeds produced per flower from single visit experiments. Differences in plant density, pollen viability, and ovules per flower also could not account for a significant amount of the variation. A resource augmentation experiment (water and fertilizer application) resulted in a decrease in seeds per flower per bee visit for the water treatment at the Wellhouse population only. For both populations, pollen deposition, pollen viability, and ovules per flower were unaffected by the resource augmentation. Alternative possibilities for the observed differences in seeds per flower per bee visit are discussed.     

Resource allocation: a conflict in the fig/fig wasp mutualism?

Conflicts of interest are omnipresent between mutualist species. In the monoecious fig/pollinator wasp mutualism, each female flower produces either a seed or a pollinator offspring (which has fed on a single seed). Pollen from a syconium (i.e. fig, a closed urn-shaped inflorescence) is only dispersed by female pollinator offspring born in this syconium. Thus the fig tree is selected to produce both seed and pollinator offspring whereas for the pollinator there is no short term advantage in seed production. Using controlled pollination experiments (pollen injection, and foundress introduction), we show that 1) The relative proportion of seeds and pollinator offspring produced (i.e., the effective allocation between female and male function) depends mainly on the number of foundresses that entered the syconium. 2) Many female flowers within every syconium mature neither a seed nor a wasp (from 25% to 33%). 3) All the female flowers within a syconium that are not vacant at maturity have the potential to produce a seed, and at least 80% of them can produce a pollinator. Several hypotheses concerning mechanisms that govern the partitioning between seed and wasp production are discussed, and their evolutionary consequences are considered.     

Seed set variation in wild Clarkia populations: teasing apart the effects of seasonal resource depletion,pollen quality,and pollen quantity

In habitats where resource availability declines during the growing season, selection may favor early‐flowering individuals. Under such ephemerally favorable conditions, late‐blooming species (and individuals) may be particularly vulnerable to resource limitation of seed production. In California, a region prone to seasonal drought, members of the annual genus Clarkia are among the last to flower in the spring. We compared pollen limitation (PL) of seed set and outcrossing rates between early‐ and late‐flowering individuals in two mixed‐mating Clarkia taxa to detect whether flowering time is associated with changes in seed set due to resource depletion, PL, or increased selfing. In 2008–2010, we hand‐pollinated one flower on a total of 1855 individual plants either Early (near the onset of flowering) or Late (near the end of flowering) in the flowering season and compared seed set to adjacent, open‐pollinated flowers on the same stem. To assess the contribution of pollen quality to reproduction, we first (2008) used allozymes to estimate outcrossing rates of seeds produced by Early and Late open‐pollinated flowers. Second (2009), we conducted an anther‐removal experiment to estimate self‐pollen deposition. Seed set in Clarkia unguiculata was not pollen‐limited. Clarkia xantiana ssp. xantiana was pollen‐limited in 2008 and 2010, but not 2009. PL did not differ between Early and Late treatments. In both taxa, seed set of Early flowers was greater than Late flowers, but not due to PL in the latter. Reproduction was generally pollinator‐dependent. Most pollen deposition was xenogamous, and outcrossing rates were >0.7 – and similar between Early and Late periods. These results suggest that pollen receipt and pollen quality remain seasonally consistent. By contrast, the resources necessary to provision seeds decline, reducing the fitness benefits associated with resource allocation to ovules.     

The inheritance of partial self-compatibility in Brassica oleracea L. inbreds homozygous for different S-alleles

Summary In a study of partial self-compatibility in Brassica oleracea, flower number, seeded siliqua and seed production were recorded on self and cross-pollinated inflorescences of 32 progenies obtained by inter-crossing and selfing 8 plants homozygous for the incompatibility alleles S₂, S₅, S₁₅ and S₄₅.Progeny differences for both self-and out-cross seed production could be largely attributed to G.C.A. effects which were essentially uncorrelated. For cross-pollinated inflorescences heterosis was also important. Significant differences were found for selfed seed set and its two components, the proportion of flowers producing seeded siliquae and the numbers of seed per seeded siliqua, between parents with the same S-allele which could not be attributed to S-genotype alone. No evidence of increased self-compatibility in particular S-allele heterozygotes (mutual weakening) could be found.Outcross seed production depended primarily on the numbers of seeds set per seeded siliqua while self seed production was largely determined by the proportion of flowers which produced seeded siliqua. It is suggested that this is a key character for the production of inbred lines with reduced partial self-compatibility.     

Enhancement of fruit quality in Capsicum annum through pollination by Hypotrigona gribodoi in Kakamega,Western Kenya

A study was carried out in Kakamega forest, in the western region of Kenya, to evaluate the effectiveness of the stingless bee Hypotrigona gribodoi (Magretti, 1884) on the pollination of green pepper. Three treatments were applied and consisted of self‐pollination, pollination by feral pollinators in the open field and pollination by H. gribodoi in a net cage. The differences in fruit yield and seed quality were compared among treatments. Flowers pollinated by H. gribodoi produced the heaviest fruits with the highest seed numbers followed by feral pollinators and lastly self‐pollinated flowers. Moreover, seeds were significantly bigger in size in fruits resulting from flowers pollinated by H. gribodoi compared to fruits obtained from self‐pollinated flowers or flowers pollinated by feral insects. We, therefore, conclude that H. gribodoi is an efficient pollinator of green pepper in the tropical region of East Africa.     

Plant size,breeding system,and limits to reproductive success in two sister species of Ferocactus (Cactaceae)

Plant reproductive output can be limited by a variety of factors, bothintrinsic and extrinsic. I investigated the reproductive biologies of twospecies of unbranched short-columnar cacti, Ferocactuscylindraceus and F. wislizeni. I recordedfemalereproductive output (flowers produced, fruit set, seeds per fruit and seedmass), plant size and growth, and used hand-pollination experiments todeterminebreeding systems and pollen limitation. In both species, the ability to selfvaried among individuals, but self-pollination resulted in very few seeds,suggesting strong inbreeding depression. Neither species was pollen-limited.Numbers of flowers produced increases with plant size for both species, andseeds per fruit may also be related to plant size, although the relationship isunclear. Seed mass is not correlated with plant size. Flower production wassimilar in both species, but F. cylindraceus producedfewerseeds per fruit than F. wislizeni, and its seeds weighedless. Fruit set by F. cylindraceus was heavily impacted bya florivorous lepidopteran. Fruit set was very high (94 to 96%) inF. wislizeni, suggesting that architectural constraints(e.g., meristem limitation) are more limiting than resource levels or the levelof pollinator services. In F. cylindraceus, numbers ofseeds per fruit was positively correlated with seed mass, whereas inF. wislizeni, the relationship was negative (tradeoff).Thegrowth rates of F. wislizeni are affected by rainfall theprevious season, and growth rates increase as the plant ages.Ferocactus cylindraceus and F.wislizeni are thought to be sister species, meaning that observeddifferences between them are more likely to be the result of recentevolutionaryprocesses in their lineages rather than differing phylogenetic histories.     

Non‐pollinating Fig Wasps Decrease Pollinator and Seed Production in Ficus andicola (Moraceae)

Fig trees ( Ficus spp.) and Agaonine fig‐wasps participate in an obligate mutualism. Fig wasps can only develop within fig inflorescences (syconia) and they are the only organisms capable of pollinating fig flowers. Other non‐pollinating wasps that lay eggs by inserting their ovipositors from the outside can also develop in syconia. These parasitic wasps may be parasitoids of either pollinating or other non‐pollinating wasps, or form galls in fig flowers or other tissues. Depending on this interaction, parasitic wasps may have various effects on the production of pollinating wasps and seeds. Wasps in the genus Idarnes, which parasitize New World figs (subgenus Urostigma), have an effect on wasp production but not on seed production. Heterandrium spp., which have short ovipositors and lay on external flowers, are infrequent and no effect on seed production has been documented. In the Colombian Andes, Idarnes spp. and Heterandrium spp. are the most frequent parasites of the Ficus andicola — Pegoscapus sp. mutualism, affecting 62 and 43 percent of syconia, respectively. Controlling for other factors that influence wasp and seed production, such as number of foundresses, syconium size and tree, we found that Idarnes reduced pollinator production by almost half but did not reduce seed production, whereas Heterandrium reduced seed production by 40 percent, and marginally affected pollinator production. Our results provide the first clear documentation of Heterandrium spp. impact on fig seed production. Whether the relative abundance of this genus is a generalized phenomenon in montane forest remains to be determined.     

Pollination and reproduction enhance the invasive potential of an early invader: the case of Lythrum salicaria (purple loosetrife) in South Africa

The potential of an alien plant to spread rapidly and colonize new habitat may be related to the mode of reproduction and the ability to attract pollinators. Most studies focus on widespread invasive plants, in which pollinators are rarely limiting. Here, we assess the ability of a recent invader in South Africa, the tristylous Lythrum salicaria to self-reproduce and whether this can explain the delay between introduction and spread. This study was conducted in one of the largest known populations (a total of 7 populations in South Africa) of L. salicaria in the Liesbeek river in the fynbos biome. We assessed the importance of pollinators and autonomous selfing in L. salicaria by comparing seed set between pollinator excluded and naturally pollinated flowers. Overall, 5 pollinators (4 native and 1 alien) were recorded with Cape honeybees and Africa Monarch butterflies the most prominent. Seed and fruit set were significantly higher in open pollinated flowers compared to pollinator excluded flowers. Also, seed and fruit set in pollinator excluded flowers were higher in long and medium morphs compared to short morphs. Germination was high for seeds from pollinator, but also from pollinator excluded treatments. This shows that L. salicaria in South Africa is self-compatible to some extent, but it is frequented by pollinators, significantly increasing seed production. Despite L. salicaria being tristylous, all 3 morphs are present in South Africa and with a huge seed production, this species has the potential to become a major invader of rivers and wetlands in South Africa.

     

PATHOGEN IMPACT ON SEXUAL VS. ASEXUAL REPRODUCTIVE SUCCESS IN ARISAEMA TRIPHYLLUM

Populations of Arisaema triphyllum commonly harbor a systemic fungal pathogen, Uromyces ari-triphylli, which reduces leaf area and leaf longevity. Infected plants produced 42% fewer asexual progeny (cormlets). Furthermore, all asexual progeny from infected parents were themselves infected with Uromyces. Mean seed production of infected plants was only 21% of that among healthy plants. A hand pollination experiment demonstrated that 1) infected male plants can produce viable pollen, 2) the low seed production of naturally pollinated infected females was not due to inadequate pollination, and 3) seed production among healthy female plants was strongly pollinator limited. Seeds from infected and healthy parents had similar viability, and all seeds germinating from both types of parents were uninfected. The contrast in disease transmission to sexual vs. asexual progeny suggests that pathogen attack may be one selective factor favoring sexual reproduction in A. triphyllum populations.     

影响对叶榕及其传粉者繁殖的生态学因素

在西双版纳,分别统计了对叶榕(Ficus hispida)雌花期雌雄果的进蜂量和花后期雌雄果繁殖的多个特征值,以此来探讨自然条件下,影响对叶榕及其传粉榕小蜂(Ceratosolen solmsi marchali)繁殖的因素。结果表明:单果内有效进蜂数量是影响种子生产和传粉榕小蜂繁殖的首要因素,而雌花期进果的传粉榕小蜂并不是都能全部进入果腔传粉或产卵,大部分蜂还未进到果腔就被夹死在顶生苞片层的通道里,能进入雌果内传粉的榕小蜂为(2.72±2.04)只·果^-1,约占总进蜂量的52%;而在雄果里,能进入果腔的蜂量只有(2.08±1.65)只·果^-1,占35%左右。由于雌果内的雌花显著比雄果内的雌花多,结合单果进蜂量雌多雄少的格局,最终单果生产的种子数量 (1 891.63 ± 471.53)比传粉榕小蜂的数量 (367.20 ± 208.02) 多5倍有余。在雌果里,供给传粉的雌花数量与所生产的种子数量之间呈显著的正相关,而没有接受到花粉或不能正常受精的雌花数量与种子数量呈显著的负相关。雄果不仅生产花粉,也是传粉榕小蜂繁殖的场所,在相关于传粉榕小蜂自身繁殖力的因子中,传粉榕小蜂产卵制造的瘿花数量对其种群数量有最大的影响;影响次之的是发育过程中死亡的个体数量,它可降低30%左右的传粉榕小蜂数量;影响排在第三位的是寄主的雌花数量。此外,3类非传粉者的存在,单果内平均可减少30多只传粉小蜂。     

Pollination ecology of Christmas Bells (Blandfordia nobilis): Effects of pollen quantity and source on seed set

The effect of a number of experimental handpollination regimens on the numbers of seeds set by Blandfordia nobilis flowers was assessed. Individuals were found to be self-incompatible and to require pollinator visits to set fruit. Pollen limited the female component of reproduction in the two populations studied while pollen source did not have a significant effect on the numbers of seeds set. Experiments using a stuffed honeyeater indicated that maximal seed set could be achieved after just one probe by the pollinator. Appreciable heterogeneity in flowering phenology, the number of seeds naturally setting and the number of seeds setting as a result of hand-pollinations existed within a small area across a single flowering season.