The same site was sampled previously in — and also showed the presence of Bombus spp. Forup et al. However, the wet bog itself possesses limited resources to attract bees other than the pitcher plants. The areas where the pitchers are growing are NVC classified M2, so the only flowers in and around the pitchers are occasional bog asphodel Narthecium ossifragum , oblong-leaved sundew Drosera intermedia and round-leaved sundew Drosera rotundifolia Rodwell There will also be the occasional cross-leaved heather Erica tetralix in the surrounding area outside the M2 classified area.
Local monthly weather data suggest that and were quite similar for June and July in terms of temperature, sunshine and rainfall MetOffice However, the weather data summarise months and as such does not have the resolution to look for extended periods of dry and wet weather. Extremes in weather possibly impacted bumblebee foraging behaviour, with hot dry weather maybe inducing water foraging from within pitchers Ferry and Corbet and wet weather inhibiting foraging altogether Moret and Schmid-Hemplel In addition, dry weather may reduce the efficiency of pitcher plant trapping due to the absence of trapping liqueur or reducing surface slipperiness Newell and Nastase ; Bauer et al.
The finding that there were a greater number of bumblebee captures in July than in June in is likely to be linked to the abundance of bumblebees, as colonies of the bumblebee species captured reach their maximum sizes and demand for resources in July and August Prys-Jones This is also the time at which these bumblebee species produce their sexually reproductive individuals, queens and male bees Prys-Jones It is also likely that there would have been a greater number of male bumblebees around in the July period and in addition these males would have been outside the nest, searching for queens Prys-Jones The flowers of Sarracenia purpurea, which bloom in June and July in the UK, could also be attracting bumblebees.
The bumblebee Bombus affinis has been recorded to take large pollen loads from S. If the same pollination occurs in the UK, S.
Sarracenia: Native Pitcher Plants
Bumblebee colonies store very few resources, making them sensitive to changes in resource availability; therefore, bumblebee colonies are at their most vulnerable when they are founding in spring and when their colonies are at maximum size during the production of sexual brood Williams and Christianson ; Westphal et al. Although this study did not explore the effects of S. This is because S. At Lower Hyde Heath, this reduction in viability in the second year is particularly pronounced as the pitchers are being winter grazed by wild Sika deer Anita Diaz Personal Observation.
For a conflict to occur, plant fitness must depend on pollinators and pollinators must also be possible prey. In addition, many pitcher plants use temporal separation between flowering and pitcher production to avoid predating upon their pollinators Anderson and Midley Sarracenia purpurea in the UK overlap their pitcher and flower production. Previous studies have shown that Sarracenia invertebrate captures do not change or decrease with increased plant density Cresswell However, this study observed that more bumblebees are captured by pitcher plants in dense patches.
This may be driven by bumblebees foraging for nectar or pollen and using optimal foraging strategies, as insects preferentially visit bigger floral patches Thomson ; Schmid-Hempel and Speiser ; Grindeland et al. The trapping efficiency of pitcher plants could also have an effect on bumblebees foraging interactions, whether that is the general efficiency of the pitchers Newell and Nastase or an intermittency in their effectiveness Bauer et al. In a study by Newell and Nastase the capture efficiency of S. This means approximately only 1 in invertebrates that visit the pitchers were actually caught.
From their experiment, Newell and Nastase estimate that pitcher with five separate pitcher traps would be likely to catch one prey item every three days Newell and Nastase Newell and Nastase also found that ants, although the most abundant prey item in pitchers, were also the one with the lowest capture rate, at 0.
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In a similar scenario, pitcher plants could be providing bumblebees with a substantial nectar resource Deppe et al. For confirmation of this, observations of live bumblebee and pitcher plant trap interactions need to be obtained. It has been reported in some pitcher plants that there is an intermittent nature to their trapping Bauer et al. In the Nepenthes spp.
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In the natural environment, this results in the intermittent effectiveness of traps. During dry, inactive periods, it is probable that invertebrates can feed at the pitchers with a much lower risk of becoming trapped. In the case of the ants in the study, creating recruitment trails to the inactive, dry pitcher plants.
This is adaptive for the plant as when its traps become active, it traps returning and recruited insects Bauer et al. Whether Sarracenia purpurea captures more effectively with a wet surface was not tested in this study, but the presence of water within the traps is known to be important for prey capture and retention Newell and Nastase During dry periods, it is plausible that bumblebees and other insects could be feeding from the plants at a much lower risk level.
It is of interest that male bumblebees are being attracted to and trapped in pitcher plants despite only being driven to forage for themselves Goulson and they would mainly be attracted by the nectar not the pollen from flowers. The distribution of bumblebees in pitchers did not indicate an effect of gender on capture. There was no indication that the opposite or same sex attracted others into the traps. Males are reproductive units for colonies unlike the workers Wilson , although workers do contribute indirectly to the colony fitness through foraging and late season male production Free et al.
Laboratory-reared colonies of Bombus terrestris have been known to have an average of This study caught 25 males in a sample of the Lower Hyde Heath pitcher population. It is not possible to estimate the impact of the entire population of pitchers in terms of bumblebee consumption as it is almost impossible to quantify the numbers of pitchers. It is unknown how many colonies the sampled bumblebees come from, as many of our captured bumblebees could be sisters from the same colony and there are no accounts of the density of bumblebee nests in wet heathland areas.
The results show there were two representative species for males and six for females.
In order to ascertain the number of colonies, the plants would have been affecting and sistership would need to be evaluated using microsatellite markers Knight et al. The observation of high instances of multiple bumblebees in pitchers and low numbers of single captures seems at first counterintuitive, for if a bumblebee observes another visiting an inflorescence, then that resource is likely to be depleted, and therefore not worth visiting immediately Goulson However, pitcher plants do not fit a standard flower format and this may result in bumblebees following others to pitcher plants due to the novelty of the resource; it has been suggested that social information from conspecifics and intraspecifics could be adaptive when it alluded to a novel resource Worden and Papaj ; Kawaguchi et al.
This interpretation of bumblebee distribution is speculative in terms of foraging on pitcher plants because we do not know the proximity of events in time, only that the distribution of bumblebees is not normal or random. Current interpretations are based on data about dead bumblebees. Observations of live interactions with pitcher plants are needed to affirm the above speculations.
It is almost impossible to quantify the effect that the Sarracenia purpurea population has on the native bumblebees at Lower Hyde Heath as we would need to know how many colonies were present and how their reproduction was affected. However, this study does show that bumblebees are being consumed by the pitcher plants and this is not consistent over years or over the months of June and July Figs. In this study, none of the bumblebee species caught were considered threatened or rare by the Bumblebee Conservation Trust This study also produced evidence that the bumblebees could be using the pitcher plants as a resource as bumblebees appear more attracted to dense patches of S.
These native flowering plants would not recruit a large number of foraging bumblebees compared with the resource rich heathland outside of the mire Ballantyne et al. The capture success per invertebrate interaction of Sarracenia purpurea has been reported as about 1 in Newell and Nastase This means that the majority of bumblebee interactions with pitcher plants could be beneficial to the bumblebees.
Considering the isolated nature, slow dispersal Ellison and Parker ; Walker and rarity of such populations 21 were known of in the British Isles in Walker , even in a high consumption year the effect of S. To conclude, the invasive pitcher plant Sarracenia purpurea preys upon native Bombus spp.
New plants grow from seeds, but flytraps also send out horizontal, underground stems that develop into new plants—clones of the parent plant. Clones can be split off from parent plants to start new Venus flytraps. To stay healthy, Venus flytraps need the same conditions as those in their natural habitat: poor, acidic soil; wet roots; high humidity; and full sun. Saturating the soil with deionized water is important; tap water contains trace minerals that will cause the plants to decline or die.
During the growing season, a Venus flytrap needs only a couple of small bugs or slugs each month. Plants go dormant and die back in the winter, but new growth sprouts in spring. Like breeds of dogs, cultivated varieties called cultivars are the same species, but they are propagated specifically for certain characteristics, such as size and color.
Sarracenia: Native Pitcher Plants - Brooklyn Botanic Garden
Growers have developed dozens of cultivars, with colorful names like "Maroon Monster," "Jaws," "Werewolf," and "Giant Clam. While the Venus flytrap is a successful hunter, it faces threats of its own. Much of its wetland habitat has been converted for urban development; fire suppression has altered the environment, and for years collectors dug up and sold the botanical wonders. The result is that these unique plants are endangered. With a range of only a square-mile area in North and South Carolina, a single disaster could threaten the existence of the natural, wild population. There is hope, however.
But poaching illegal collection remains a threat. If you decide to grow a Venus flytrap, you can help by purchasing your plant or seeds from a reputable grower. Spring, summer, and fall are the best times to view the Venus flytraps at the Zoo, as they are dormant during the winter. Today, approximately species of carnivorous plants are known, almost half of which belong to the adhesive flypaper trap type, including ca.
Besides the straight forward predator-prey relationship and possible pollinator-prey conflicts [ 5 , 6 ] , several commensalistic relationships have been described between carnivorous plants and animals, mainly arthropods. Almost all pitcher plants i. New World Sarraceniaceae and carnivorous Bromeliaceae, and Old World Nepenthaceae and Cephalotaceae appear to have commensal animal species infauna living in the phytotelmata i.
The pitcher inhabitants range from bacteria to large arthropods such as freshwater crabs, and vertebrates such as frogs, which feed on captured prey or other infauna, depending directly or indirectly on the prey trapped by or merely attracted to these plants [ 7 — 19 ]. Although often ignored in the literature, interactions between animals and carnivorous plants not forming phytotelmata are more frequent than previously thought, especially in carnivorous plants with adhesive traps, which are known to be home to several arthropods that move freely between the sticky tentacles on the leaves.
Adults of the family Syrphidae Insecta: Diptera are commonly called flower- or hoverflies. They are conspicuous anthophilous Diptera, often mimicking stinging bees or wasps in coloration, appearance and behavior [ 31 , 32 ]. Flower flies are frequently observed on various types of flowers that are often used as mating sites and energy sources, most adults feed on nectar or pollen or both [ 33 — 35 ].
Syrphid larvae are found in various habitats and have diverse feeding habits [ 36 ], including species predatory of soft-bodied arthropods, scavengers, saprophages in litter and decaying wood, coprophagous, phytophagous, aquatic detritus feeders, or specialized inquilines in nests of social insects, such as ants, termites, wasps, and bees [ 37 , 38 ]. Approximately species of flower flies are currently recognized [ 39 , 40 ] and circa one third occur in the Neotropical Region, the richest biogeographic region in terms of taxa and one of the centers of biodiversity of Syrphidae [ 39 , 41 — 43 ].
The large genus Toxomerus is a monophyletic group of predatory flower flies from the subfamily Syrphinae endemic to the New World [ 39 , 44 ], and it is one of the largest and most abundant genera of syrphids in the Neotropics [ 45 , 46 ]. The genus comprises more than known species, mostly from Central and South America, with only 16 species occurring in the Nearctic Region [ 39 , 42 , 47 ].
In Brazil in particular, 36 species of Toxomerus are recorded [ 48 ]. Adults have been reported as floral visitors feeding on pollen and nectar of a wide range of plants, including Drosera [ 49 , 50 ]. Most Toxomerus larvae have been reported to be predators, a feeding mode assumed to be the norm within this genus, as it is in the majority of Syrphinae [ 56 ]. However, there are some exceptions in this subfamily, with zoophagous larval habits of some taxa e. Larvae of at least three Toxomerus species have been discovered to be pollen feeders of several plant families [ 52 , 60 ].
The larvae were observed to feed on prey captured by the adhesive traps of Drosera , but apparently only after the trapped insects were dead. Eventually, the larvae would pupate and their green to brown-black pupae were seen hanging from the lower leaf surfaces of the sundew plants.
Unusual Facts About Pitcher Plants
The larval biology of this syrphid species was completely unknown until now, and no dipteran inhabitants of Drosera had been reported yet. The field study did not involve endangered or protected species. Pupae were kept in glass vials with drilled lids, at room temperature, in the dark. Preserved puparia were studied and compared with the larvae and puparia of other Toxomerus species, as well as all known preimaginal descriptions in the literature [ 52 , 60 , 63 — 65 ]. Debris adhered to the puparial integument was removed by placing the specimens in an ultrasonic cleaner P-Selecta Ultrasons 6L for a few minutes.
In the case of pupae, cleaned specimens were examined with SEM but using the less destructive variable-pressure low vacuum mode. The positions of the sensilla are numbered sequentially from the dorsal to the ventral surface for each segment [ 36 ]. Whole specimens adults and larvae were used for DNA extraction.
Amplified DNA was electrophoresed on 1. The sequences were edited for base-calling errors and assembled using Geneious version 7. Larvae and pupae were observed on six different Drosera species at several locations Fig 1 ; Table 1. DNA barcodes were obtained for four adults and one L3 larva, each of nucleotides long. Two different haplotypes were found among the obtained DNA barcodes, with an uncorrected pairwise distance of 1. This corroborates that larvae and pupae taken from the Drosera plants belong to the same species, T. Larvae on the glandular lamina of Drosera graomogolensis , Botumirim, Minas Gerais note the larval posterior spiracles in C.
Length 8—9 mm, maximum width 1. Oval in cross-section with a flattened ventral surface, tapering anteriorly and slightly truncate posteriorly Fig 2A. Dorsal habitus wrinkled, all segmental sensilla are much reduced, papilliform and without segmental spines Fig 2A, 2E and 2G.
Dorsal surface smooth, without integumental vestiture except the dorsal surface of prothorax. Posterior breathing tube short, spiracular plates on a slightly projecting fleshy bar and not joined by sclerotization Fig 2A. Head much reduced Fig 2B and 2C , mouthparts adapted for piercing-feeding [ 68 ] with distinctive features of predacious syrphid larvae. Lateral margins of mouth present a pair of triangular pointed sclerites only slightly sclerotized. Mandibles slender, extended anteriorly into the fleshy projections on which antenno-maxillary organs are situated.
Head skeleton with labrum and labium strongly sclerotized and sharply pointed, which are curved respectively dorsal and ventral. Antenno-maxillary organs well developed Fig 2C and 2D , located on fleshy projections and separated by a groove between them acting as a guide for the retractile apex of the head skeleton. Seven pairs of locomotory prominences present on abdominal segments 1—7. Prolegs with a band of small backwardly directed spicules just before the sensilla 11—9 , aggregated in a polygonal pattern Fig 2E and 2F.
A second band of small backwardly directed spicules aggregated in a polygonal pattern on fold just behind the prolegs Fig 2F. Length 5—6 mm, maximum width 1. Pear-like, sub-cylindrical in cross-section. Anterior extreme truncated, slightly tapering posteriorly and flattened ventrally. Dark green coloration, similar to pupae of Toxomerus floralis [ 60 ]. Integumental vestiture and segmental spines absent. Color of empty puparium light brown. Posterior breathing tube completely sclerotized, including the projecting fleshy bar that joins the spiracular plates Fig 2H.
Although a large number of Toxomerus species have been described, biology and feeding habits of only 13 species are known, and only five of them have some data on preimaginal morphology [ 52 , 60 , 63 ], making Toxomerus one of the poorest known genera of Syrphinae [ 39 ]. Most of these descriptions lack diagnostic characters or are very general, and chaetotaxy studies of Toxomerus are only present in a couple of publications [ 52 , 64 ].
Based on these previous works and the present study, a diagnostic characteristic for Toxomerus larvae may be the disposition of the spiracular plates, which are on a slightly projecting fleshy bar and are not joined by sclerotization Fig 2A , as well as the pattern of the spiracular slits, with slits II and III clearly separated from slit I Fig 2F see Fluke [ 65 ] for an explanation. The larva of T. Another diagnostic character is the almost total absence of ornamentation on the dorsal surface, with the segmental sensilla reduced to very small papillae and without setae Fig 2G.
The reduction of ornamentation might be related with its mode of living, as a smooth body surface could facilitate the movement on the glandular adhesive leaves of Drosera. The well-studied larvae of T. The pointed and heavily sclerotized ends of the labrum and labium of T. The labrum and labium protrudes along the groove of the dorsal lip and pierces the prey. Nevertheless, the cephalopharyngeal skeleton of T.
These features are the dorsally curved apex of the labrum and ventrally curved apex of the labium. These characteristics are shared with phytophagous species such as Fazia micrura and Toxomerus apegiensis. According to some authors [ 52 , 59 ] these features may be adaptations to a pollen- feeding mode of the larvae, and the outwardly curved labrum and labium assist in breaking into the flowers of the host plant to access pollen.
These features have also been observed in T. Larvae of different sizes were observed on the lower and upper surfaces of the Drosera leaves however usually not more than a single larva on a small percentage of plants per population , where they crawled freely and did not appear to adhere to the viscous water-based mucilage secreted by the glandular emergences Fig 1A—1E. Apparently, this species spends its entire larval life on the leaves of the sundew. Most often, the larvae were seen moving, resting, or feeding among the glandular emergences of the sundew leaves, where they are well-camouflaged on Drosera species with yellow-green leaves Fig 1E , and where they fed on the immobilized or dead prey captured by the sundews.
The return of nutrients to the plant from larval excretions is not likely, as Syrphinae larvae do not defecate during their feeding period until they pupate which, in T. Therefore, the larvae live on the plant as so-called kleptoparasites following the definition of Hamilton [ 69 ] , as they abstract part of the arthropod prey that was caught by the plant for its own nutrient supply.
When disturbed, the larvae crawled on the lower surface of the leaves, or towards the base of the leaves, into the center of the sundew rosettes. Pupae were found attached to the lower non-glandular leaf surfaces of D. Dynamic fluctuations of larval abundance were observed at some sites, where Toxomerus larvae were sometimes not found in sundew populations where they had been noticed in previous years. This suggests that there may be certain times of the year when larvae are predominately present, although no pattern has yet been identified.
Generally, larvae were observed on Drosera leaves both during the dry and wet season Table 1. However, this may vary according to geography, host sundew species, available insect prey and possibly even Toxomerus species in case further species other than T. Kleptoparasitism, i. Toxomerus is also not the first reported syrphid having larvae as inhabitants of carnivorous plants in general.
Larvae of the Old World genus Nepenthosyrphus Syrphidae: Eristalinae develop inside the pitcher trap fluid of Nepenthes in South-East Asia, where they are aquatic sit-and-wait predators of other pitcher infauna [ 13 , 73 , 74 ]. Several examples of kleptoparasitic and commensalistic behavior are known where predators feed on immobilized insects captured by sticky plant surfaces, including on carnivorous plants. Most well-known examples involving insects are capsid bugs Hemiptera: Miridae , ranging from opportunistic feeders to mutualistic symbionts [ 4 , 27 , 75 , 76 ].
The abundance of dead and decaying animals turns such traps into attractive habitats for different organisms. This is especially true for carnivorous plants with adhesive traps, such as Drosera , where prey is presented more or less freely exposed on the leaf surfaces, although the leaf blades of some species are able to fold over their prey to reduce loss from rain, commensals and kleptoparasites [ 1 , 4 ]. Interestingly, the larvae of Toxomerus were observed most frequently on species with erect, less mobile laminae e. With the exception of the small-sized D. Larger sundew species may generally capture more and larger prey, offering a more stable and safe environment for the larva, but it is also possible that, contrary to rosetted Drosera species with leaves flat on the ground, those with semi-erect leaves may either offer more exposed oviposition sites for the adult flies, or better protection from ground-dwelling predators.
Although oviposition of T. Similarly, the herbivorous caterpillars of the sundew plume moth Buckleria hatch from eggs deposited by the adult moths on the non-glandular parts of its host plant Drosera , namely flower scapes, seed capsules or petioles [ 77 ]. Due to the low dispersal capacity of the syrphid larvae, the choice of oviposition location is crucial for predatory syrphines, because the quality of oviposition sites can greatly affect the progeny growth and the survival of the offspring [ 78 ].
A targeted oviposition on the host plant of the preferred prey is known from many aphidophagous syrphids, but several factors may affect the choice of the oviposition site [ 79 ]. This is also the case with the Toxomerus larvae observed on Drosera leaves, which are well camouflaged at least on those sundew species with greenish leaves Fig 1E.
The viscoelastic, aqueous polysaccharide mucilage secreted by Drosera glands [ 1 , 80 , 81 ] has only a limited retention capacity, which delimitates possible prey size for the plant as it allows larger, more vigorous insects to escape from the sticky traps [ 82 , 83 ]. This limited retention capacity is probably also what enables the apodal Toxomerus larvae to freely move on the adhesive sundew leaves. Further, syrphid larvae secrete a watery fluid that lubricates their ventral body surface for movement [ 38 ]—this fluid secretion might also prevent the larvae from adhering to the Drosera glands.
For locomotion on sticky surfaces, the strength of viscoelastic glue also depends on animal dynamics [ 87 ], hence the ability to move through sundew mucilage could also rely on a special locomotion behavior of the larvae. Little is known about locomotion of Toxomerus larvae in general in order to have enough data for comparison, and the larvae of T.
The Toxomerus larvae described here are also apparently not adversely affected by the numerous digestive enzymes present in the mucilage of Drosera. This is not surprising due to the general design and cuticle of acephalous dipteran larvae—a fact that is well-known from various other dipteran larvae including syrphids which live in hostile, digestive fluids such as acidic vertebrate stomach fluid or pitcher plant digestive fluids [ 13 , 88 , 89 ].
Adlassnig et al. However, not only do commensals and kleptoparasites live on Drosera , as summarized here, but also arthropod herbivores such as caterpillars [ 77 , 91 ], and phytoparasites such as aphids [ 92 , 93 ] are frequently encountered feeding on Drosera , despite the phytochemical defenses. Usually, predatory Syrphinae larvae feed on relatively immobile or slow moving, soft-bodied prey such as aphids or immature stages of other arthropods [ 36 , 51 ].
Thus, it is not unexpected that immobilized arthropods stuck to adhesive plant surfaces would prove to be an easily exploitable food source. The adaptation to new food sources might have become necessary in tropical latitudes, as aphids, the predominantly preferred prey of predatory syrphid larvae, are largely absent in the Neotropics [ 94 ]. This might have driven predatory Neotropical syrphids to evolve different, alternative feeding strategies exploiting an unusually wide range of prey [ 95 , 96 ] and other available food sources such as pollen-feeding or phytophagy [ 52 , 59 ].
Larvae of Toxomerus basalis likely feed on any available insect prey captured by the sundew leaves, although the majority of the Drosera prey spectrum identified thus far from the few Brazilian species studied consists mostly of small to medium sized adult midges, mosquitos and gnats [ 61 , 97 ]. It is therefore likely that the larval diet of T. Although the larval biology of only a handful of Toxomerus species is known, the diversity of prey taxa is extraordinary [ 51 , 53 — 55 , 98 ].
The larvae of at least one species of predatory flower fly feed on adult diptera [ 96 ], and larvae of a few species including Toxomerus geminatus prey on larvae of small dipterans, butterflies or beetles [ 51 , 98 ]. However, all known predatory syrphine larvae studied thus far feed on living prey. Here, the first Syrphinae larva feeding on immobilized or dead prey is reported. The evolutionary scenario for the genus Toxomerus is even more fascinating after Jordaens et al.
It is possible that Toxomerus species with larvae living on Drosera and other viscous plants are more common and widespread than what we have observed. It is also probable that the larvae may occur on more sundew species in Brazil and South America, and that more than one species of Toxomerus is involved.
Similar syrphid larvae have casually been observed on two different species of the glandular-adhesive, non-carnivorous genus Chamaecrista Fabaceae: Caesalpinioidae in Minas Gerais state. We are confident that T. This is the first record of dipteran larvae living as kleptoparasites of a sticky carnivorous plant, and it is the first report of a syrphid species using this unique feeding strategy. Thus far, the knowledge of Neotropical carnivorous plant infauna was limited to pitcher plants the sarraceniacean genus Heliamphora and the carnivorous bromeliads Brocchinia and Catopsis [ 9 , 99 , ].
Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract A new interaction between insects and carnivorous plants is reported from Brazil. Introduction Carnivorous plant-animal interactions Carnivorous plants attract, trap and digest animal prey, benefitting from the end products of digestion in overall growth [ 1 , 2 ]. Predatory flower flies Adults of the family Syrphidae Insecta: Diptera are commonly called flower- or hoverflies.