Locomotion in a sticky terrain
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The mirid bug Pameridea roridulae lives mutalistically on the protocarnivorous plant Roridula gorgonias. The latter resembles an effective, three-dimensional flypaper trap which captures numerous flying insects. We have recently shown that P. roridulae bugs are not trapped by the plant, because they are covered with a layer of epicuticular grease, which is considerably thicker than in other insects. The present study demonstrates that the bugs’ morphology and locomotory characteristics also contribute to their specialisation for life on the adhesive plant surface. A structural analysis of the mirid bug’s attachment system, and an experimental study on its attachment ability were carried out. In traction force tests, maximum forces of 8.8 mN were measured on adaxial R. gorgonias leaves, corresponding to 126 times the bug’s body weight. On smooth surfaces, generated forces were only 47 times the bug’s body weight. Compared to closely related mirid bug species avoiding contact with plant adhesive secretion, P. roridulae is distinctly stronger and heavier, and holds its body close to the plant substrate. Two locomotion strategies on the glandular hairy plant surfaces are suggested for mirid bug species from the tribus Dicyphini: (1) avoidance strategy, characterised by the slim body held at a large distance from the plant surface by using long, slender legs, and (2) defense strategy, where trapping of the heavy bugs, situated close to the plant surface, is overcome by generating strong forces during locomotion and by having a thick anti-adhesive epicuticular greasy layer on the bugs’ cuticle.
KeywordsAttachment Biomechanics Bryocorinae Heteroptera Insect-plant interactions Miridae Traction force Trichomes
South African bugs Pameridea roridulae Reuter (Heteroptera, Miridae, Bryocorinae, Dicyphini) are obligately associated with protocarnivorous plants Roridula gorgonias Planch. (Roridulaceae; Reuter 1907; Dolling and Palmer 1991; Ellis and Midgley 1996; Anderson and Midgley 2002; Anderson 2006). The host plant is densely covered with glandular trichomes of three different types (short, middle-sized, and long tentacle-shaped ones; Fenner 1904; Bruce 1907; Voigt et al. 2009). It is a three-dimensional, meshed, sticky, flypaper trap that has been observed to capture numerous insects of considerable body mass (Marloth 1903, 1910). Nevertheless, P. roridulae live and walk confidently on the sticky plant surface. The surface of these mirid bugs is covered with an anti-adhesive, greasy, epicuticular layer that prevents the bugs’ adherence to the plant secretion (Voigt and Gorb 2008) and enables them to live in a digestive mutualism with R. gorgonias (Ellis and Midgley 1996). Mirid bugs feed on the insects captured by plant trichomes and defecate on their leaves (Marloth 1903; Loyd 1934). The nitrogen in the bugs’ faeces is absorbed, for nutrition, through the thin leaf cuticle of the plant, since the plants themselves produce no enzymes to digest captured insects (Marloth 1910; Lloyd 1934; Ellis and Midgley 1996; Anderson and Midgley 2002, 2003). Furthermore, juveniles of Pameridea are primary pollinators of Roridula’s flowers (Anderson et al. 2003).
Recent coevolutionary studies on mutualistic interactions resulted in phylogenetic and geographical associations, suggesting cospeciation, coadaptation, and long-term coexistence in the Roridula-Pameridea complex (Anderson et al. 2004; Anderson 2006). In host choice experiments with Roridula dentata L. (Roridulaceae) and Pameridea marlothi Poppius (Heteroptera, Miridae), bugs preferred host plants over unrelated host plant species and closely related sister species (Anderson et al. 2004). The presence of an intermediate number of P. marlothi caused positive growth rates in R. dentata (Anderson and Midgley 2007).
Only a few data about mutualistic effects on bug’s fitness and specific adaptations are currently available. Since relationships between insects and plants are highly diverse associations, they need broad studies of various factors and features at different conditions for a better understanding and evaluation (Thompson 1988). Besides genetic, fossil, taxonomic, geographical, ecological, and biochemical evidence, insights into the functional morphology and ethology may indicate associations and coadaptations (Futuyma and Slatkin 1983).
Similar to R. gorgonias and P. roridulae, relationships between mirid bugs and carnivorous plants have been reported from representatives of the plant genera Byblis and Drosera in Australia (e.g. Schuh 1995). These bug species are representatives of the mirid bug subfamilies Orthotylinae and Bryocorinae, which are known to be specialised in living on glandular hairy plants (Reuter 1913; Kullenberg 1946; Falkingham 1995; Dolling and Palmer 1991; Wheeler 2001; Sugiura and Yamazaki 2006; Voigt et al. 2007). Such mirid bugs have been reported to bear elongated, curved, sharp claws and free, rather large pseudopulvilli (Reuter 1913; Wagner 1955). Besides specialised claws, they have slim bodies as well as long, slender legs (Roberts 1930; Southwood 1986; Voigt et al. 2007). In contrast to P. roridulae, other related species have been observed avoiding contact with sticky glandular plant secretions by means of morphological adaptations.
Additionally, mirid bugs may show a particular behaviour. For example, Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae, Dicyphini) stalks along the plant surface touching only trichome tips and stops frequently to groom itself (Southwood 1986; Voigt et al. 2004). For D. errans, non-glandular and glandular hairy plant substrates have been experimentally demonstrated to be important attachment substrates (Voigt et al. 2007), whereas geometrical variables of trichomes (length and diameter) significantly influenced the bug’s attachment ability. Trichomes have been found to provide suitable interlocking sites for attachment and locomotion of this tiny mirid bug. It clings to single trichomes using one part of the paired claw.
Length of anterior leg
Width of anterior tibia
Width of anterior femur
Possibly, not only the anti-adhesive, greasy, epicuticular layer enables these bugs to live on the sticky plant surface, but also other morphological and behavioral characteristics contribute to it′s ability. The stronger build of P. roridulae may result in a larger muscle mass, due to which mirid bugs could generate stronger forces during locomotion on the sticky substrate, where they have possibly to free themselves from trichomes’ viscous secretion. As a specialist species, it is strongly associated with its single host plant (Anderson et al. 2004; Anderson 2006). Similar to related species of Miridae, they have to attach properly to the surface, not only during locomotion and feeding, but also during copulation, molting and oviposition of eggs into the plant tissue (Wheeler 2001).
Thus, the question arises, how do P. roridulae bugs attach and walk on their host plant? Do their attachment devices and attachment ability differ from those of related mirid bugs? Are they specialised for the surface of R. gorgonias? Previously, pretarsal structures in the genus Pameridea have been described to be similar to those of the genus Dicyphus, bearing short, curved claws, triangular pseudopulvilli and a straight, bristle-like parempodia (Dolling and Palmer 1991). However, up to now, no illustrations of these structures are available in the literature.
The present study should contribute to the better understanding of the complex mutualistic relationship between the protocarnivorous plant and the associated mirid bugs, in particular at the interface between the plant surface and insect attachment system. Using light and cryo-scanning electron microscopy (cryo-SEM), we analyzed the pretarsal structures of P. roridulae. Its forces, generated in a traction experiment, were measured on various substrates: glandular hairy adaxial and abaxial leaf surfaces of the bug’s host plant, smooth adaxial and sparsely hairy abaxial leaves of Rumex obtusifolius L. (Polygonaceae) and glass.
Materials and methods
Insects and plants
Shrubs of R. gorgonias (seeded, potted, 1–3 year old) with P. roridulae, were obtained from a private glasshouse culture (Klaus Keller, Augsburg, Germany). They were kept under laboratory conditions during experiments (23.7 ± 1.7°C, 47.3 ± 10.0% RH, 16 h photoperiod), and fed with wingless, adult Drosophila melongaster Meigen (Diptera, Drosophilidae; Zoo-Schöniger, Stuttgart, Germany).
Leaves from plants of Rumex obtusifolius L. (Polygonaceae) at eight-leaf stage were collected from the wayside in a humid mixed forest in Stuttgart-Büsnau (Baden-Württemberg, Germany). Its adaxial leaf surface is uneven because of the prominent venation and irregularly shaped convex epidermal cells and has a maximum height of about 9 μm (Holloway 1967; Gorb and Gorb 2009). The cells are relatively large (50.0 ± 9.04 μm long, 30.7 ± 7.45 μm wide), covered with a cuticle and a smooth, amorphous, epicuticular wax layer (0.1 ± 0.05 μm thick). Sporadically, very sparse small wax crystals occur in some places on the surface. The crystals have irregular scale-like or granular shapes and vary in size (0.5 ± 0.16 μm long, 0.3 ± 0.07 μm wide, and 0.1 ± 0.0 μm thick) (Gorb and Gorb 2009). The abaxial leaf side is roughly similar to the adaxial, however, convex cells are striated and tiny (Holloway 1967).
Observations and structural studies
The attachment positions of five male and five female freely walking P. roridulae to the plant surface were studied (1) visually without optical instruments, (2) visually with a stereomicroscope Olympus SZX 12 with a DF PLAPO 1xPF objective (Olympus Corp., Tokyo, Japan), and (3) using digital recordings. Images were taken using (1) a digital single lens reflex camera Canon EOS 20D combined with the Canon macro lens EF 100 mm, 1:2.8, USM and the Canon macro twin lite MT-24EX (Canon Inc., Japan), and (2) a Nikon Coolpix E995 digital camera adapted to the stereomicroscope with a C-Mount adapter and MDC 2 relay lens MXA 29005 (Nikon Corp., Tokyo, Japan).
To analyze the morphology of the mirid bug′s attachment system and the interaction with the plant surface, a cryo-SEM Hitachi S-4800 (Hitachi High-Technologies Corp., Tokyo, Japan) equipped with a Gatan ALTO 2500 cryo-preparation system (Gatan Inc., Abingdon, UK) was used. Fresh samples of mirid bug legs and plant leaves were cut out using a razor blade, mounted on metal holders by Tissue-Tek® O.C.T.TM Compound (Sakura Finetek Europe B. V., Zoeterwoude, Netherlands), frozen in the preparation chamber at −140°C, sputter-coated with gold–palladium (6 nm thickness) and examined in a frozen state in the cryo-SEM at 3 kV and −120°C.
To visualize in detail how mirid bugs’ claws interlock with trichomes on the host plant surface, leaf samples of R. gorgonias with attached P. roridulae were prepared, clamped perpendicularly on holders, and examined in the cryo-SEM as described above. Additionally, from SEM micrographs of 10 randomly selected pretarsi of adult specimens (males and females pooled together), the inner length of the claw, diameter of a circle fitting the inner curvature of the claw, and length of the setiform parempodia were estimated, using Sigma Scan Pro 5 (SPSS, Inc., Chicago, IL, USA) software.
Traction force experiment
Traction force measurements were carried out according to Gorb et al. (2004) and Voigt et al. (2007). Insects were anaesthetised with CO2 and attached to a 10 cm long human hair with a molten wax droplet. Their forewings were glued together. Bugs were weighed using an analytical balance AG 204 Delta Range (Mettler Toledo GmbH, Greifensee, Switzerland). Following anaesthesia, insects were allowed to recover for 1 h. Then, the free end of the hair was connected to the force sensor.
Fresh leaves were removed from the middle part of R. gorgonias plants and attached to a horizontal glass plate using double-sided tape. Pieces (5 × 5 cm2) were cut out with a razor blade from the intercostal leaf areas of the non-host plant R. obtusifolius. Using a FORT-10 force transducer (10 g capacity, Biopac Systems Ltd., Santa Barbara, CA, USA), the traction force was measured in males and females of P. roridulae. Each specimen was tested (1) walking distally on the adaxial and abaxial leaf surface of R. gorgonias (contact angle of water could not be determined), (2) walking proximally on the adaxial and abaxial leaf surface of R. gorgonias, (3) walking distally on the non-host plant R. obtusifolius (contact angle of water 40–70°, surface energy 35.43 mN*m−1; Gorb and Gorb 2009), and (4) walking on a glass surface (contact angle of water 55°, surface energy 42.9 mN*m−1). The succession of different substrates (1–4) was randomly organised during the experiment. Before the exchange of substrates, bugs were allowed to groom and to walk over KIMTECHScienceTM precision wipes (Kimberly-Clark Europe Ltd, Surrez, UK).
Using AcqKnowledge 3.7.0 software (Biopac Systems Ltd, Goleta, CA, USA), force–time curves were recorded to estimate the maximal traction force produced by a single bug during five consecutive runs on a test substrate. On each plant surface, five males and five females were tested individually. In total, 70 individual tests with 10 different specimens were carried out (N = 7 substrates, n = 10 individual tests). Kruskal–Wallis one-way ANOVA on ranks followed by all pair-wise multiple comparision procedures (Dunn’s test) was applied to determine differences in forces between test surfaces (software SigmaStat 3.1.1®, Systat Software, Inc., Richmond, California, USA). Force measurements in various walking directions on the same leaf surface of R. gorgonias were included because trichomes are oriented distally and thus some anisotropical effects could occur. In contrast to R. gorgonias, the dock plant R. obtusifolius represents a non-host plant having a totally different surface. Since no structural anisotropy was found on dock plant leaf surfaces, traction was tested only for mirid bugs walking distally on the leaf.
The attachment system of Pameridea roridulae
Traction force of Pameridea roridulae
Leaves of R. obtusifolius appear adaxially predominantly smooth, slightly textured by convex cells having sparse cuticular foldings (Fig. 3c), and a few discrete patches of epicuticular crystal wax granules and stomata (Fig. 3d–e). On the abaxial leaf side, convex cells and venation are more prominent. Larger veins are covered with papilla-shaped trichomes (Fig. 3f). Numerous stomata are found (Fig. 3g).
Statistical differences of forces between males and females, generated in the traction experiment on various surfaces (N ♂♂ = 5, N ♀♀ = 5, n = 5). See also Fig. 2
Surface and traction direction
Roridula gorgonias, adaxial leaf side, distal
t = 1.020, P = 0.313
Roridula gorgonias, adaxial leaf side, proximal
t = 1.797, P = 0.079
Roridula gorgonias, abaxial leaf side, distal
T = 761.000, P = 0.017
Roridula gorgonias, abaxial leaf side, proximal
t = 0.477, P = 0.636
Rumex obtusifolius, adaxial leaf side, distal
t = 2.893, P = 0.006
Rumex obtusifolius, abaxial leaf side, proximal
t = 0.561, P = 0.578
T = 756.000, P = 0.022
Mirid bug behaviour
The locomotion mode of P. roridulae and the manner in which it attaches to plants affirm previous reports that this bug does not avoid contact with the sticky sites of the host plant surface (Voigt and Gorb 2008). Rather it frequently touches adhesive plant secretion droplets since it adheres, predominantly, to the trichome base at the lower third of the trichome stem. Thus, the body is held very close to the plant surface, unlike related species. For example, Dicyphus errans adheres to the glandular surface of Ononis sp., positioning the long tibiae and the especially long hind femuri almost vertically to the plant surface (Southwood 1986). Only the tarsal apexes come in contact with the plant surface and the body is held far away from it.
Pretarsal adaptations to the trichome-covered terrain
Although the pretarsus of P. roridulae bears similar structures found in related bryocorine bug species (Schuh 1976; Cobben 1978; Wheeler 2001), claws in P. roridulae are distinctly shorter (mean length 23.1 μm) and thicker, e.g., compared to those of the mirid bug D. errans (mean length 74.0 μm, Voigt et al. 2007). The body length is similar in both mirid bug species (Table 1), but the body of P. roridulae appears stronger and thicker. The mean female body mass in P. roridulae is 7.0 mg corresponding to 1.8 times that of the female D. errans. The body mass, in combination with trichome stem flexibility, may explain why the bugs P. roridulae predominantly cling to the basal part of trichomes. Knowing trichome spring constants and bending behaviour (tentacle-shaped: 0.02 Nm−1, bending at the tip; medium-sized: 0.08 Nm−1, bending at the tip; short: 0.95 Nm−1, bending at the base Voigt et al. 2009), the trichome’s deflection, caused by the load of a mirid bug, can be estimated. Since the geometry of trichomes is similar, the deflection of short trichomes may also be considered as for the base of tentacle-shaped ones. Assuming a resting female (7 mg) having all six legs clinging to trichomes, a tentacle-shaped trichome would bend 1 mm at the tip but only about 20 μm at the base. For comparison, a female D. errans (3.8 mg) would cause a trichome deflection of 250 μm at the trichome’s tip and about 7 μm at the base. Less trichome bending allows more effective bug attachment, as shown in previous studies on D. errans, where long and thin trichomes with a high aspect ratio resulted in lower traction forces (Voigt et al. 2007).
The heavier body of P. roridulae led us to assume a generally larger portion of muscles enabling this bug species to generate stronger forces compared to lighter related species. The assumption is confirmed by traction forces measured with P. roridulae on various surfaces. Traction force corresponds to the friction between insect pretarsi and the substrate. The proper adherence to trichomes and applying a pulling force to them while remaining in a certain position, is important in behavioural situations where mirid bugs’ bodies move back and forth or up and down the substrate (Kullenberg 1946; Voigt et al. 2004; Voigt 2005). (1) During sucking the head and thorax are repeatedly moved up and down, supporting the rostrum bending inside the prey. (2) During the final phase of copulation the male and female couple their abdominal tips, heads facing in opposite directions, and move their bodies back and forth, as in a “tug of war”. (3) The oviposition requires strong up and down movements of the female abdomen and therefore strong attachment to the plant substrate in order to insert the saw-shaped ovipositor into the plant tissue. (4) Molting nymphs and emerging imagines free themselves from old cuticle by pulling their body distally. For P. roridulae, the challenge is to perform these actions even upon its adhesive host plant terrain. Possibly, for this reason P. roridulae may generate higher traction forces (126 times higher than the body mass) than the related D. errans (34.2 times higher than the body mass) on both a glandular hairy plant surface as well as on glass (P. roridulae: 47, and D. errans: 6.1 times higher than the body mass). The latter values indicate that mirid bugs may also adhere sufficiently to microstructured and smooth surfaces such as those of R. obtusifolius and glass. Thus, smooth sites on R. gorgonias (trichome-free spaces on the leaf and wide, non claw-fitting trichome stems) provide suitable attachment substrates for P. roridulae bugs. Considering the lowest generated force on a smooth glass surface (females: 0.7 mN, median), a bug may still free itself from 10 tentacle-shaped trichomes adhering coincidentally to the bug’s epicuticle (median adhesion force of a single trichome: 0.07 mN, Voigt and Gorb 2008).
Pameridea roridulae bugs were observed predominantly interlocking to trichomes using claws. Although their claws are much shorter (average length 23 μm) than those of D.errans (74 μm), the average diameter of an ideal circle fitting the concavity of claws in both species is about 16 μm. Since mean stem diameters of trichomes on the surface of R. gorgonias are from 75 μm in median-sized to 120 μm in tentacle-shaped ones (Voigt et al. 2009), claws of P. roridulae may only interlock with some sites of these trichome stems. Nevertheless, on rough surfaces, higher traction forces were measured compared to smooth ones. For example, on the abaxial leaf side of R.obtusifolius, small papilla-shaped trichomes provided interlocking sites for claws and therefore, a stronger traction force of mirid bugs was recorded than on the smooth adaxial leaf side. P.roridulae bugs performed best on their host plant. Since forces did not differ significantly between leaf sides and pull direction, leaves of R.gorgonias, in general, can be assumed to be a suitable attachment substrate for male and female bugs.
Sexual dimorphism in traction force generation
Compared to females, males generated significantly higher forces on the abaxial leaf side of R. gorgonias, on the adaxial leaf side of R. obtusifolius, and on glass. Differences between sexes have been previously found in traction force experiments with leaf beetles Chrysolina polita L. (Coleoptera, Chrysomelidae; Stork 1980) and ladybird beetles Coccinella septempunctata L. (Coleoptera, Coccinellidae; Gorb et al. 2008). Males of both species adhere stronger to smooth surfaces, whereas females performed better on rough ones. However, attachment systems of beetles (hairy) and mirid bugs (smooth) differ completely and cannot be compared outright in the context of our results (Beutel and Gorb 2001). Since significances between male and female force values occur on predominantly smooth substrates, one may conjecture that differences in material properties between male’s and female’s pseudopulvilli exist. These pad-like attachment structures in mirid bugs, adhering to smooth surfaces, need further micromechanical analyses for better understanding of their functionality depending on sex and species.
Two locomotion strategies of mirid bugs
To what extent the hypothesized strategies may be the case for other mirid bug species, is difficult to appraise, because neither detailed comparative nor experimental studies have been previously carried out. Representatives of the mirid bug subfamilies Orthotylinae and Bryocorinae are generally known to be specialised in living on glandular hairy plants (Reuter 1913; Kullenberg 1946; Cassis 1984; Falkingham 1995; Dolling and Palmer 1991; Wheeler 2001; Sugiura and Yamazaki 2006; Voigt et al. 2007). Several of them even live on insectivorous plants of the genera Drosera and Byblis (e.g. China and Carvalho 1951; China 1953; Southwood 1986; Falkingham 1995). These bugs also feed on trapped insects, but unlike P. roridulae, they avoid the contact with the sticky surface of their host plants (Russell 1953).
Only one previous report on different modes of locomotion on glandular plant surfaces is found in literature, however, for other true bug families than Miridae (Schwoerbel 1956). Stilt bugs Gampsocoris punctipes Germ. (Heteroptera, Berytidae) avoid the contact with glandular plant secretion of the spiny restharrow Ononis spinosa L. (Fabaceae) by means of their slim, small body and long, slender legs, whereas juveniles Corizus hyoscami L. (Heteroptera, Rhopalidae) appear stronger and walk unhamperedly between trichomes like a “snowplow” on the same plant surface (Schwoerbel 1956). Thus, for non-mirid species, the avoidance strategy is not only characteristic of generalists, because the specialist G. punctipes is obligatory associated with O. spinosa.
Pameridea roridulae lives in a complex, three-dimensional, sticky terrain where it moves without hindrance. In contrast to related species within the tribe Dicyphini of the family Bryocorinae, P. roridulae do not avoid adhesive secretions but rather walk between glandular trichomes and touch them very frequently. Previously, an anti-adhesive epicuticular layer protecting mirid bugs from being captured by the adhesive plant secretion has been described. The present results show that the mode of attachment and locomotion on the plant surface also contributes to the specialisation of P.roridulae to a life on the protocarnivorous flypaper trap R.gorgonias. There are direct, biomechanical interactions at the interface between the plant surface and insect attachment system. Dicyphine bugs use claws to cling to trichomes and use pad-like pseudopulvilli for adhesion to smooth hairless patches or to thick trichome stems. This strategy allows them to generate distinctly higher traction forces if compared to other mirid bug species. Thus, P.roridulae may even overcome contact with the adhesive secretion of numerous trichomes. Based on available data, we have hypothesized, here, two strategies of locomotion and attachment on glandular hairy plant surfaces within the mirid bug tribus Dicyphini: (1) avoidance strategy, characterised by the slim body held at a large distance from the plant surface by using long, slender legs, and (2) defense strategy, where trapping of the heavy bugs, situated close to the plant surface, is overcome by generating strong forces during locomotion and by having a thick anti-adhesive epicuticular greasy layer on the bugs’ cuticle. The proper attachment and locomotion on the host plant surface may result in the better fitness of insects. Additionally, living on an adhesive plant trap has several long-term adventages for P. roridulae (e.g., protection, less competition, permanent food supply). The defense strategy could be specific to Pameridea species indicating specialized adaptations of bugs to the plant surface, which would support previously suggested coevolutionary processes in the Roridula-Pameridea complex. Further comparative broad screenings of pretarsal structures combined with attachment experiments on different substrates and analyses of epicuticular grease, including various species of mirid bugs and glandular hairy plants, will shed light on the evolutionary tendencies in this insect-plant mutualism.
Klaus Keller (Augsburg, Germany) is kindly acknowledged for provision of plants and bugs. The bug species was determined by Kurt Arnold (Geyer, Erzgebirge, Germany). Victoria Kastner (Max-Planck Institute for Metals Research, Stuttgart, Germany) provided linguistic corrections of the manuscript. This study was supported by the Federal Ministry of Education and Research, Germany (BMBF project Inspirat 01RI0633D).
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