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1 December 2003 Lubber grasshoppers, Romalea microptera (Beauvois), orient to plant odors in a wind tunnel
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Abstract

We tested the response of individual adult lubber grasshoppers in a wind tunnel to the odors of 3 plant species and to water vapor. Grasshoppers moved upwind to the odors of fresh-mashed narcissus and mashed Romaine lettuce, but not to water vapor, or in the absence of food odor. Males and females showed similar responses. Upwind movement tended to increase with the length of starvation (24, 48, or 72 h). The lack of upwind movement to water vapor implies that orientation toward the mashed plants was not simply an orientation to water vapor. These results support a growing data base that suggests that grasshoppers can use olfaction when foraging in the wild.

Introduction

How grasshoppers find their food has long been of interest to researchers (Uvarov 1977). Acridoids are thought to use visual, chemical, and tactile senses when searching for, identifying, biting, and accepting food (Chapman 1988, 1990). For example, many grasshoppers orient visually to emergent plants, certain colors, or to two-dimensional images drawn on paper; vertical contrasting stripes are especially attractive (Kennedy 1937, 1939; Williams 1954; Wallace 1958; Mulkern 1967, 1969; Bailey & Harris 1991; Szentesi et al. 1996).

Evidence that some grasshoppers can use olfaction to orient to food plants comes from many sources (Watson & Bratley 1940, Volkonsky 1942, Slifer 1955, Dadd 1963). In the field, grasshoppers sometimes move upwind toward odorous plants, synthetic plant chemicals, carrion, or baits (Boppré et al. 1984; Modder 1984; Bomar & Lockwood 1994b,c; Lockwood et al. 2001). For example, Chapman (1990) observed a marching band of Chortoicetes terminifera nymphs turn upwind toward fresh grass. Also, grasshopper antennae possess numerous olfactory sensilla (Kang & Chen 1997, Bland 1989, Blaney & Simmonds 1990, Chen & Kang 2000) that respond electrophysiologically to a range of plant odors, including the green leaf odors (Blust & Hopkins 1987, White & Chapman 1990a, Dickens et al. 1993, Kang et al. 1995, Hansson et al. 1996, Njagi & Torto 1996, Chen & Kang 2000). A smaller number of olfactory sensilla are found on grasshopper palps (Blaney 1977, Blaney & Simmonds 1990), and apparently also on all parts of the legs (Slifer 1954, 1956). In addition, rates of turning, antennation, palpation, and biting often increase in the presence of food odors (Kennedy & Moorhouse 1969, Mordue 1979, Chapman 1988, Chapman et al. 1988). Grasshoppers will also retreat from the odors of deterrent plants or chemicals (Kennedy & Moorhouse 1969, Chapman 1974). However, the most convincing evidence that grasshoppers use olfaction in food search comes from wind tunnel and olfactometer experiments, showing that grasshoppers can orient upwind in response to food odors. To date, 3 grasshopper species, Schistocerca gregaria, S. americana, and Melanoplus sanguinipes, have been shown, in the laboratory, to move upwind to the odors of damaged plants (Haskell et al. 1962, Kennedy & Moorhouse 1969, Moorhouse 1971, Hopkins & Young 1990, Lee et al. 1987, Njagi & Torto 1996, Szentesi et al. 1996). Melanoplus sanguinipies also oriented to various synthetic green-leaf volatiles (Hopkins & Young 1990, Szentesi et al. 1996), and S. gregaria were attracted to the odors of 3 ammonium salts (Haskell et al. 1962). In addition, numerous grasshopper species oriented in wind tunnels to the odors of carrion or fatty acids (Bomar & Lockwood 1994a, Lockwood et al. 2001). Movement upwind is assumed to be via odor-induced anemotaxis (Kennedy & Moorhouse 1969, Szentesi et al. 1996). However, there is evidence that grasshoppers can also orient to odors in still air (Slifer 1955, Szentesi 1996).

After contacting a potential food item, further identification and acceptance of that plant probably relies primarily on taste (Muralirangan et al. 1997, Chapman & Sword 1993). Indeed, nonvolatile plant chemicals can strongly influence grasshopper feeding (Blaney 1975, Mole & Joern 1994). Grasshopper antennae, mouthparts, and tarsi are richly supplied with contact chemosensilla (Chapman 1988, Blaney & Simmonds 1990, White & Chapman 1990b), and prior to biting, grasshoppers typically antennate and rapidly palpate the leaf surface, and touch it with their labrum (Blaney & Chapman 1970, Blaney & Simmonds 1990, Chapman 1990). This brings gustatory sensilla into contact with leaf chemicals, and grasshopper gustatory sensilla respond electrophysiologically to numerous compounds (Blaney 1975; Simpson et al. 1990, 1991).

Mechanoreceptors on the palps, labrum, and galeae function to locate and align the mandibles with the leaf edge (Sinoir 1969). Prior to biting, grasshoppers usually glide their heads over the leaf surface while rapidly palpating it, until the leaf edge is located (Chapman 1988). Continued feeding presumably relies on input from gustatory receptors on the mouthparts and in the buccal cavity (Blaney & Simmonds 1990), and mechanoreceptors continue to guide the food into and through the mouth.

The most controversial step in the above scenario is medium- to long-range olfactory orientation (Bailey & Harris 1991). This is because many species in the field appear not to use olfaction in host search. Some grasshoppers remain on their food plants for most of their lives, and therefore appear not to require strong olfactory senses. Other grasshoppers wander on the ground and sample (bite) nearly every plant they encounter, lending support to the idea that most diet selection in acridids begins, not with olfaction, but with random biting (Dadd 1963; Mulkern 1967; Sinoir 1969, 1970; Bland 1981). Few authors have rigorously demonstrated odor orientation to undamaged plants in either the lab or field, and others found little or no evidence of olfactory orientation (Williams 1954, Dadd 1963, Mulkern 1967, Bland 1981).

In this paper we report that adult Eastern Lubber grasshoppers, Romalea microptera (Beauvois), orient to the odors of damaged plants in a wind tunnel. This species is excellent for this type of study because it is polyphagous, large, flightless, docile, and easily reared in the laboratory (Matuszek & Whitman 2001). In addition, early reports suggest that R. microptera exhibits long-distance orientation to food odors (Watson & Bratley 1940). In 2 successive years, Watson (1941) noted large numbers of R. microptera nymphs marching in long columns toward fields planted with narcissus, a favored food. In the 1st year, narcissus was planted about 300 m to the northeast of the hatching site, and the nymphs marched to the northeast. In the 2nd year, narcissus was planted to the west, and the nymphs marched to the west, suggesting that group marching in this species was directed toward a food source.

Methods and Materials

Insects.—Eastern Lubber grasshoppers, Romelea microptera (Beauvois) were obtained from the Illinois State University colony, maintained in 1 m3 wire-mesh cages at 23 to 34°C and L:D 14:10 photoperiod, and fed Romaine lettuce, wheat bran, and oatmeal ad libitum, with supplements of green onion, green bean pods, and carrot leaves and roots, 3 times per week (Chladny & Whitman 1997, Matuszek & Whitman 2001). The colony was established from wild animals captured in Copeland, Florida in 1997. Experimental animals consisted of 9 to 35 d-old adults, and were provided with narcissus for 2 or 3 d prior to starvation.

Wind Tunnel.—We tested the walking response of individual grasshoppers to odors in a 183 × 30.5 × 15 cm wooden wind tunnel, with a transparent plexiglass lid (wind speed: 47 cm/s; air temperature: 30 to 32°C; light source: eight 40 W fluorescent bulbs, 2 m above and parallel to the chamber). A double layer of black nylon screen at the upwind end of the tunnel allowed air flow, but blocked visual stimuli. During tests, odor sources were placed on the floor, in the center of a separate 15 × 30.5 × 15 cm odor chamber attached to the upwind end of the wind tunnel. A variable-speed fan sucked air through the odor chamber, then the tunnel, and then vented it through a duct outside the room. Preliminary tests using “fog” from dry ice placed in warm water, demonstrated a relatively steady, laminar and turbulence-free air flow, through the wind tunnel, and allowed us to determine wind speed. The floor of the wind tunnel was lined with white paper, which was changed with each new animal. Grid marks allowed us to measure the location of the test insect as it moved up or downwind.

Experiment 1: Response to food odors.—We tested individual adult R. microptera to each of 4 odor sources vs 3 starvation treatments, for a total of 12 odor × starvation combinations. Five to 10 different animals were used for each combination. Each animal was tested once. Odor sources included 50 g of Romaine lettuce (Lactuca sativa L. var. longifolia), green onion (Allium cepa), narcissus (Narcissus pseudonarcissus), and a no-odor (empty chamber) control. Lettuce, narcissus, and onion are favored foods for R. microptera. Starvation treatments included animals starved for 24, 48, or 72 h. Animals were starved by keeping them in a food and water-free container, held under similar environmental conditions as described above for the stock colony. During starvation, no cannibalism occurred.

Experiment 2: Response to water vapor.—We tested individual adult R. microptera to 2 odor sources vs 3 starvation treatments, for a total of 6 odor × starvation combinations. Six different animals were used for each combination. Odor sources used were the presence or absence of 50 g of H2O. Starvation treatments included animals starved for 24, 48, or 72 h. Animals were starved as per Experiment 1.

Odor preparation.—In a separate room, immediately before the test, 50 g of fresh plant material (leaves of Romaine lettuce, or leaves, stems, and bulbs of green onion or narcissus) were chopped, macerated, and placed into a new clean 1-cm deep × 12-cm diameter plastic tray. For Experiment 2, 50 g of tap water were placed in a similar plastic tray. For no-odor controls, in both Experiments 1 & 2, we used empty clean trays.

Testing procedure.—For both Experiments 1 & 2, individual adult grasshoppers were placed on the floor in the exact center of the wind tunnel, facing the wall and perpendicular to the wind flow. We alternated between male and female grasshoppers for each run. After 15 min, we recorded the upwind (+) or downwind (−) distance moved by the grasshopper.

Statistical Analysis.—In both experiments we first used independent-measures t-tests to test for sexual differences. We then used a 2-way fixed-effect model of the GLM (general linear model) procedure for both Experiments 1 & 2, to analyze the effects of starvation time versus food type or water vapor on grasshopper movement in the wind tunnel. Post-hoc testing was conducted using the Ryan-Einot-Gabriel-Welsch (REGWQ) multiple range test. All statistical tests were conducted using SPSS version 9.0 (SPSS Inc.) or SAS (SAS Institute Inc.).

Results

Experiment 1: response to food odors

We pooled the results from males and females because we found no significant difference (two-independent sample t-test t96 = 0.720, P>0.05) in upwind distance traveled by males (x̄± s = 21.7 ± 6.7 cm, N=49) vs females (29.1 ± 7.7 cm, N=49). We then used a 2-way fixed-effect GLM procedure to examine the effect of both food type and starvation time and to check for potential interactions between starvation time and food type. This analysis demonstrated that there were significant differences among the treatments (F11,86=2.66, P<0.05), but no significant interaction between food type and starvation time (F6,86=1.22, P>0.05). Food type demonstrated significant differences among the various treatment groups (food type F3,86=5.30, P<0.05). Post-hoc analysis of the food type groups demonstrated 2 different REGWQ groupings. Significant differences were found in the upwind distance traveled by animals exposed to either Romaine lettuce or narcissus compared to the no-food controls (Fig 1). There was a strong trend, but no significant difference (F2,86=2.41, P>0.05) in mean distance moved upwind between the 24-h starved (17 cm), 48-h starved, (38 cm) and 72-h starved (46 cm) groups (Fig. 2).

Experiment 2: response to water vapor

As in Experiment 1 we pooled the results from males and females, because we found no significant difference (t34 = −0.807, P>0.05) in distance traveled upwind by males (x̄±s = 11.2 ± 7.2 cm, N=18) vs females (0.4 ± 11.3 cm, N=18). We conducted further tests using a two-way fixed effect GLM procedure to examine the effects of both water vapor and starvation time and to check for potential interactions between starvation time and water vapor. This analysis demonstrated that there were significant differences among the treatments (F5,30=4.35, P<0.05), but no significant interaction between water vapor and starvation time (F2,30=1.71, P>0.05). Further, there was no significant difference between the animals tested in the presence, vs the absence, of water vapor (F1,30=1.10, P>0.05) (Fig. 3). However, there were significant differences among the 3 starvation treatments (F2,30=8.62, P<0.05). Post-hoc analysis of starvation time (for combined water and no-water treatments) demonstrated 2 different REGWQ groupings. The first group demonstrated no significant difference in the mean distance traveled by the 24-h starved (−0.3 cm), and 48-h starved (−18.5 cm), individuals. The 2nd group consisted of the 72-h starved individuals, who traveled significantly further upwind (36.1 cm) than either the 24-h or 48-h starved groups (Fig. 4).

Discussion

Our study demonstrates that adult lubber grasshoppers can respond to food odors by moving upwind. These results support previous work on the use of olfactory cues in the Acrididae (Chapman 1988). Among grasshoppers, S. gregaria, S. americana, and M. sanguinipes have been shown to move upwind to the odors of crushed or cut plants in wind tunnels or y-tube olfactometers (Kennedy & Moorhouse 1969, Lee et al. 1987, Hopkins & Young 1990, Njagi & Torto 1996, Szentesi et al. 1996). M. sanguinipes also moved upwind toward the odors of undamaged grasses and individual and mixed green leaf volatiles in the laboratory (Hopkins & Young 1990, Szentensi 1996), and Zonocerus species oriented in the field to plants releasing pyrrolizidine alkaloids (Boppré & Fischer 1994). In addition, many grasshoppers orient to the odors of carrion or volatile fatty acids, in the field or in wind tunnels (Lockwood 1989a,b; Bomar & Lockwood 1994a,b,c; Whitman et al. 1994; Lockwood et al. 2001).

In our tests, odors from fresh mashed narcissus elicited greater orientation responses than did odors from mashed onion, suggesting that plants vary in their attractiveness. Electrophysiological studies demonstrate that grasshopper sensilla can discriminate among odors (Blaney & Simmonds 1990, Njagi & Torto 1996). Haskell et al. (1962) and Hopkins and Young (1990) also reported that different plants and individual volatile compounds elicited different levels of orientation in wind tunnels, implying that grasshoppers can discriminate among different plant odors from a distance.

Although grasshoppers possess hygroreceptors (Slifer 1955, Bland 1981, Blaney & Simmonds 1990), we were unable to demonstrate an upwind movement to water vapor alone, suggesting that orientation toward the mashed plants in our study was not simply a response to water vapor, but was in response to other plant volatiles. Although some authors have provided limited evidence that grasshoppers could orient toward or away from water vapors (Bodenheimer 1944; Slifer 1955; Riegert 1959, 1960; Lockwood 1989a), other have suggested otherwise (Kennedy 1937, Aziz 1957, Haskell et al. 1962, Bomar & Lockwood 1994a). Clearly, this area requires further study.

In our second experiment, upwind movement increased with starvation time, with 72-h starved individuals demonstrating a significant upwind movement when compared to either the 24-h, or 48-h starved groups. A similar nonsignificant trend was observed in Experiment 1 (Fig. 2). Previous authors have noted that hunger stimulates locomotion (Williams 1954, Kaufman 1968, Mulkern 1969, Bland 1981, Chapman 1988) or odor orientation (Haskell et al. 1962, Kennedy & Moorhouse 1969, Moorhouse 1971) in grasshoppers. However, we failed to find a significant odor × starvation interaction, suggesting that in R. microptera, increased starvation influenced response to wind, but not to odor.

Do grasshoppers commonly use olfaction when orienting to food plants in nature?—To date, only 4 grasshopper species from 3 subfamilies, have been shown to orient to plants via olfaction in the laboratory, and virtually all of these studies used cut, bruised, or macerated plants. One notable exception was Hopkins and Young (1990) who used both damaged, and whole undamaged plants. It is well known that damaged plants release different and substantially greater amounts of volatiles than undamaged plants, and thus these various laboratory studies may not accurately reflect what occurs in nature. Likewise, although grasshoppers will orient to baits, carrion, or volatile fatty acids in the field, this does not necessarily mean that they normally use olfaction to orient to plants. Observations of olfactory orientation to plants in nature are mostly anecdotal (Watson 1941, Chapman 1990). In contrast, Zonocerus variegatus and Z. elegans clearly use olfaction to orient to pyrrolizidine alkaloid-containing plants (Boppré et al. 1984, Modder 1984), but this orientation may be primarily for purposes of pharmacophagy instead of nutrition (Boppré & Fischer 1994). Hence, at this time, there is strong evidence that grasshoppers use olfaction in host search, but rigorous field confirmation is needed. It will be especially important to test monophagous and oligophagous species from a diversity of subfamilies, communities, and life-forms (geophilous, arboricoles, etc.) to odors from undamaged and slightly damaged plants, in the field. Despite these limitations, we believe that the evidence to date makes it highly likely that free-living grasshoppers incorporate at least short-range olfaction when searching for food plants.

In conclusion, our results reaffirm the idea that grasshoppers use not only visual, acoustic, thermal, gustatory, and tactile senses to monitor and orient to the environment, but also olfaction. The growing evidence of orientation to food odors by grasshoppers parallels an increasing awareness of the importance of intraspecific odor communication (pheromones) for both gregarious and solitary grasshoppers (Whitman 1990, Heifetz et al. 1996, Pener & Yerushalmi 1998, Stauffer et al. 1998, Hassanali & Torto 1999, Niassy et al. 1999, Torto et al. 1999, Despland 2001, Njagi & Torto 2002), suggesting that olfaction is more important to grasshoppers than previously realized.

Acknowledgments

This research was initiated and supported by Dr. Scott Sakaluk's Animal Behavior class and the Undergraduate Research Training (CRUI) Program at Illinois State University, and by NSF grant DBI-9978810.

References

1.

S. A. Aziz 1957. The reactions of the Desert Locust, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae), to physical factors, with special reference to relative humidity. Bulletin of Entomological Research 48:515–531. Google Scholar

2.

E. V. Bailey and M. O. Harris . 1991. Visual behaviors of the Migratory Grasshopper, Melanoplus sanguinipes F. (Orthoptera: Acrididae). Journal of Insect Behavior 4:707–726. Google Scholar

3.

R. G. Bland 1981. Survival and food detection by first-instar Melanoplus femurrubrum (Orthoptera: Acrididae). Great Lakes Entomologist 14:197–204. Google Scholar

4.

R. G. Bland 1989. Antennal sensilla of Acrididae (Orthoptera) in relation to subfamily and food preferences. Annals Entomological Society of America 82:368–384. Google Scholar

5.

W. M. Blaney 1975. Behavioural and electrophysiological studies of taste discrimination by the maxillary palps of larvae of Locusta migratoria (L). Journal of Experimental Biology 62:555–569. Google Scholar

6.

W. M. Blaney 1977. The ultrastructure of an olfactory sensillum on the maxillary palps of Locusta migratoria (L). Cell and Tissue Research 184:397–409. Google Scholar

7.

W. M. Blaney and R. F. Chapman . 1970. The functions of the maxillary palps of Acrididae (Orthoptera). Entomologia Experimentalis et Applicata 13:363–376. Google Scholar

8.

W. M. Blaney and M. S. J. Simmonds . 1990. The Chemoreceptors, pp. 1–37. In: Chapman R.F., Joern A. (Eds) Biology of Grasshoppers. John Wiley and Sons, New York. Google Scholar

9.

M. H. Blust and T. L. Hopkins . 1987. Olfactory responses of a specialist and a generalist grasshopper to volatiles of Artemisia ludoviciana (Nutt.) (Asteraceae). Journal of Chemical Ecology 13:1893–1902. Google Scholar

10.

F. S. Bodenheimer 1944. Studies on the ecology and control of the Moroccan Locust (Dociostaurus maroccanus) in ‘Iraq. I. Results of a mission of the ‘Iraq Department of Agriculture to N. ‘Iraq in spring 1943. Bull. Dir.-gen. Agric. ‘Iraq 29:121. Google Scholar

11.

C. R. Bomar and J. A. Lockwood . 1994a. Olfactory basis of cannibalism in grasshoppers (Orthoptera: Acrididae): I. Laboratory assessment of attractants. Journal of Chemical Ecology 20:2249–2260. Google Scholar

12.

C. R. Bomar and J. A. Lockwood . 1994b. Olfactory basis of cannibalism in grasshoppers (Orthoptera: Acrididae): II. Field Assessment of attractants. Journal of Chemical Ecology 20:2261–2272. Google Scholar

13.

C. R. Bomar and J. A. Lockwood . 1994c. Olfactory basis of cannibalism in grasshoppers (Orthoptera: Acrididae): III. Use of attractants on carbaryl wheat bran bait. Journal of Chemical Ecology 20:2273–2281. Google Scholar

14.

M. Boppré and O. W. Fischer . 1994. Zonocerus and Chromolaena in West Africa, pp. 107–126. In: Krall S., Wilps H. (Eds) New Trends in Locust Control. Deutsche Gesellschaft für Tecnische Zusammenarbeit, Eschborn. Google Scholar

15.

M. Boppré, U. Seibt, and W. Wickler . 1984. Pharmacophagy in grasshoppers? Zonocerus attracted to and ingesting pure pyrrolizidine alkaloids. Entomologia Experimentalis et Applicata 35:115–117. Google Scholar

16.

R. F. Chapman 1974. The chemical inhibition of feeding by phytophagous insects: a review. Bulletin of Entomological Research 64:339–363. Google Scholar

17.

R. F. Chapman 1988. Sensory aspects of host-plant recognition by Acridoidea: questions associated with the multiplicity of receptors and variability of response. Journal of Insect Physiology 34:167–174. Google Scholar

18.

R. F. Chapman 1990. Food selection, pp. 39–72. In: Chapman R.F., Joern A. (Eds) Biology of Grasshoppers. John Wiley and Sons, New York. Google Scholar

19.

R. F. Chapman and G. Sword . 1993. The importance of palpation in food selection by a polyphagous grasshopper (Orthoptera: Acrididae). Journal of Insect Behavior 6:79–91. Google Scholar

20.

R. F. Chapman, E. A. Bernays, and T. Wyatt . 1988. Chemical aspects of host-plant specificity in three Larrea-feeding grasshoppers. Journal of Chemical Ecology 14:561–579. Google Scholar

21.

H. H. Chen and L. Kang . 2000. Olfactory responses of two species of grasshoppers to plant odours. Entomologia Experimentalis et Applicata 95:129–134. Google Scholar

22.

T. Chladny and D. Whitman . 1997. A simple method to culture grasshopper eggs with long egg diapause. Journal of Orthoptera Research 6:82. Google Scholar

23.

R. H. Dadd 1963. Feeding behaviour and nutrition in grasshoppers and locusts, pp. 47–109. In: Beament J.W.L., Treherne J.E., Wigglesworth V.B. (Eds) Advances in Insect Physiology. Academic Press, London. Google Scholar

24.

E. Despland 2001. Role of olfactory and visual cues in the attraction/repulsion responses to conspecifics by gregarious and solitarious Desert Locusts. Journal of Insect Behavior 14:35–46. Google Scholar

25.

J. C. Dickens, G. D. Prestwich, C. Ng, and J. H. Visser . 1993. Selectively fluorinated analogs reveal differential olfactory reception and inactivation of green leaf volatiles in insects. Journal of Chemical Ecology 19:1981–1991. Google Scholar

26.

B. S. Hansson, S. A. Ochieng', X. Grosmaitre, S. Anton, and P. G. N. Njagi . 1996. Physiological responses and central nervous projections of antennal olfactory receptor neurons in the adult Desert Locust, Schistocerca gregaria (Orthoptera: Acrididae). Journal of Comparative Physiology A 179:157–167. Google Scholar

27.

P. T. Haskell, M. W. J. Paskin, and J. E. Moorhouse . 1962. Laboratory observations on factors affecting the movements of hoppers of the Desert Locust. Journal of Insect Physiology 8:53–78. Google Scholar

28.

A. Hassanali and B. Torto . 1999. Grasshoppers and locusts. In: Hardy J., Minks A. (Eds) Pheromones of Non-lepidopteran Insects Associated with Agricultural Plants. CABI, London. Google Scholar

29.

Y. Heifetz, H. Voet, and S. W. Applebaum . 1996. Factors affecting behavioral phase transition in the Desert Locust, Schistocerca gregaria (Forskal) (Othoptera: Acrididae). Journal of Chemical Ecology 22:1717–1734. Google Scholar

30.

T. L. Hopkins and H. Young . 1990. Attraction of the grasshopper, Melanoplus sanguinipes, to host plant odors and volatile components. Entomologa Experimentalis et Applicata 56:249–258. Google Scholar

31.

L. Kang and H. H. Chen . 1997. Antennal sensilla of grasshoppers (Orthoptera: Acrididae) in relation to subfamily and biological habit. Metaleptea 17:215. Google Scholar

32.

L. Kang, R. Charlton, and T. L. Hopkins . 1995. Olfactory response of the grasshopper Melanoplus sanguinipes to plant odours and volatile compounds. Entomologia Sinica 2:136–144. Google Scholar

33.

T. Kaufmann 1968. A laboratory study of feeding habitats of Melanoplus differentialis in Maryland (Orthoptera: Acrididae). Annals Entomological Society of America 61:173–180. Google Scholar

34.

J. S. Kennedy 1937. The humidity reactions of the African Migratory Locust, Locusta migratoria migratoriodes R. and F., gregarious phase. Journal of Experimental Biology 14:187–197. Google Scholar

35.

J. S. Kennedy 1939. The behaviour of the Desert Locust (Schistocerca gregaria) (Forsk) (Orthoptera) in an outbreak center. Transactions Royal Entomological Society London 89:385–542. Google Scholar

36.

J. S. Kennedy and J. E. Moorhouse . 1969. Laboratory observations on locust responses to wind-borne grass odour. Entomologica Experimentalis et Applicata 12:487–503. Google Scholar

37.

J. C. Lee, E. A. Bernays, and R. P. Wrubel . 1987. Does learning play a role in host location and selection by grasshoppers, pp. 125–127. In: Labeyrie V., Fabres G., & Lachaise D. (Eds) Insects-Plants. Proceedings of the 6th International Symposium on Insect-Plant Relationships (PAU 1986). Dr W. Junk, Dordrecht, Netherlands. Google Scholar

38.

J. A. Lockwood 1989a. Cannibalism in rangeland grasshoppers (Orthoptera: Acrrididae): attraction to cadavers. Journal Kansas Entomological Society 61:379–387. Google Scholar

39.

J. A. Lockwood 1989b. Ontogeny of cannibalism in rangeland grasshoppers (Orthoptera: Acrididae). Journal Kansas Entomological Society 62:534–541. Google Scholar

40.

J. A. Lockwood 2001. Canola oil as a kairomonal attractant of rangeland grasshoppers: an economical liquid bait for insecticide formulation. International Journal of Pest Management 47:185–194. Google Scholar

41.

J. V. Matuszek and D. W. Whitman . 2001. Captive rearing of Eastern Lubber Grasshoppers Romalea microptera. Invertebrates in Captivity. pp. 56–63. Google Scholar

42.

W. W. D. Modder 1984. The attraction of Zonocerus variegatus (L.) (Orthoptera: Pyrgomorphidae) to the weed Chromolaena odorata and associated feeding behaviour. Bulletin of Entomological Research 74:239–247. Google Scholar

43.

S. Mole and A. Joern . 1994. Feeding behavior of graminivorous grasshoppers in response to host-plant extracts, alkaloids, and tannins. Journal of Chemical Ecology 20:3097–3109. Google Scholar

44.

J. E. Moorhouse 1971. Experimental analysis of the locomotor beaviour of Schistocerca gregaria induced by odour. Journal Insect Physiology 17:913–920. Google Scholar

45.

A. J. Mordue 1979. The role of the maxillary and labial palps in the feeding behaviour of Schistocerca gregaria. Entomologia Experimentalis et Applicata 25:279–288. Google Scholar

46.

G. B. Mulkern 1967. Food selection by grasshoppers. Annual Review of Entomology 12:59–78. Google Scholar

47.

G. B. Mulkern 1969. Behavioral influences on food selection in grasshoppers (Orthoptera: Acrididae). Entomologia Experimentalis Applicata 12:509–523. Google Scholar

48.

M. C. Muralirangan, M. Muralirangan, and P. D. Partho . 1997. Feeding behaviour and host selection strategies in Aacridids, pp. 163–182. In: Gangwere S.K., Muralirangan M.C., Muralirangan M. (Eds) The Bionomics of Grasshoppers, Katydids and Their Kin. CAB International. Google Scholar

49.

A. Niassy, B. Torto, P. G. N. Njagi, A. Hassanali, D. Obeng-Ofori, and J. N. Ayertey . 1999. Intra- and interspecific aggregation responses of Locusta migratoria migratorioides and Schistocerca gregaria and a comparison of their pheromone emissions. Journal of Chemical Ecology 25:1029. Google Scholar

50.

P. B. N. Njagi and B. Torto . 1996. Responses of nymphs of desert locust, Schistocerca gregaria to volatiles of plants used as rearing diet. Chemoecology 178:172–178. Google Scholar

51.

P. G. N. Njagi and B. Torto . 2002. Evidence for a compound in Comstock-Kellog glands modulating premating behavior in male Desert Locust, Schistocerca gregaria. Journal of Chemical Ecology 28:1065–1074. Google Scholar

52.

M. P. Pener and Y. Yerushalmi . 1998. The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44:365–377. Google Scholar

53.

P. W. Riegert 1959. The humidity reactions of grasshoppers. Humidity reactions of Melanoplus bivitattus (Say.) and Camnula pellucida (Scudd.): reactions of normal grasshoppers. Canadian Entomologist 91:35–40. Google Scholar

54.

P. W. Riegert 1960. The humidity reactions of Melanoplus bivittatus (Say) (Orthoptera, Acrididae): antennal sensilla and hygro-reception. Canadian Entomologist 92:561–570. Google Scholar

55.

C. L. Simpson, S. Chyb, and S. J. Simpson . 1990. Changes in chemoreceptor sensitivity in relation to dietary selection by adult Locusta migratoria. Entomologia Experimentalis et Applicata 56:259–268. Google Scholar

56.

S. J. Simpson, S. James, M. S. J. Simmonds, and W. M. Blaney . 1991. Variation in chemosensitivity and the control of dietary selection behaviour in the locust. Appetite 17:141–154. Google Scholar

57.

Y. Sinoir 1969. Le rôle des palpes et du labre dans le comportement de nourriture chez la larve du criquet migrateur. Ann. Nutr. Alim 23:167–194. Google Scholar

58.

Y. Sinoir 1970. Quelques aspects du comportement de prise de nourriture chez la larve de Locusta migratoria migratorioides (R and F). Annales Société Entomologique France (N.S.) 6:391–405. Google Scholar

59.

E. H. Slifer 1954. The reaction of a grasshopper to an odorous material held near one of its feet (Orthoptera: Acrididae). The Proceedings Royal Entomological Society of London 29:177–179. Google Scholar

60.

E. H. Slifer 1955. The detection of odors and water vapor by grasshoppers (Orthoptera: Acrididae) and some new evidence concerning the sense organs which may be involved. Journal of Experimental Zoology 130:301–317. Google Scholar

61.

E. H. Slifer 1956. The response of a grasshopper, Romalea microptera (Beauvois) to strong odours following amputation of the metathoracic leg at different levels. Proceedins Royal Entomological Society London A 31:95–98. Google Scholar

62.

T. W. Stauffer, S. G. Hegrenes, and D. W. Whitman . 1998. A laboratory study of oviposition site preferences in the Lubber Grasshopper, Romalea guttata (Houttuyn). Journal of Orthoptera Research 7:217–221. Google Scholar

63.

A. Szentesi, T. L. Hopkins, and R. D. Collins . 1996. Orientation responses of the grasshopper, Melanoplus sanguinipes, to visual, olfactory, and wind stimuli and their combinations. Entomologia Experimentalis et Applicata 80:539–549. Google Scholar

64.

B. Torto, Y. O. H. Assad, P. G. N. Njagi, and A. Hassanali . 1999. Evidence for additional pheromonal components mediating oviposition aggregation in Schistocerca gregaria. Journal of Chemical Ecology 25:835–845. Google Scholar

65.

B. Uvarov 1977. Grasshoppers and Locusts: A Handbook of General Acridology. Centre For Overseas Pest Research, London. Google Scholar

66.

M. Volkonsky 1942. Observations sur le comportement du criquet pelerin (Schistocerca gregaria) (Forskal) dans le sahara Algero-nigerien. Arch. Inst. Pasteur Alger 20:236–248. Google Scholar

67.

G. K. Wallace 1958. Some experiments on form perception in the nymphs of the Desert Locust, Schistocerca gregaria (Forskal). Experimental Biology 35:765–775. Google Scholar

68.

J. R. Watson and H. E. Bratley . 1940. Preliminary report on Lubberly Locust control. Florida Entomologist 23:7–10. Google Scholar

69.

J. R. Watson 1941. Migrations and food preferences of the Lubberly Locust. Florida Entomologist 24:40–42. Google Scholar

70.

P. R. White and R. F. Chapman . 1990a. Olfactory sensitivity of gomphocerine grasshoppers to the odours of host and non-host plants. Entomologia Experimentalis et Applicata 55:205–212. Google Scholar

71.

P. R. White and R. F. Chapman . 1990b. Tarsal chemoreception in the polyphagous grasshopper Schistocerca americana: behavioural assays, sensilla distributions and electrophysiology. Physiological Entomology 15:105–121. Google Scholar

72.

D. W. Whitman 1990. Grasshopper chemical communication, pp. 357–391. In: Chapman R.F., Joern A. (Eds) Biology of Grasshoppers. John Wiley, New York. Google Scholar

73.

D. W. Whitman, M. S. Blum, and F. Slansky . 1994. Carnivory in phytophagous insects, pp. 161–205. In: Ananthakrishnan T.N. (Ed) Functional Dynamics of Phytophagous Insects. Oxford and IBH Publishing CO. PVT. LTD., New Delhi. Google Scholar

74.

L. H. Williams 1954. The feeding habitats and food preferences of Acididae and the factors which determine them. Transactions Royal Entomological Society of London 105:423–454. Google Scholar

Fig 1. Direction and mean distance traveled (x̄+s) by adult R. microptera grasshoppers in a wind tunnel, when exposed to various food odors (starvation treatments combined). A GLM analysis demonstrated significant differences among treatments (F3,86=5.30, P<0.05). Post-hoc analysis using REGWQ multiple range test demonstrated two groupings (designated a and b). A significant difference between the mean distance traveled upwind for the narcissus and romaine lettuce-treatments compared to the no-food odor group is clearly seen. The onion-treatment group is a member of both groupings.

i1082-6467-12-2-135-f01.gif

Fig 2. In Experiment 1, GLM analysis of the effect of starvation period on the mean distance traveled by R. micropetra grasshoppers (food treatments combined) demonstrated a strong trend, but no significant differences among the treatments (F2,86=2.41, P>0.05).

i1082-6467-12-2-135-f02.gif

Fig 3. Mean distance (x̄+s) traveled upwind by adult R. microptera grasshoppers in a wind tunnel exposed to either the presence or absence of water vapor (starvation treatments combined). GLM analysis showed no significant difference (F1,30=1.10, P>0.05) between the 2 groups.

i1082-6467-12-2-135-f03.gif

Fig 4. The effect of starvation period on upwind movement of R. microptera grasshoppers in a wind tunnel (response to water vapor and no water vapor combined). REGWQ multiple range test demonstrated 2 groupings (designated a & b) with the 72-h starved grasshoppers moving significantly further upwind than either the 24-h or 48-h starved insects.

i1082-6467-12-2-135-f04.gif
Jeff B. Helms, Carrie M. Booth, Jessica Rivera, Jason A. Siegler, Shannon Wuellner, and Douglas W. Whitman "Lubber grasshoppers, Romalea microptera (Beauvois), orient to plant odors in a wind tunnel," Journal of Orthoptera Research 12(2), 135-140, (1 December 2003). https://doi.org/10.1665/1082-6467(2003)012[0135:LGRMBO]2.0.CO;2
Published: 1 December 2003
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