Syril A. Blondheim and Eliezer Frankenberg.
'Protest' sounds of a grasshopper: predator-deterrent signal?
Psyche 90(4):387-394, 1983.

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'PROTEST'SOUNDS OF A GRASSHOPPER:
PREDATOR-DETERRENT SIGNAL?*
BY SVRII. A. BI.ONDIEIM AND El-IEZER FRANKENBERG Zoology Dept., Hebrew University of Jerusalem Jerusalem. Israel
Some animals emit sounds when grasped or handled. Referred to as alarm, protest, distress or disturbance signals-the sounds themselves, the behavior accompanying their emission and the mechanisms responsible for their production have been described, analyzed and discussed (Haskell 1974). But only recently have experimental data become available in support of the oft-stated hypothesis that these sounds may startle a predator into releasing a noisy morsel (Bauer 1976; Smith and Langley 1978; Masters 1979; Buckler et al 1981).
The grasshopper Pareuprepocnemis xyriaca Giglio Tos (Acridi- dae) when grasped, immediately begins to chirp (the biology and acoustic behavior of this grasshopper will be described separately). Though there are individual differences in intensity and quality of the sounds. males have a greater tendency to squeak while females tend to click. Emission of the sounds is easily observed to correspond to movements of the mouthparts; if the labrum is lifted, the mandibles can be seen rubbing against one another to the rhythm of the chirps. Immobilization of the mouthparts prevents sound emission.
It had been observed in our laboratory that on casual feeding of this grasshopper to representatives of several lizard families (La- certidae, Scincidae. Gekkonidae) the grasshopper was captured. then promptly released. A male grasshopper introduced into the cage of the lizard Lacerfa danfbrdi was caught head-first and held in the mouth of the lizard for several seconds, after which the lizard slowly opened its mouth and the grasshopper fell free. Several addi- tional grasshoppers of this species were offered to two Euhlepharifi macularius, a gecko from Pakistan present in the vivarium at the



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[Vol. 85
time. They grabbed, then released the insects. Additional observa- tions were then made with a microphone in the cage transmitting sounds to earphones worn by the investigator. A skink, Mabuva vittata caught and then released a sound-producing P. sj~riaca male; three geckos, P. h. guttatus each caught and promptly released sound-producing males of P. syriaca. These rejected grasshoppers were removed and immediately replaced by mute grasshopper nymphs of L. m. migratorioides, equivalent in size to the rejected P. syriaca males; the nymphs were caught and immediately consumed, one by each gecko. These preliminary observations raised the ques- tion: were the sounds emitted by the grasshoppers a factor in their release? The following experiments were designed to answer this question.
Grasshoppers: Adult males of P. syriaca were field caught in the hills of Jerusalem a few days prior to experiments and were main- tained in 60 1 laboratory cages providing fresh plants, light and heat. As males were lifted from the cage for assignment to an experiment, the thorax was squeezed gently. Of 48 males squeezed, only three failed to produce sound. Half the sound-producing males were then silenced by releasing a drop of melted paraffin onto the closed mandibles; when it hardened, these males could no longer emit sound, though they hardly differed in appearance from untreated males.
Fourth instar nymphs of Locusta migratoria migratorioides R & F maintained in the gregarious state in stock cages in the laboratory, served as additional controls. Their size, dark color and small wing buds provided a phenotypically reasonable facsimile of the brachyp- terous adult male of P. sjiriaca. These nymphs did not produce sound when handled.
Predators: Ptyodact.\~lus hasselquistii guttatus von Heyden was selected as the predator for the series of experiments. The candidacy of this gecko was supported by the following credentials: P. h. gutta- tus, a poikilotherm like P. syriaca, is at least partially sympatric with it and shares its biotope; it is an opportunistic insectivore; like P. s>\?riaca, it emerges from its retreat in rock ledges and crevices in warm weather and has been known to feed during daylight (Werner 1965; Perry & Werner 198 1); juveniles could handle a grasshopper



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19831 Blondehim & Frankenberg - Sounds of Grasshopper 389 the size of the P. syriaca male, while adults could handle even the large female; the frequency spectrum of the sounds of P. syriaca falls within the hearing range of P. h. guttatus (Werner 1976); and finally, a laboratory stock of this gecko was available. Though wild- caught. the geckos had been kept in captivity in the vivarium for months to years. Though the memory span of this gecko species is not known, it may well be that the long laboratory incarceration had dimmed recollections of possible previous encounters with this grasshopper and its ruse.
Experimental procedure: A series of three grasshoppers was introduced simultaneously into the cage of a gecko whose habitual diet of fly maggots had been removed at least a day previous: an untreated P. s.~*riaca male, a silenced P. svriaca male and a fourth instar nymph of L. m. migratorioides. The insects were introduced at noon, prior to the peak activity hours of the gecko (Frankenberg 1979), and observations were made every half hour from noon to 5:00 PM and from 8:00 AM to noon. The first item eaten was assigned the number 1; the second item, 2; and the third, 3. If two grasshoppers disappeared between any two readings, both were assigned the same number. In the few instances in which all three grasshoppers were alive and apparently unharmed at the end of 24 hours, it was assumed that the gecko was not hungry; the experi- ment was not included in tallying the results. After an interval of several days, the gecko was used again. Silenced P. syriaca were checked at the end of the experiment to ascertain that they were indeed still unable to produce sound.
In the cages of the 26 geckos tested, no untreated P. syriaca was ever the first to disappear and 69% were never eaten at all. The silenced P. s.lqriaca was eaten first in 46% and the L. m. migrato- rioides nymphs in 78% of the experiments (Table I and Fig. 1). A G-test (Sokal and Rholf 1969) was carried out to test for indepen- dence between the three choices of prey and the order of predation. It was found significant (G = 49.9; df = 6, p< 0,001). A sign test (Siege1 1956) between each of the three combinations of paired insects for all the 26 instances in which a grasshopper was eaten showed that silenced P. syriaca were eaten before untreated ones in 18 experiments (p<O.002), L. m. migratorioides were eaten before



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390 Psyche Cv^<
Table 1: Order of predation* by the gecko P. h. ~i/tfida/̤.v on a c 'Ìö- o i 4
grasshoppers.
serial
normal silenced
4th ins-ar
number P. 'i~riucu P. xyriucu
nymr>=-
geck o male male
L.~Y.PY a.
I 0 I I
2 0 I I
3 0 1 1
4 3 I 2
5 3 2 I
6 2 0 1
7 0 I 0
8 0 I 1
9 2 3 I
10 3 I 2
I I 0 2 1
12 2 3 I
13 0 0 I
14 0 I 0
15 3 I I
16 0 2 I
17 0 0 I
18 0 I 0
19 3 I 2
20 0 0 I
2 1 0 2 I
22 0 1 1
23 0 2 I
24 0 0 I
25 0 2 I
26 0 0 I
*The numbers I, 2, and 3 represent order of predation; 0 indicates å´ hat grasshopper was alive at the end of the 24 hr test period. The same numbe r F^or r than 1 grasshopper indicates that they were consumed between the sa me observation periods.
the untreated P. syriaca in 23 experiments (ps$ 0.001) and "å´^e
silenced ones in 14 experiments (p = n.s.). It is therefore co n<z^lu< that the protest sounds produced by P. syriaca apparently red predation on it by P. h. guttatus.
To a hungry caged gecko offered a choice between fly mags and grasshoppers, the latter are invariably preferred. how eve^ r, i



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19831 Blondehim & Frankenberg - Sounds of Grasshopper 39 1 apparent from the present results that the appetite for grasshoppers may be tempered by their behavior. In the present case, mandibu- lar sounds emitted by P. syriaca appeared to interfere with preda- tion by this gecko.
Because of its confinement in the cage of the gecko during exper- iments, a grasshopper which had chirped its way to freedom was prevented from escaping its predator as it might in the wild. P.
.s.I-riaca, though it cannot fly, is an excellent jumper and under nat- ural field conditions would probably have jumped far and hidden itself well before the predator had recovered from its encounter. The sound itself has a wide frequency spectrum such as that characterizing alarm calls of birds (Marler 1957; Morton 1977). The utility of sounds such as these might include conspecific warning, since these grasshoppers occur in loose aggregates. However, hold- ing a chirping male in close proximity to conspecifics, or playing the recorded sound back into a cage of P. sjlriaca failed to produce any discernible reaction.
It was observed that these grasshoppers are often seized head first. It is suggested that the hollow bones of birds, or the large buccal cavity of lizards may act as a resonating chamber, enhancing the intensity of the insect's sounds or vibrations. For the few grasshopper species known to producemandi bular sounds spontaneously or in encounters with conspecifics, an in t ra- specific communicative function has been suggested: (Para~j*loiropi- did hrunneri, Alexander 1960; Oedaleonotusfu.scipes, Varley 1 939; Callipiamus italicus, Faber 1949) but no experiments have been reported in support of this hypothesis. Henry (1942) reports that Mesamhria duhia emits a shrill creak when seized and investigation may reveal that this sound, like the protest sound of P. s~~~riac~a studied here, may play a predator-deterrent role. Whether a remnant of an intraspecific communicative cue or a language of predator deterrence, a signal such as that presented here has quite probably been playing a part in the evolutionary history of the struggle for survival in this species. This paper is intended to answer the question of Dr. David Blondheim, who at age 10 asked his mother (SAB) why P. s.19riacci made those strange noises with its mouth when you caught it. Thanks are extended to Dr. N. Ben-Eliahu and to Profs. R. Galun.



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L.m.migratorioides
P. syriaca silenced
P.syriaca normal
order of predation
IVol. 85
Fig. 1.
Order of predation on sound producing and silenced P. .syriacu males and mute nymphs of I.. 111. mi,qru~orioH/e.'i. Legend:
The numbers 1, 2, and 3 in the abscissa represent order of predation; 0 indicates that the grasshoppers were alive at the end of the 24-hr. test period.



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19831 Blondehim & Frankenberg - Sounds of Grasshopper 393 Y.L. Werner, J. Camhi, S. Friedman, E. Nevo and S. H. Blondheim for helpful comments on the manuscript. We also thank Prof. Y.L. Werner for making the inmates of the vivarium available for these experiments; and P. Amitai who drew the figure. Partial support to EF by the Center of Absorption in Science of the Ministry of Absorption is acknowledged with thanks.
Mandibular sounds produced by the grasshopper Pareuprepoc- nemis .s.rriaca Giglio Tos, when seized, appear to reduce predation on it by a probable natural predator, Ptyodart.1*lus hasselquistii guttatus von Heyden, an insectivorous gecko. Sound-producing grasshoppers which had been silenced by treatment in the labora- tory, untreated sound-producing grasshoppers, and silent Locusta migratoria migratorioides nymphs were introduced simultaneously to the geckos. Survival of normal, sound-producing P. syriaca far surpassed that of both controls.
AI.KXANDKR. R. D.
1960.
Communicative mandible-snapping in Acrididae. Science 132: 152-3. BAIYR. I.
1976.
Experimente 7ur Frage der biologischen Bedeutung des Stridulations- verhaltens von Kafern. Z. Tierpsychol. 42: 57-65. Bit-III.I:R. E. R., T. B. WRIGIIT AND E. D. BROWN 1981.
On the functions of stridulation by the Passalid beetle 0chwioiaeniu.s disjunclus (Coleoptera:Passalidae). Animal Behavior 29: 483-486. FAHER. A.
1949.
Eine Bischer unbekannte Art der Lauterzeugung europaischer Orthop- teren: Mandibellaut von Cal1ip1amu.s italicus. Z. Naurforsch 46: 367-9. FRANKENHERG, E.
1979.
Influence of light and temperature on daily activity patterns of 3 Israeli forms of Ptyodactylus (Reptilia: Gekk~ninae). J. Zool. Lond. 185: 2 1 -30.
H ASKEI-I.. P. T.
1974.
Sound Production in The Physiology of Insecta. Second ed. 354-405. M. Rockstein. ed.. Academic Press.
HENRY, G. M.
1942. Three remarkable stridulatory mechanisms in Acrididae (Orthop). Proc. Roy. Ent. Soc. Series A 17: 59-62.
MARLEU, P.
1957. Specific distinctiveness in the communication signals of birds. Behaviour 11: 13-39.




================================================================================

Psyche
MASTERS. W. M.
1979.
Insect disturbance stridulation: its defensive role. Behav. Ecol. Soci obiol. 5: 187 200.
M~RT~N. E. S.
1977.
On the occurrence and significance of motivation- structural ru les in some bird and mammal sounds. Am. Nat. Ill: 855869. PERRY. G. AND Y. I.. WERM:R
198 1.
Food of P~oc/u~u.'i has.<it'/qt~ts/ti KIJ//UILJ.S (Reptilia: Gekkon i d ae) at two locations in Israel in summer. Proc. Zool. Soc. Israel in Isr. J . Zool.
30: 98-9.
sll~il;l,. S.
1956. Nonparametric Statistics. McGraw Hill. N.Y. SMITH. R. 1.. AND W. M. I.ANGI.I:Y
1978.
Cicada stress sounds: an assay of its effectiveness as a predator defense mechanism. Southwest Nt. 23: 187-96.
SOKAI.. R. R. AND F. J. RIIOI.I:
1969. Biometry. Freeman, San Francisco.
WERNER. Y.I..
1965.
U ber die Israelischen Geckos der Gattung P~,~.oda~ux u n d i hre Biologic. Salamandra 1: 15 25.
1976.
Optimal temperatures for inner-ear performance in gekkonid liza rds. J. EX^. Zool. 195: 319-352.
VARIH. G. C.
1939. Unusual methods of stridulation in a cicada (Cliclophleps c/i-sfanti (Van D.)) and a grasshopper ~O~~~luleonoius,fu.s~~i/~e.s Scud.) in Ca I i fo rnia. Proc. R. ent. Soc. Lond. A 14: 97- 100.




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