Scraping Sounds Produced by a Social Wasp (Asteloeca ujhelyii,

Hymenoptera: Vespidae)

Fabio S. Nascimento*, Michael Hrncir�, Adam Tolfiski� & Ronaldo Zucchi*

*Departamento de Biologia, FFCLRP, Universidade de Sao Paulo, Ribeirao Preto,SP Brazil; �Institute of Zoology, Biocenter, University of Vienna, Vienna, Austria;�Department of Pomology and Apiculture, Agricultural University, Krakow, Poland

Abstract

A distinct behavior performed by workers of the social wasp Asteloecaujhelyii is described: guard wasps, sitting outside of the nest around the entrancehole, scratch the nest envelope with their forelegs, thereby producing an audible�scraping sound�. Field observations revealed a relationship between the occur-rence of the scraping behavior and the occurrences of wasps entering and leavingthe nest. The scraping was experimentally reproduced in the laboratory bymoving a dissected wasp’s leg parallel to the plane of the nest envelope. Theresulting substrate-borne vibrations propagate very well over a distance of a fewcentimeters. The amplitude of these vibrations depends on the velocity of thescraping movements. The possible role of the scraping behavior in the wasps�communication is discussed.

Correspondence: Fabio S. Nascimento, Departamento de Biologia,FFCLRP, Universidade de Sao Paulo, Av. Bandeirantes, 3900, 14040-901,Ribeirao Preto, SP Brazil. E-mail: fsnascim@usp.br

Introduction

In neotropical swarm-founding wasps, most species live in large and complexcolonies, and sophisticated mechanisms of communication have evolved tocoordinate the activities among nestmates (Jeanne 1991). Although chemicallymediated communication during both alarm recruitment and swarm trailmigration have been well studied in epiponine wasps (Naumann 1975; Jeanne1981; West-Eberhard 1982; O’Donnell et al. 1997), the occurrence and commu-nicative function of sounds or substrate-borne vibrations remains poorly knownin almost all taxa. So far, the best-known example of such a �mechanicalcommunication� was studied in Synoeca surinama, which produces an audiblewarning signal by vibrating their wings on the nest envelope in response to adisturbance of the nest, (Evans & Eberhard 1970). Moreover, recent studies

Ethology 111, 1116—1125 (2005)

� 2005 Blackwell Verlag, Berlin

showed that Parachartergus colobopterus workers produce an alarm signal bytapping their abdomina against the nest carton (Strassmann et al. 1990; Jeanne &Keeping 1995).

In several species of Polistes, vibrations produced by body oscillations anddrumming against the nest surface are known to be used for communication(Hermann & Dirks 1975; Gamboa et al. 1978; Gamboa & Dew 1981; Pratte &Jeanne 1984; reviewed in Starr 1991; Savoyard et al. 1998). Oscillatorymovements of the body are generally performed by dominant females wheninspecting brood cells, and occur during interactions between adults and thebrood (Gamboa & Dew 1981; Pratte & Jeanne 1984). In Vespa orientalis, audiblesounds generated through abdominal vibrations against the comb signal the startof morning activities. Tapping the comb with the tarsi of the mid- and hindlegsoccurs in V. tropica during feeding the larvae (Ishay et al. 1974; Ishay 1977).

The aim of this paper is to describe the scraping behavior performed by theguard workers of Asteloeca ujhelyii, and to investigate whether activity offoragers affects this scraping behavior. Moreover, by moving a dissected wasp’sleg on the nest envelope, we imitated the behavior and studied the transmissionof substrate-borne vibrations on the nest envelope generated by the scrapingaction.

Materials and Methods

Species

Asteloeca ujhelyii, first described as Polybia ujhelyii by Ducke (1909), is amedium-sized wasp (body length, 11–12 mm), found in Amazonian Bolivia,French Guiana, and Brazil (Carpenter et al. 2004). Dome-like astelocyttarousnests are small to medium-sized (230–450 cells) and covered with a fragile-glossyenvelope (Wenzel 1998). Colonies of A. ujhelyii can contain from a dozen to a fewhundred adult individuals. The nest entrance is like an upward collar, whichallows the passage of a single wasp at a time. Additional information ontaxonomy and biology of Asteloeca species has recently been reported inCarpenter et al. (2004) and Nascimento et al. (2004).

Study Colony, Scraping Recordings, and Worker Specialization

Field studies were conducted between Jul. and Aug. 2001 at FazendaCatuaba (10�04¢36¢¢S 67�37¢40¢¢W), 20 km east of Rio Branco, Acre State,Brazil. A mature colony (labeled as colony A) was the main subject in thisstudy. Fifty-eight adult females and the nest were collected after theexperiments, but 116 females had been individually marked and observedthroughout the observations. Additional observations of scraping behaviorwithout video recordings were made with another young nest (colony B: 52individuals) located at a different site (Xapuri – Acre State, 10�49¢S 68�22¢W).Voucher specimens are deposited at the collections of Departamento de

1117Scraping Sounds in a Social Wasp

Biologia, Universidade de Sao Paulo, Ribeirao Preto, Brazil and AmericanMuseum of Natural History, NY, USA.

The scraping behavior and resulting sound were recorded with a digital Hi8Sony camcorder (TRV110) equipped with a microphone. Recording sessions weretaken either during morning or afternoon periods resulting in a total 60 h of fieldobservations. The video recordings were analyzed by detecting the events offoraging wasps entering and leaving the nest, and recording the time spent byother wasps with scraping within 10 s intervals preceding and following each ofthese events. Additionally, the amount of scraping was determined during theremaining 10 s intervals. If scraping occurred, the number of wasps involved wasrecorded. To test whether the occurrence of the scraping behavior was a responseto the transit of wasps, a Spearman’s correlation test was used to verify theassociation between the number of scraping wasps and the number of exiting andentering workers per sequence of behavior. To avoid ambiguous analysis, we onlyconsidered entrance/exit-scraping behavior as a sequence when they occurredwithin 3 s of observation.

All behaviors performed by marked wasps on the nest envelope werescanned and recorded. Worker specialization on scraping behavior was verifiedby comparing the distribution of the number of repetitions of the behavior byindividuals against the expectations of a Poisson’s distribution (Visscher et al.1999). We compared the frequency of scraping performed by workers facingthe nest entrance (named scrapers) and all other wasps sitting on the nestenvelope. In addition, during 2 d we observed the performance of thefollowing outside nest tasks: �scraping�, �fanning�, �receiving prey�, and �receivingliquid�. Only workers engaged in each behavior on at least four occasionsduring a given day were included in the analysis. Individual task specializationwas calculated using the Shannon–Wiener index (Lehner 1979; O’Donnell &Jeanne 1990):

HðxÞ ¼ �X

pðxÞ log2 pðxÞwhere p(x) is the proportion of a worker’s effort devoted to a given task (x).

Artificial Vibration Signals and Envelope Properties

To imitate the scraping action in the laboratory, we fixed a dissected wasp’sforeleg on the tip of a vibrator (V106, Ling Dynamic Systems, Royston,Hertfordshire, UK). Only the tarsal claws touched and scraped on the substratenear to the nest entrance. The movement of the leg was parallel to the envelope.Different amplitudes of the leg’s movement resulted in different scraping velocities(15.1, 8.0, and 3.8 mm/s). The vibrations (perpendicular to the surface of theenvelope, henceforth: vertical vibrations) elicited by the scraping were measuredat five different points on the envelope, using a portable laser vibrometer (PolytecPDV 100, Walbronn, Germany) connected to a notebook. The five points were:close to the source of the scraping (0 cm, reference point) and at distances of 1, 2,3 and 4 cm from the scraping point.

1118 F. S. Nascimento, M. Hrncir, A. Tolfiski & R. Zucchi

Signal Analysis

To analyze the scraping sounds recorded in the field, and the substrate-bornevibrations generated in the laboratory experiments, we used the sound-analyzingcomputer programs spectra pro 3.3 and sound forge 4.0, respectively.

Results

Scraping Behavior

During daytime, there was a group of 8–37 workers (�x� SD ¼17.73 ± 12.47 wasps, n ¼ 3 nests, 24 h/colony) sitting on the outer surface ofthe A. ujhelyii nests. Most of the workers remained almost completely inactive butone to four (�x� SD ¼ 2.2 ± 1.14 wasps, n ¼ 3 nests, 24 h/colony) of themfrequently performed scraping behavior. This distinct behavior consisted ofworkers repeatedly moving their forelegs back and forth while the tarsal clawshad contact with the envelope surface. The performing scraping behavior waspositioned close to the nest entrance and facing it. Occasionally, they insertedtheir antennae into the entrance hole. The number of scraping workers duringperiods of intense activity (measured by the number of wasps leaving or enteringthe nest per hour) tended to be higher than during periods of foraging inactivity(rs ¼ 0.71, p < 0.0001; y ¼ 3.51 + 1.71x; n ¼ 27 h).

The scraping time was significantly shorter during the 10 s intervals withoutactivity (2.9 ± 3.82 s; n ¼ 406 intervals; Fig. 1a) than during intervals precedingand following an event of wasps entering (7.7 ± 3.03 s; n ¼ 106 intervals;Fig. 1b; Mann–Whitney test: Z ¼ 10.62, p < 0.001) or leaving the nest(6.9 ± 3.53 s; n ¼ 114 intervals; Fig. 1c; Mann–Whitney test: Z ¼ 9.33,p < 0.001). However, there was no difference between the intervals with waspentering and the intervals with wasp leaving the nest (Mann–Whitney test: Z ¼1.66, p ¼ 0.096, n1 ¼ 106, n2 ¼ 114).

During the intervals preceding events of a wasp entering the nest, the time ofscraping was shorter than during intervals following the event (�x� SD:7.0 ± 3.40 and 8.4 ± 2.44 s, respectively; Mann–Whitney test, Z ¼ )2.14,p < 0.05, n1 ¼ n2 ¼ 53). Moreover, during intervals preceding the forager’sdeparture from the nest wasps scraped significantly less than after the event(�x� SD: 6.0 ± 3.81 and 7.7 ± 3.04 s, respectively; Mann–Whitney test, Z ¼)2.93, p < 0.01, n1 ¼ n2 ¼ 57).

Scrapers were highly specialized workers. They devoted 95% ± 4.3 (n ¼ 26)of the time observed to this task. The Shannon–Wiener specialization index was0.7 ± 0.27 (n ¼ 26), supporting specialization among scrapers. Other wasps onthe nest occasionally scraped the envelope, but the distributions were far differentfrom a random Poisson’s distribution (Fig. 2a. Colony A: D ¼ 0.73, p < 0.01,n ¼ 76; Colony B: D ¼ 0.63, p < 0.01, n ¼ 22). The group of specializedworkers scraped significantly more than the other wasps sitting on the nestenvelope (Colony A: t-test ¼ 7.74, df ¼ 74, p < 0.001; Colony B: t-test ¼ 7.97,

1119Scraping Sounds in a Social Wasp

df ¼ 49, p < 0.001). There were overlapping of tasks functions performed byworkers on the nest, but scraping workers were specialized in their function atleast 3 d within the period of observation. In general, workers engaged inreceiving food and water before starting as scrapers, and in foraging activitieslater (F.S. Nascimento, unpub. data).

Fig. 1: Distributions of scraping times during: (a) 10 s intervals without wasps entering or leaving thenest, (b) intervals preceding and following an event of wasp entering the nest and (c) intervalspreceding and following an event of wasp leaving the nest. There was no scraping in more than 50% ofintervals without wasp entering or leaving the nest (a) in contrast to less than 10% of intervals with

wasp entering or leaving the nest (b and c)

1120 F. S. Nascimento, M. Hrncir, A. Tolfiski & R. Zucchi

Scraping Noise

The scraping behavior of the wasps resulted in an audible, broad-bandedfrequency sound (Fig. 3) which could be perceived by human ear even from adistance of 2 m from the nest. A dominant frequency of about 1430 Hz(1428 ± 69 Hz, n ¼ 10; Fig. 3) contained within the broad-banded noise couldbe attributed to the scraping.

Scraping per individual0 10 20 30 40 50 60 70 80 90 100 110 120

0

10

20

30

40

50

60

Num

ber

ofw

orke

rs

Colony AColony B

Fig. 2: Number of wasps that scraped the nest envelope during 3 d of observation in the colony A(black bars) and colony B (white bars)

Fig. 3: Example of the scraping sound produced by three workers of A. ujhelyii. The sonogram showsthe broad frequency spectrum of the scraping noise. Vertical lines indicate the entire period of thescraping, DF indicates the dominant frequency of the spectrum that can be attributed to the scraping.

Note the noisy background that impeded a more detailed analysis of the scraping sound

1121Scraping Sounds in a Social Wasp

Artificial Scraping and Transmission Properties of the Nest Envelope

In the laboratory, we imitated the scraping by moving a wasp’s leg (mountedonto a vibrator) parallel to the nest envelope with only the tarsal claws touchingthe substrate. Scraping the envelope this way near the nest entrance resulted invertical vibrations of the substrate (Fig. 4a) which could be measured at any pointof the envelope. Independent of the velocity of the leg’s movement, the substrate-borne vibrations elicited by the scraping movement showed a main frequency of700 Hz and its harmonics (1400 and 2100 Hz) (Fig. 4b). However, the velocityamplitude of the vertical substrate vibrations depended on the velocity of the leg’smovement. At the scraping point (0 cm, reference point), the velocity of the

Fig. 4: Artificial scraping. A wasp’s leg attached to a vibrator was used to imitate the scrapingbehavior observed in the field. (a) The movement of the leg parallel to the nest envelope (top) resultedin vibrations perpendicular to the substrate (bottom). (b) The main frequency (MF) and its harmonics(H1, H2) of the substrate vibrations elicited by the scraping were similar at all studied scrapingvelocities (15.1 mm/s, open triangles; 8.0 mm/s, open squares; 3.8 mm/s, filled circles). The amplitude(dB) is given in relation to the maximum measured (0 dB). (c) The nest envelope amplified frequenciesaround 500 Hz. The relative transmission (dB/cm) was calculated as the frequency amplitude measuredat a given distance in relation to the amplitude of this frequency at the point of scraping (reference,

0 dB). Symbols are same as in (b).

1122 F. S. Nascimento, M. Hrncir, A. Tolfiski & R. Zucchi

vertical vibrations was about half of the scraping velocity, and the vibrationamplitude decreased with increasing distance to the scraping point (Table 1). Inorder to study which frequencies of the substrate vibrations elicited by thescraping are best transmitted across the nest envelope, we analyzed the envelope’stransmission properties. Indifferently of the velocity of the scraping movement,vibration frequencies of around 500 Hz were amplified across the envelope(Fig. 4c). The transmission of frequencies above 700 Hz differed between thedifferent scraping velocities. However, the transmission of frequencies below700 Hz was similar at all studied velocities of the leg’s scraping movements(Fig. 4c).

Discussion

In the present study we described for the first time a behavior performed byguards of A. ujhelyii wasps. The guards occasionally produced audible sounds byscraping the nest envelope with their forelegs. We clearly demonstrated that thisbehavior occurred mainly when other wasps were entering or leaving the nest. Thescraping started before a wasp arrived or left the nest and continued for some timeafterwards. The scraping before a wasp entered the nest was triggered by clearlyvisible returning foragers. However, it is more difficult to explain how thescrapers, sitting outside the nest, perceived foragers approaching the nest entrancefrom inside. Although we do not know what happens inside the nest we assumethat scrapers receive a signal just before foragers go out of the nest.

We demonstrated that substrate-borne vibrations are elicited when adissected wasp’s leg is moved repeatedly along the surface of the nest envelope.Unfortunately, we had no opportunity to record the velocity of the scrapingmovements by the wasps in the field. However, our experiments demonstratethat both the main frequency of the substrate vibrations generated by scrapingand the amplification of frequencies below 700 Hz by the nest envelope wereindependent from the velocity of the scraping movement (Fig. 4). Moreover,artificial movements from the leg with 8.0 mm/s produced a similar frequencyfound in the field, thus it could indicate that in nature wasps move their legs

Table 1: Substrate-borne vibrations elicited by scraping. Artificial scraping movements ofthree different movement velocities (15.06, 7.98, and 3.76 mm/s peak–peak) inducedvibrations of the nest envelope. The velocity amplitude (peak–peak) of these substrate-borne vibrations was measured at different distances from the point of scraping (0 cm) near

the nest entrance

Scrapingvelocity(mm/s)

Response (mm/s)

0 cm 1 cm 2 cm 3 cm 4 cm

15.06 6.73 5.10 4.20 2.48 1.627.98 3.52 2.39 1.97 1.13 0.793.76 1.73 1.14 1.03 0.55 0.37

1123Scraping Sounds in a Social Wasp

very close to this velocity during the scraping. In hymenopterans the ability todetect substrate-borne vibrations has been predominantly attributed to thesubgenual organ, a chordotonal organ in the proximal part of the tibia of eachleg (Autrum & Schneider 1948). This vibration sensitive organ reacts tovibrations in the axial direction of the tibia. Hence the sensory cells arepredominantly stimulated by vertical vibrations (perpendicular to the substrateon which the animal stands) (Rohrseitz & Kilpinen 1997). The subgenual organof honey bees (Apis mellifera) is most sensitive to substrate-borne vibrations atfrequencies of 500 Hz (Kilpinen & Storm 1997). Interestingly, the nest envelopeof A. ujhelyii amplifies vibration frequencies around 500 Hz (Fig. 4c). Unfor-tunately, no detailed study on the vibration sensitivity in wasps is available.However, our findings that substrate vibrations are elicited by scrapingmovements, and that the nest envelope transmits and even amplifies frequenciesthat could be relevant for the animal’s perception, give reason to suggest thatthe scraping could well be used as signal in these wasps. Previous studies inVespidae showed that the vibrations transmitted via the nest envelope canprovide information about food availability (Pratte & Jeanne 1984 andreferences therein) and about the presence of enemies. In fact, some evidencein Synoeca spp. and P. colobopterus indicate that a generalized warning signalcan be transmitted across the nest envelope in response to human disturbances,army ant attacks or parasitoids (Chadab 1979; West-Eberhard 1982; Strassmannet al. 1990; Jeanne & Keeping 1995).

We assume that scraping behavior in A. ujhelyii could be associated withcolony defense as well. It is performed by guards and occurs mainly when waspspass the nest entrance. We hypothesize that the small nest entrance is guardedboth inside and outside the nest envelope. The vibration produced duringscraping behavior can inform the guards on the other side of the envelope whetherthat the wasp passing the nest entrance is a nestmate or an enemy. This wouldmake defense against enemies more effective. However, more data about thebehavior of wasps during colony defense are needed to verify this hypothesis.

Acknowledgements

Part of this study was presented in the XXVIII International Ethological Conference. Theauthors thank to Jim Carpenter and two anonymous reviewers for helpful comments on themanuscript, and Jim Hunt for stimulating discussion on the scraping behavior. Financial support toF.S.N. was provided by Fapesp (Procs. 02/12540-9 and 03/10663-5).

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Received: December 10, 2004

Initial acceptance: March 22, 2005

Final acceptance: April 8, 2005 (S. Forbes)

1125Scraping Sounds in a Social Wasp