Vibrational/substrate communication in insects

Transcription

1 Rocio Villanueva 1 Vibrational/substrate communication in insects What is vibrational/substrate communication and why is it used? o Signal in which most of its energy is propagated in a solid substrate (Stolting et al. 2002) o An often practiced communication in insects, where different substrates provide a way by which signals can be transmitted o Especially important for ground-dwelling insects o Can be used to communicate with members of same species o Acoustic signaling is one of the major modes of communication in insects (Bailey 1991 in Hirschberger 2000) o Widespread form of communication, mainly used for defense, mate attraction and aggression displays (Travassos & Pierce 2000) o Vibrations produced in ways including: percussion (drumming), tremulation (abdominal or body jerking), tymbal clicking, stridulation, and combinations of these methods (Stewart 1997) Percussion: striking of body part (abdomen) directly on substrate drumming Single, low frequency vibration wave Tremulation: some form of body jerking, without striking the surface Low frequency, transverse waves Used by katydids, crickets, stoneflies, alderflies, female planthoppers, etc Sounds produced in this manner are not sensed by potential predator o Disadvantage for insects who use this due to complex wave transmission in heterogenous substrates in their habitat (Stewart 1997) o Producing vibrations cost less energy than producing high-frequency airborne sounds (Stewart 1997) Can t obtain information on behavior from fossil record, so little is known History o First discovered in insects o New and intriguing ideas arise continuously a growing field o Ancestral method of signal production in Plecoptera is percussion (Stewart 1997) Variety of substrates used o Plants (most popular) Insects in general use plant stems, leaves and roots as substrates touching leaves, stems or roots can transfer signals from one plant to the other when insects reach a branching point, they must decide which one to take (like N. viridula) (Ota & Cokl 1991)

2 Rocio Villanueva 2 Abiotic factors influence capability of detecting vibratory signals Wind usually interferes with plant-borne vibrations, and rain can be a factor as well (especially at low frequencies) (Casas et al. 1998) Small insects who can t emit airborne sounds efficiently at low frequencies communicate w/vibratory signals transmitted through plants (Miklas et al. 2001) Many insects communicate w/broad band vibratory songs b/c it s more likely that some of the frequency bands will get through to the receiver (Miklas et al. 2001) Use bending waves (Pavlovcic & Cokl 2001) Conflict: narrow band vibrations of frequencies of approximately 100 Hz are characteristic for songs produced by body vibration (Ewing 1989 in Blassioli-Moraes et al. 2005) Stink-bug species (T. pallidovirens and T. c. accerra) use it to find each other in the complexity of plants (McBrien et al. 2002) Unanswered questions: does the use of different host plant species generate divergent selection on signals? (Cocroft & Rodriguez 2005) Balclutha incise by vibrations of abdomen (Nuhardiyati & Bailey 2005) Number of pulse components help female decipher male information (status or quality) Signal attenuation is greater during transmission through lamina than veins (Cokl et al. 2004) Prolongation of vibratory signals increase w/decreasing signal duration (Cokl et al. 2000) Enchenopa binotata form mating pairs after exchange of plant borne vibrational signals (Rodriguez et al. 2004) Calloconophora pinguis communicate by means of vibrational signals along stems and leaves of host plants (Cocroft 2005) Spissistilus festinus communicate through plant vibrational signals (Hunt 1993) Atta cephalotes use plant leaves as their medium of signal transport (Roces & Holldobler 1995) A. hilare, green stink bug, uses plants (much like N. viridula) (Cokl et al. 2001) Plecoptera use plant as their substrate for communication, and their vibrational communication is thought to be the most complex (Stewart 1997) o Water Water striders (Hill 2001) o Soil

3 Rocio Villanueva 3 o Air Male prairie mole cricket, Gryllotalpa major produce vibrations w/same temporal scale and pattern as the airborne signal through an unknown mechanism (Hill & Shadley 2001) Stridulation with the file-and-scraper mechanism produce the song and is sufficient to set up the vibrations (this is also seen in the leaf-cutter ant) Leaf vibrations by leafminer induce air movements in immediate surrounding in (Casas et al. 1998) N. viridula perform airborne sounds (Miklas et al. 2001) o Dung Airborne signals by males of North American cicada Okanagana rimosa induce substrate vibrations (Stolting et al. 2002) Energy signals generated by timbals of males induce loud airborne sounds and consequently induce strong vibrations in the substrate as well Among tetiigoniids, airborne sound-induced vibrations as well as vibratory signals have been found (Stolting et al. 2002) J. evagoras produce vibratory and airborne signals (Travassos & Pierce 2000) Signals can be absorbed, refracted, and attenuated by plant leaves (Bell 1980; Michelsen et al. 1982; in Ota & Cokl 1991) Aphodius ater by means of an abdominolary stridulatory organ (Hirschberger 2000) Communication for o Known to be used during or after disturbance serve in different behavioral contexts o Mating Sexual communication system is important for fertilization mechanism, it lets individuals find each other under natural conditions and has been called the specific-mate recognition system (SMRS) (Jeraj & Walter 1998) Stridulation in Aphodius ater (dung-beetles), where female presence is crucial to male stridulation (Hirschberger 2000) Stink-bug species (T. pallidovirens and T. c. accerra) use it to find each other in the complexity of plants (McBrien et al. 2002) Better signal by male usually results in female choice b/c signal quality is often correspondent with reproductive success N. viridula produce vibrations after being attracted to each other by pheromones V. arquata number, distribution, and behavior of conspecifics (social environment features) should be taken into account b/c it might be a source of selection (Cocroft 2003) N. viridula female calls vibratory stimulus duration, repetition rate, amplitude, and frequency determine the level of male response (Miklas et al. 2001)

4 Rocio Villanueva 4 Gryllotalpa major males produce signals to attract females to their acoustical burrow (Hill & Shadley 2001) Songs emitted during mating by male and female Holcostethus strictus (Pavlovcic & Cokl 2001) Male katydid Conocephalus nigropleurum produce vibrations in courtship and mate attraction (Luca & Morris 1998) Males perform tremulation a vibratory behavior where with all six legs on substrate, he oscillates quickly without touching the substrate itself (Bell 1980; Morris 1980 in Luca & Morris 1998) Encodes critical information on body size, and females prefer larger males (produce shorter inter-pulse interval so tremulation signal occurs more often) Acrosternum hilare, green stink bug, produces vibrations to attract mates (Cokl et al. 2001) Spissistilus festinus males and females use vibrational signals to attract each other (Hunt 1993) o Warning Male vs. male competitive interactions (Cocroft & Rodriguez 2005) Vibrational cues are thought to initiate chorusing behavior in Graminella nigrifrons males, which are used in courtship disruption (Hunt & Morton 2001) To let others know that s your feeding site, like drepanid moth larvae (Cocroft & Rodriguez 2005) Alarm uses by termites (Howse1964), ants (Markl & Fuchs 1972), and land bugs (Gogala 1985b) (Stewart 1997) o Activity information Feeding and locomotion vibrations Cleaning call in the male leafhopper Balclutha incise (Nuhardiyati & Bailey 2005) Dancing bees use vibration to communicate with rest of hive (Sandeman et al. 1996) Larvae of Phelypera distigma (weevil) vibrate when moving or in contact w/ conspecifics (Costa et al. 2004) C. pinguis vibrate to communicate w/rest of group when discover a new feeding site (Cocroft 2005) In leaf-cutting ant Atta cephalotes foraging column, the smallest workers hitchhike on leaf fragments carried by large workers and sense them by stridulatory vibrations produced by large workers while cutting the leaf (Roces & Holldobler 1995) o Member detection along some distance In stink-bug species (T. pallidovirens and T. c. accerra) who find each other in plants (McBrien et al. 2002) Mating behavior on ivy suggest directionality cue from female song (Cokl et al. 1999)

5 Rocio Villanueva 5 N. viridula communicate by long-range calling and close-range courting, rivalry and repelling (Cokl et al. 2000) Mate location on the ivy Hedera helix (Ota & Cokl 1991) P. mesaensis uses vibrations in sand to determine both direction and distance of prey species (Hill 2001) o But, predators and parasitoids can also sometimes hear/feel vibrations Has to be kept in mind that this type of communication is thought to reduce the likelihood of eavesdropping by natural enemies (Hunt & Morton 2001) Feeding and locomotion vibrations used by predators to find their prey or vice versa (Cocroft & Rodriguez 2005) For example, how spiders may be attracted by katydids; insects in general attract predatory ants, true bugs (Hymenoptera) and other predatory insects Vibrocrypticity lets some insects move past predators without them noticing, because of unnoticeable vibrational production (Cocroft & Rodriguez 2005) Unanswered questions: to explore potential for predators to exploit insect vibrational communication (Cocroft & Rodriguez 2005) Vibrations in Okanagana rimosa may have helped in evolution of the ear in a group of parasitoid flies (Stolting et al. 2002) Why has it been successful? o Species specific T. pallidovirens and T. c. accerra differ in their songs from other previously studied pentatomid species (McBrien et al. 2002) N. viridula female song is only species-specific cue for locating a mate in that species (Cokl et al. 1999) Conflict: male courtship song enables species recognition (Cokl et al. 2000) N. viridula from Australia and Slovenia cannot communicate well with each other due to their species specific calls no mating between individuals of two separate populations (Ryan et al. 1996) So N. viridula males from different populations respond differently to the same stimulus and they can differentiate calling songs of females of different geographical origin (Miklas et al. 2001) Conflicting evidence: Slovenian females and Australian males do not respond, but Slovenian females and Australian males respond and copulate regularly (Jeraj & Walter 1998) ((is this happening because they were under laboratory conditions?)) o Differences in the song repertoire of Slovene and Brazilian populations were shown to be genetically determined (Pavlovcic & Cokl 2001)

6 Rocio Villanueva 6 When butterfly species J. evagoras and ant-symbioses communicate, they do so through vibrational signals, so not all calls are species specific (Travassos & Pierce 2000) Pupae produce sound when disturbed, w/intro of a conspecific larva, and presence of attendant ants of I. anceps H. strictus male courtship songs show highest level of species specificity among vibrational songs in Pentatomidae (Pavlovcic & Cokl 2001) M. histrionica produce species specific songs (Cokl et al. 2004) E. binotata use vibrational communication (Michelsen et al. 1982; Gogala 1985 in Rodriguez et al. 2004) Social interactions between parents and offspring, siblings and mates (Hunt et al. 1992; Hunt 1993, 1994; Cocroft 1996, 1999a, b, 2001 in Rodriguez et al. 2004) o Sex specific Nomadically foraging species signaling plays a role in the formation of foraging groups (Cocroft 2001; Greenfield 2002 in Cocroft 2005) Plecoptera have complex, species specific male-female exchanges (Stewart 1997) Interval, rate, length and additional pulses all indicate energy, and male Balclutha incise with succeeding components get the female (Nuhardiyati & Bailey 2005) N. viridula use sound vibrations for sexual sound communication (Ryan et al. 1996) Acrosternum impicticorne, Euschistus heros, Piezodorus guildinii and Thyanta perditor communicate w/sex specific vibratory signals (Blassioli-Moraes et al. 2005) o Large predators might not hear/fell the vibrations Species that complete development on a single stem use vibrational communication for an anti-predator function (Cocroft 2005) A. cephalotes use stridulatory vibrations to communicate between castes about parasites (Roces & Holldobler 1995) o May be important in mediating ant-symbioses Males and females perform songs o Pupal cells, larvae and adults communicate in this manner 2 kinds of pupal calls and three larval calls have been noted in the common blue butterfly, Jalmenus evagoras (Travassos & Pierce 2000) Calls from both play a significant role in the communication between J. evagoras and its attendant ants; pupal calls are thought to be more than just signals to deter predators o Males usually sing first and females respond in some way (but there are

7 Rocio Villanueva 7 some exceptions) Only males perform vibrations while females may only chirp at end of song in Aphodius ater (dung-beetles) (Hirschberger 2000) Female stink-bug species (T. pallidovirens and T. c. accerra) can vibrate first and then males respond (McBrien et al. 2002) N. viridula Australian males always call first in homogametic duets (Jeraj & Walter 1998) Female songs in N. viridula are performed first and trigger male approaches with typical search behavior, who then perform a courtship song (Miklas et al. 2001) M. histrionica males perform vibrational signals first (Cokl et al. 2004) Mainly produced to reach short distances A. hilare females produce vibrational signals first (Cokl et al. 2001) o More than one song may be performed by each insect Aphodius ater perform both a basic and rhythmic song, after which they are known to copulate (Hirschberger 2000) T. pallidovirens and T. c. accerra have a calling and copulating song (McBrien et al. 2002) Density related changes in signaling behavior by V. arquata (Cocroft 2003) N. viridula females perform vibrational pulses that include either short pulses and long pulses (FCS-1) or just short pulses (FCS-2) songs are well suited for efficient transmission in plants (Miklas et al. 2001) J. evagoras pupae produce three distinct signals (Travassos & Pierce 2000) Grunts (produced during ant attendance), hisses (produced in the 1 st 5 min after discovery by a worker ant), drumming (can be produced by tended or untended larvae) Males of Murgantia histrionica (harlequin bug) produce 5 different vibrational songs while females only produce one (Cokl et al. 2004) o Overlapping duets are possible a temporary pair-bond? Stink-bug species T. pallidovirens and T. c. accerra, during the calling phase (McBrien et al. 2002) Leafhopper Balclutha incise w/female signal after136 ms of male s call If an N. viridula of the opposite sex recognizes vibratory signals, responds appropriately to them, then a duet is set up followed by copulation (Jeraj & Walter 1998) H. strictus emit duet songs during copulation (Cokl et al. 2004) E. binotata mating occurs after a duet (Rodriguez et al. 2004) Pair formation plays a role in reproductive isolation

8 Rocio Villanueva 8 Females of the stonefly Pteronarcella badia can distinguish between fit and unfit males by time they take to find her after a duet (Stewart 1997) o Songs are usually low wavelength (high frequency) Conflict: low frequency in plant vibrations (Gogala 1984 in Cokl et al. 2000) Sounds of Hz by Aphodius ater (Hirschberger 2000) N. viridula (and many other terrestrial pentatomid bugs) perform dominant frequencies between 80 and 150 Hz (Miklas et al. 2001) Between 85 and 123 Hz (Cokl et al. 2000) Signals at around 100 Hz are best suited for transmission properties of plants (Miklas et al. 2001) Only small frequency of vibration changes less than 10% may change the vibration amplitude by 10 to 30 db (Miklas et al. 2001) Songs by O. rimosa have its energy peak at around 7-10Hz. These and other cicadas can discriminate different frequencies important for signal recognition (Stolting et al. 2002) Gryllotalpa major produce energy spikes in the range of 30 to about 300 Hz (Hill & Shadley 2001) J. evagoras pupae produce 7.5 metallic click-like pulses per second, each w/ a frequency of 2300 Hz (Travassos & Pierce 2000) Holcostethus strictus vibrational signals have a dominant frequency peak between 100 and 260 Hz (Pavlovcic & Cokl 2001) o Songs can be as short as 150 ms But can be as long as 3 hr in Aphodius ater (Hirschberger 2000) N. viridula males pulses less than 300ms (Cokl et al. 2000) o Insects sense vibrations mainly by their legs Since walking reduces the number of legs in contact w/the substrate, insects stop to detect signals Different combinations of leg and antennae sequences are used by Nezara viridula to compare vibratory signals (Cokl et al. 1999) Dancing bees detect vibrations by the legs. Organ not known but not subgenual organ (most sensitive to frequencies between 300 and 600 Hz not what s used by the bees) and so might be tibiofemoral and tibio-tarsal joints (Sandeman et al. 1996) M. histrionica detect vibrations by legs (Cokl et al. 2004) Atta cephalotes minim workers (smallest ones) sense vibrations by their legs (Roces & Holldobler 1995) General information: o Alteration of songs may be due to an inhibitory-resetting mechanism o Helps group-living herbivorous insects to exploit plant resources Leaf-cutter ants communicate to let others know when they found good resources, especially if they are a high-quality substrate for growing fungi (Cocroft & Rodriguez 2005)

9 Rocio Villanueva 9 Can also help them avoid predation, where an individuals signaling probability is directly correlated with its risk of predation (Cocroft & Rodriguez 2005) Further studies need to be done with social insects Important for locating and remaining in a group, locating food resources and avoiding predation (Cocroft 2001) Group living sawfly Perga dorsalis, chrysomelid beetle Polychalma multicava, and many others Membracid treehoppers Calloconophora caliginosa and C. pingius nymphs search for new shoots and produce vibrations to inform others Membracid treehopper Umbonia crassicornis nymphs produce vibrations to call mom so she can protect them from invertebrate predators o Vibrations are analyzed by their spectral properties Frequency spectra of airborne sounds and vibrations have identical ranges, but more energy in low frequencies in the vibrations (Stolting et al. 2002) o Calling involves high energy consumption and so increases the risk of predation o Distances of vibration reach differ from commonly being 30cm-2 m and in large insects up to 2m-4m (Cocroft & Rodriguez 2005)

10 Rocio Villanueva 10 Bibliography. Blassioli-Moraes MC, Laumann RA, Cokl A, Borges M (2005) Vibratory signals of four Neotropical stink bug species. Physiological Entomology 30: Casas J, Bacher S, Tautz J, Meyhofer R, Pierre D (1998) Leaf vibrations and air movements in a leafminer-parasitoid system. Biological Control 11: Cocroft RB (2001) Vibrational communication and the ecology of group-living, herbivorous insects. American Zoologist 41: Cocroft RB (2003) The social environment of an aggregating, ant-attended treehopper (Hemiptera: Membracidae: Vanduzea arquata). Journal of Insect Behavior 16: Cocroft RB (2005) Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proceedings, Biological sciences 272: Cocroft RB, Rodriguez RL (2005) The behavioral ecology of insect vibrational communication. BioScience 55: Cokl A, Presern J, Virant-Doberlet M, Bagwell GJ, Millar JG (2004) Vibratory signals of the harlequin bug and their transmission through plants. Physiological Entomology 29: Cokl A, Virant-Doberlet M, McDowell A (1999) Vibrational directionality in the southern green stink bug, Nezara viridula (L.), is mediated by female song. Animal Behaviour 58: Cokl A, Virant-Doberlet M, Stritih N (2000) The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia. Physiological Entomology 25: Cokl A, McBrien HL, Millar JG (2001) Comparison of substrate-borne vibrational signals of two stink bug species, Acrosternum hilare and Nezara viridula (Heteroptera: Pentatomidae). Annals of the Entomological Society of America 94: Costa JT, Fitzgerald TD, Pescador-Rubio A, Mays J, Janzen DH (2004) Social behavior of larvae of the Neotropical processionary weevil Phelypera distigma (Boheman) (Coleoptera: Curculionidae: Hyperinae). Ethology 110: De Luca PA, Morris GK (1998) Courtship communication in meadow katydids: female preference for large male vibrations. Behaviour 135: Hill PSM (2001) Vibration as a communication channel: A synopsis. Integrative and Comparative Biology 41:

11 Rocio Villanueva 11 Hill PSM, Shadley JR (2001) Talking back: sending soil vibration signals to Lekking prairie mole cricket males. American Zoologist 41: Hirschberger P (2000) Stridulation in Aphodius dung beetles: Behavioral context and intraspecific variability of song patterns in Aphodius ater (Scarabaeidae). Journal of Insect Behavior 14: Hunt RE (1993) Role of vibrational signals in mating-behavior of spissistilus-festinus (Homoptera, Membracidae). Annals of the Entomological Society of America 86: Hunt RE, Morton TL (2001) Regulation of chorusing in the vibrational communication system of the leafhopper Graminella nigrifrons. American Zoologist 41: Jeraj M, Walter GH (1998) Vibrational communication in Nezara viridula: a response of Slovenian and Australian bugs to one another. Behavioural Processes 44: McBrien HL, Cokl A, Millar JG (2002) Comparison of substrate-borne vibrational signals of two congeneric stink bug species, Thyanta pallidovirens and T. custator accerra (Heteroptera: Pentatomidae). Journal of Insect Behavior 15: Miklas N, Stritih N, Cokl A, Virant-Doberlet M, Renou M (2001) The influence of substrate on male responsiveness to the female calling song in Nezara viridula. Journal of Insect Behavior 14: Nuhardiyati M, Bailey W (2005) Calling and duetting behavior in the leafhopper Balclutha incise (Hemiptera: Cicadellidae: Deltocephalinae): Opportunity for female choice? Journal of Insect Behavior 18: Ota D, Cokl A (1991) Mate location in the southern green stink bug, Nezara viridula (Heteroptera: Pentatomidae), mediated through substrate-borne signals on ivy. Journal of Insect Behavior 4: Pavlovcic P, Cokl A (2001) Songs of Holcostethus strictus (Fabricius): a different repertoire among landbugs (Heteroptera: Pentatomidae). Behavioural Processes 53: Roces F, Holldobler B (1995) Vibrational communication between hitchhikers and foragers in leaf-cutting ants (Atta cephalotes). Behavioral Ecology and Sociobiology 37: Rodriguez RL, Sullivan LE, Cocroft RB (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution 58:

12 Rocio Villanueva 12 Ryan MA, Cokl A, Walter GH (1996) Differences in vibratory sound communication between a Slovenian and an Australian population of Nezara viridula (L.) (Heteroptera: Pentatomidae). Behavioural Processes 36: Sandeman DC, Tautz J, Lindauer M (1996) Trasmission of vibration across honeycombs and its detection by bee leg receptors. The Journal of Experimental Biology 199: Stewart KW (1997) Vibrational communication in insects: epitome in the language of stoneflies? American Entomologist 43: Stolting H, Moore TE, Lakes-Harlan R (2002) Substrate vibrations during acoustic signaling in the cicada Okanagana rimosa. Journal of Insect Science 2: 1-7 Travassos MA, Pierce NE (2000) Acoustics, context and function of vibrational signaling in a lycaenid butterfly-ant mutualism. Animal Behaviour 60: 13-26