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Testing the disturbance hiss of the Madagascar hissing Cockroach (Gromphadorhina portentosa) as an anti-predatory response

Testing the disturbance hiss of the Madagascar hissing Cockroach (Gromphadorhina portentosa) as... BioscienceHorizons Volume 7 2014 10.1093/biohorizons/hzu010 Research Testing the disturbance hiss of the Madagascar hissing Cockroach (Gromphadorhina portentosa) as an anti-predatory response Robin Shotton* Institute of Science and the Environment, The University of Worcester, Henwick Grove, Worcester WR2 6AJ, UK *Corresponding author: 72 Pearce Close, Dudley, West Midlands DY1 2LX, UK. Email: rob.karen101112@gmail.com Project Supervisor: Dr Debbie Holmes, Institute of Science and the Environment, The University of Worcester, Henwick Grove, Worcester WR2 6AJ, UK. The display of the disturbance hiss by the Madagascar Hissing Cockroach (Gromphadorhina portentosa) is considered to be an anti-predatory response despite there being little direct evidence linking the hiss with survival. Many studies have investi- gated the roles of the aggression and courtship hisses, displayed in this social species, but few have considered the role of the disturbance hiss. This study looked at the stimulus for the disturbance hiss response by placing unfamiliar individuals into different social contexts. A total of 10 male and 10 female G. portentosa were kept separately before being placed into four different social situations for 5 min at a time. The individuals were placed into an established colony of all females, an estab- lished colony of all males and an established colony of mixed sex G. portentosa. The subjects were also placed in the presence of a predator, an Emperor Scorpion (Pandinus imperator Koch). All interactions and hisses were recorded both by video and on a sound-recording device. There was a highly significant difference in the setting in which the disturbance hiss was shown and a highly significant difference in the display rates of the disturbance hiss between the sexes in general, with most displays of the disturbance hiss being when introduced to a mixed sex colony. The findings suggest that the role of the disturbance hiss is not an anti-predatory response when presented with a predator of limited auditory senses. Further study into the behav- ioural ecology of this species is recommended to understand the range of anti-predatory responses used by this species when presented with different predators. It was also found that there is some social context for the display of the disturbance hiss which warrants further study. Key words: hissing cockroach, Gromphadorhina portentosa, disturbance hiss, anti-predator, behavioural ecology, startle response Submitted on 9 December 2013; accepted on 12 October 2014 Introduction air through the respiratory spiracles, a hiss is emitted that serves as an auditory social signal. The hiss takes three The large, wingless cockroach Gromphadorhina portentosa recognized forms: aggression, courtship and disturbance (Schaum) is a long-lived social arthropod with a lifespan of (Nelson and Fraser, 1980; Clark and Moore, 1995a). between 2 and 5 years which is endemic to the tropical low- The aggression hiss is displayed by the male during agonistic land forests of Madagascar (Clark and Shanklin, 2013). encounters which form hierarchies within the colony (Clark and The species has the unique ability among insects of being Moore, 1995b). The courtship hiss is again only displayed by able to communicate using modified spiracles on its abdomen males and is essential for successful mating (Clark and Moore, (Nelson and Fraser, 1980). Most other invertebrates commu- 1995a). It is thought that females may use the hiss to elicit pref- nicate by stridulation, rubbing body parts together. By forcing erence in mating by choosing larger, more dominant males © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Research Bioscience Horizons • Volume 7 2014 (Nelson and Fraser, 1980; Schal et al., 1984; Clark and Moore, A sample of 20 healthy adult individuals (10 male, 10 1995b). The third type of hiss, the disturbance hiss, is easily female) were purchased from Ebay.co.uk (seller zoocentre) identifiable from the others as it is both the loudest in amplitude prior to the study at the penultimate sixth instar to ensure that and shortest in frequency (Nelson and Fraser, 1980). This hiss is they were all of the same age. Differentiation between the classified as an anti-predatory response and is displayed by all sexes is relatively easy. After the fourth instar, males are larger members of this species past the fourth instar (Clark and Moore, and possess a large pair of horns on their pronotum as well as 1995a) (full maturity is reached upon the sixth instar at around hairy antennae (Clark and Shanklin, 2013). These individuals 7 months). This particular hiss was also demonstrated in a study were separated and placed in numbered plastic insect contain- by Nelson and Fraser (1980) where hissing was reported upon ers measuring 15 × 7 × 5 cm for ease of identification and han - the following stimuli: sudden onset of light, movement of shad- dling. They were kept on beech chippings with egg crates for ows, vibration of substrate and handling. The hiss was also cover, free access to food (carrot, cucumber, Pedigree mixer found to be more vigorous when in a Gecko’s mouth although original dog biscuits or Kellogg’s cornflakes) and water jelly. how much of this was as a result of the mechanical pressure of Ideally, the cockroaches would have been isolated as the Geckos jaws around the cockroach was not described. nymphs and kept individually until maturity at 8–10 months Studies into the three social hisses have shown that there is a (Clark and Moore, 1995a). This would have ensured that no noticeable difference in the frequency and amplitude between subject had experienced social encounters previously. the types of hiss, which makes hiss identification easier ( Nelson However, due to the time constraints of this study, this meth- and Fraser, 1980; Clark and Moore, 1995a). odology was not possible and sub-adults were purchased. Habituation of this species to not display the disturbance Upon purchase, the 20 individuals were marked using a hiss is possible through regular handling by the same person silver-coloured, non-water-soluble paint (Hagler and Jackson, (Davis and Heslop, 2004). It was also found that the cock- 2001). This ensured easy identification from members of the roach was able to discriminate between handlers, suggesting established colonies, while also allowing easier monitoring that by habituating the cockroach to not display the distur- under low light conditions. After marking the cockroaches, no bance hiss their study provided the first evidence of discrimi - handling took place other than to move the subject to and nation between humans by an insect species. The study by from the established colonies during the study. This reduced Davis and Heslop (2004) was the basis for a study carried out any negative effects such as habituation, which could arise by this author in 2012 looking at the habituation of this spe- from regular handling, as demonstrated by Davis and Heslop cies. The results (Supplemental Appendix S1) showed a large (2004). difference between male and female instances of the distur- bance hiss, which is interesting when looking at other species The existing colonies consisted of 17 females with numer- of arthropod and their responses to predators. A study into ous young, 1 of 5 males and a mixed sex colony of 6 male anti-predatory response to chemical detection of a predator and 6 female G. portentosa. In addition, the subjects were carried out by Williams et al. (2001) showed that in the spot- placed in the presence of a predator in the form of an Emperor ted cucumber beetle (Diabrotica undecimpunctata Linneaus), Scorpion (P. imperator Koch). High densities of male cock- the females were in fact more likely to display an anti-preda- roach lead to more aggression being displayed which poses tory response around a predator than males. risks to the health of the individuals. To reduce the risk of injury through aggression, the males in the existing colonies The role of the disturbance hiss was the main focus of this were kept in smaller groups of five and six throughout the study as although it is classified as anti-predatory, there is study (Guerra and Mason, 2005). little direct evidence linking the disturbance hiss with sur- vival in G. portentosa (Schal et al., 1984). The studies by The established colonies were kept in 8.75 l vivariums Davis and Heslop (2004) along with the author’s study in (Living world) on beech chippings with egg crates for cover, 2012 suggested that the hiss may not be an anti-predatory which were removed 1 h prior to the study each evening. This response. Thus, displays of this hiss in the presence of a made the identification of the hisser simpler and ensured that predator and in social situations with conspecifics warrant all subjects were visible during each trial. Removing the cover further examination. 1 h prior to the trials also meant that disturbance of the col- ony was kept to a minimum at the introduction of the unfa- miliar individual. Method Pandinus imperator was kept in a 30 × 15 cm glass tank The manipulative study introduced 20 novel unfamiliar sub- (Clear seal) on a mix of Exo terra plantation soil and Lucky jects to a variety of social situations and predators for 5 min Reptile humus brick at a humidity of 70–80% with two at a time with all instances of hiss recorded. The aim was to halved plant pots for shelter. Again, the plant pots were further establish that the difference in instances of distur- removed prior to each trial to enable easier monitoring of bance hissing shown by male and female G. portentosa is each subject. shared across the entire species. The study also aimed to investigate the cause of the disturbance hiss and whether it All of the subjects were kept in a room under natural should be quantified as an anti-predatory response. light:dark photoperiod conditions with a red light lamp 2 Bioscience Horizons • Volume 7 2014 Research Figure 2. T he total number of disturbance hisses displayed: males and females. Figure 1. Range of sound produced by Gromphadorhina portentosa. Hisses recorded prior to study in natural interactions. by looking at the contraction and telescoping of its abdomen (Clark and Moore, 1995a). turned on at 7 pm. Additional heating was provided via heat Initial recordings from the established colonies were made mats (ProRep 7 W), keeping a regular temperature of 26–28°C of the disturbance, aggression and courtship hisses (Fig. 1). with ambient humidity. The 20 unfamiliar individuals were Data collected during the trials were then compared with each tested over 4 days, being placed in one of the four treat- these recordings to verify the correct identification of the dis - ments each evening at 9 pm under red light conditions to best turbance hiss. replicate the natural nocturnal habits of the species involved without disturbing the subjects. Four subjects were used each The hypothesis was tested using the extended Kruskal– night to ensure that the existing colonies were only used once Wallis two-way ANOVA test for non-parametric data per day, thus reducing the chance of confounding variables (Holmes et al., 2011) with the factors being disturbance resulting from multiple introductions on one evening. hisses displayed and the setting in which the subject was placed. This was followed up by a post hoc multiple com- The subject was removed from its container and placed in parisons (Q) test. the tank of an established colony or P. imperator for 5 min at a time. A 3-mm-thick plastic screen with 2.5 mm wide by 3.5 cm high vents along it separated the novel subject from Results the colony/predator for 1 min. This reduced the chance of Figure 2 shows the total number of disturbance hisses dis- hisses occurring due to interaction with the experimenter played by males and females in each social setting. Of the 20 being included in the recording. Once the screen was removed subjects studied that showed the disturbance hiss in the pres- the trial began, although the plastic remained in place ence of a predator, the median hiss rate was zero per encoun- throughout the trials using P. imperator to keep them sepa- ter. However, the median hiss rate of the subjects that rate and eliminate any actual predation. Here the vents in the displayed the hiss when placed in mixed sex colonies was 0.5 sheet acted to keep P. imperator separate from the cockroach per encounter. while not blocking any direct sensory detection by the cockroach. The results (Table 1) showed a highly significant differ - ence (K = 12.48, P = 0.01) in the setting in which the distur- Each trial was subject to continuous monitoring from a bance hiss was shown. There was no significant difference Panasonic SDR-S45 video camera with inbuilt dynamic ste- in the display rates of the disturbance hiss between the sexes reo microphone and a sound meter from the mobile phone in general. There was also no significant difference found in application (Smart Tools Co.). This method of monitoring the interaction between the sex of the cockroach and the helped to reduce any miscounts of hiss display by enabling setting into which it was placed. The significant effect of the later referral back to the interactions. Each interaction was setting was found to be the result of a highly significant dif - recorded by Smart Tools, and the data were uploaded onto ference when females were placed in mixed colonies com- an Excel spreadsheet from which graphs were produced pared with males being placed in male colonies and with showing decibel level and the duration of each hiss (Fig. 1). females placed with female colonies (Q = 3.84, P = 0.01) The sound recordings were made from a consistent distance and when females were placed with mixed colonies com- of 10 cm to ensure that the relative amplitude displayed dur- pared with males being placed with female colonies ing each trial was constant. Conformation of which hisses (Q = 3.35, P = 0.05). were produced by just the novel cockroach was carried out 3 Research Bioscience Horizons • Volume 7 2014 Table 1. The number of Gromphadorhina portentosa displaying the disturbance hiss in various social settings with and without subject 20 which was found to be gravid with median hisses per encounter and inter-quartile ranges Social settings Test subjects Male Female Mixed Predator Males 0 1 3 2 Females 3 0 7 1 Females without subject 20 2 1 9 2 Median hisses per 0 0 0.5 0 encounter Figure 3. T he total number of disturbance hisses displayed males and females < subject 20. Inter-quartile range of 0 0 0 0 median hisses at 25% Inter-quartile range of 0 0 3 0 median hisses at 75% Subject number 20 showed a greater response than other females during the study. After the study was completed, it became apparent that the female was gravid so the analysis was carried out again with this individual removed. The rep- resentation in Figs. 3 and 4 shows the number of hisses dis- played by males and females in each social setting without taking subject 20 into account due to her condition. Results of the test showed, as in the original analysis, a highly sig- nificant difference ( K = 12.66, P = 0.01) in the setting in which the disturbance hiss was shown but no significant Figure 4. T otal results showing the social context in which the interaction between the sex of the cockroach and the setting disturbance hiss is displayed < subject 20. into which it was placed. However, there was a highly sig- nificant difference ( K = 9.49, P = 0.01) in the display rates of structure with varying levels of aggression, dominance and the disturbance hiss between the sexes in general. activity levels (Clark and Moore, 1995a). Males show terri- torial behaviour with the dominant male often defending a Discussion 2 territory within the group. This territory is less than 1 m and may simply be a piece of wood or raised ground from which There was a highly significant difference in the setting in a dominant male will chase any other invading male (Nelson which the disturbance hiss was displayed. With half of the and Fraser, 1980). It may be hypothesized that the females subjects displaying the disturbance hiss when placed in a are using the disturbance hiss in mixed sex colonies to ward mixed sex colony, the context in which the cockroach dis- off unwanted attention from unfamiliar individuals. In all played the disturbance hiss was different to what would be instances, the hiss was directed at a male cockroach of the expected. Only 10% of the subjects in this study displayed established population which was either attempting to mate the disturbance hiss when placed with the predator. With or asserting their dominance over the subject. females displaying the hiss in this situation, we are able to categorically discount this hiss being mistaken as the aggres- Pheromones play a crucial role in cockroach communica- sion response which is only displayed by males. tion and the composition of released pheromones in relation to the disturbance hiss may be worth further investigation (Sueur The study revealed a highly significant difference between and Aubin, 2006; Bell et al., 2007). Further studies may find the sexes in the display of the disturbance hiss. Females used that the pheromones accompanying the display of the distur- the disturbance hiss almost exclusively when introduced to bance hiss differ depending on its stimulus and whether it unfamiliar males, while males used other hiss responses when originates from a predator or contact with conspecifics. introduced to unfamiliar male cockroaches. The species lives in small, mixed sex colonies. Females are gregarious in their There are many anti-predatory recognition and avoidance behaviour, and they live in groups without conflict ( Nelson strategies utilized by invertebrates; the strategy employed var- and Fraser, 1980). Males, however, have a non-linear social ies from species to species (Dicke and Grostal, 2001). In the 4 Bioscience Horizons • Volume 7 2014 Research cockroach, the most common anti-predatory response is to social situations. The study found that this species had fewer turn and flee, while there is some evidence of a few species ommatidia than predatory insects such as praying mantis and using stridulation followed by the release of noxious chemicals non-predatory cockroach species Periplaneta americana but (Dicke and Grostal, 2001). If the disturbance hiss of had wider facets that enable the eye to collect a greater G. portentosa is indeed an effective anti-predatory response, amount of light at night when the species is most active. then by not showing the hiss response the females are poten- Cockroaches however have excellent olfactory learning tially at a higher risk from predators than the males that are abilities and an olfactory memory with long retention rates more likely to display these auditory responses. One explana- for scent memories. These memories form quickly and are tion could be that the hiss is a Batesian response in that the easily rewritten (Sakura and Mizunami, 2001). The subjects species is imitating a toxin-producing species. However, G. in this investigation may have detected the indirect sensory Portentosa has many natural predators across all orders: cues from P. imperator faeces indicating its presence. insects, rodents, reptiles, amphibians and mammals. As such Chemical cues can be identified directly through taste, such there is no one animal that it could mimic to deter the wide as the detection of infochemicals from a known predator, variety of predators which each has different sensory abilities. excreta, exuviae, eggs and pheromones (Herberholz and When the cockroaches were placed in the tank alongside Marquart, 2012). Another method of chemosensation used is the predator P. imperator, they moved around briefly wav - that of indirect cues detected through olfaction such as alarm ing their antennae, before stopping, placing the antennae pheromones from injured conspecifics and any scent left on laterally along the abdomen and then remaining stationary the ground by the predator (Dicke and Grostal, 2001; throughout the remainder of the trial. There can be no Herberholz and Marquart, 2012). doubt that the subjects were aware of the presence of P. Megaloblatta blaberoides (Walker) uses mechanical sen- imperator, some remained next to the vented plastic with sory cues to detect predators with the detection of air move- the scorpion directly on the other side becoming active and ment through trichoid sensilla located on the cerci which attempting to prey upon them. The disturbance hiss could indicate the approach of a nearby predator (Schal responses during this time were significantly less than in the et al., 1982). The discovery by Roeder (1963) demonstrated social, non-predator settings. The scorpion relies on olfac- that cockroaches respond to the puff of wind on the cerci that tion and basitarsal compound slit sensilla to detect its prey could represent an approaching predator by making a swift (Brownell, 1984). These mechanoreceptors are sensitive to turn followed by forward acceleration along preferred trajec- vibration but not sound, so the disturbance hiss produced tories to escape. Structures such as the fine hairs on the body by G. portentosa may not have any startle effect on this and antennae called trichoid sensilla could assist in detecting predator but would in fact give away the cockroaches loca- close field sound from conspecifics and predators through the tion. Instead, the freezing displayed in this study may offer movement of air, adding to the sensory ability of the cock- an alternative anti-predatory response to predators with roach (Sueur and Aubin, 2006). By placing the sensitive poor auditory abilities. More studies investigating whether antennae along its abdomen and remaining still, the cock- the disturbance hiss is displayed towards other predatory roaches may have then been waiting for a direct mechanore- species which have better auditory capabilities would enable ceptory cue before acting any further. us to elucidate the purpose of the disturbance hiss. The response may in fact be two different hisses used for differ- Domenici et al. (2009) showed that P. americana has ent purposes which have individual pheromones associated preferred escape trajectories in relation to the perceived with them. Alternatively, the hiss may be a single hiss that is threat indicated by puffs of air. This evolutionary response used in multiple situations. has enabled those with a quicker response to being startled to survive while those which linger do not. Active touch to Threat detection by prey is essential to ensure the survival the antennae can also result in this reaction if the object of an individual and any individual needs to learn quickly touched is unfamiliar or recognized as a predator (Comer what constitutes a threat and what does not. It is most likely and Baba, 2011). There is little direct evidence linking the that mechanical and olfactory sensory cues are used by the disturbance hiss with survival in G. portentosa (Schal et al., cockroach and other arthropods (Comer and Baba, 2011). 1982) and examples of the escape response displayed by This was demonstrated to be the case in the spotted cucum- other non-toxin-producing species such as P. americana ber beetle (D. undecimpunctata Linneaus.), which was found (Schal et al., 1984; Domenici et al., 2009; Comer and Baba, to use both chemosensory and mechanical cues to help them 2011) are a more likely response to the indirect cue of a recognize and differentiate between the most dangerous predator. predators and other similar but less harmful species (Snyder and Wise, 2000). Finally, the behaviour of subject 20 in the study was very interesting and may shed some light on the reason for the Findings by Mishra and Meyer-Rochow (2008) suggest display of the disturbance hiss. This female was the only that vision is of lesser importance to the nocturnal scavenger female subject to display the disturbance hiss and was later G. portentosa than other senses and, as such, it is unlikely to found to be gravid, perhaps indicating that tolerance levels be the sense used by this species for predator detection or in 5 Research Bioscience Horizons • Volume 7 2014 Clark, D. and Shanklin, D. (2013) Madagascar hissing cockroach, accessed are reduced when in this condition as the effectiveness of at: http://www.ca.uky.edu/entomology/entfacts/ef014.asp (8 March flight behaviour may become impaired in gravid females. 2013). This results in reduced locomotor performance leaving the female at a greater risk from predation (Pruitt and Troupe, Comer, C. and Baba, Y. (2011) Active touch in orthopteroid insects: 2010). As a result, the anti-predatory strategies of females of behaviours, multisensory substrates and evolution, Philosophical many species alter when gravid. Transactions of the Royal Society B, 366, 3006–3015. Davis, H. and Heslop, E. (2004) Habituation of hissing by Madagascar Conclusion hissing cockroaches (Gromphadorhina portentosa): evidence of discrimination between humans? Behavioural Processes, 67, The results of this study allow us to challenge the hypothesis 539–543. that the disturbance hiss is an anti-predatory response. Instead, there appears to be some social aspect to the distur- Dicke, M. and Grostal, P. (2001) Chemical detection of natural enemies bance hiss in that it is readily displayed in other situations by arthropods: an ecological perspective, Annual Review of Ecology and, most likely, as a warning resulting from unwanted direct and Systematics, 32, 1–23. contact with conspecifics. Further investigation into the use of the disturbance hiss by G. portentosa in social situations Domenici, P., Booth, D., Blagburn, J. et  al. (2009) Escaping away from would help us to better understand the behavioural ecology and towards a threat, Communications and Integrative Biology, 2 (6), of the species. 497–500. Guerra, P. and Mason, A. (2005) Information on resource quality medi- Author biography ates aggression between male Madagascar hissing cockroaches, Gromphadorhina portentosa (Dictyoptera: Blaberidae), Ethology, 111, I am a mature student and have just completed the Animal 626–637. Biology degree at Worcester University as a top-up student after completing an HND at Pershore College in 2012. I cur- Hagler, J. and Jackson, C. (2001) Methods for marking insects: current rently work at Pershore College as both Lecturer in animal techniques and future prospects, Annual Review of Entomology, 46, care and instructor technician. I designed the study as my 511–543. final year study. I purchased the insects used, conducted the Herberholz, J. and Marquart, G. (2012) Decision making and behavioural experiments, analysed the data performing all statistical anal- choice during predator avoidance, Frontiers in Neuroscience, 6 (125), ysis and wrote up the paper. I have sole responsibility for the 1–15. study’s final content. Holmes, D., Moody, P. and Dine, D. (2011) Research Methods for the Biosciences, 2nd edn, Oxford University press, Oxford, UK. Supplementary material Mishra, M. and Meyer-Rochow, V. (2008) Fine structural description of Supplementary Material is available at BIOHOR online. the compound eye of the Madagascar “hissing cockroach” Gromphadorhina portentosa (Dictyoptera: Blaberidae), Insect Science, Acknowledgements 15, 179–192. I extend my thanks to Dr Debbie Holmes for her patience, Nelson, M. and Fraser, J. (1980) Sound production in the cockroach assistance and support provided to me throughout my study. Gromphadorhina portentosa: evidence for communication by hiss- ing, Behavioural Ecology Sociobiology, 6, 305–314. Pruitt, J. and Troupe, J. (2010) The effect of reproductive status and situ - References ation on locomotor performance and anti-predator strategies in a Bell, W., Roth, L. and Naleppa, C. (2007) Cockroaches: Ecology, Behaviour funnel-web spider, Journal of Zoology, 281, 39–45. and Natural History, The John Hopkins University Press, Baltimore, Roeder, K. (1963) Nerve Cells and Insect Behavior, Revised edition MD. [e-book], Harvard University press, Cambridge, MA, accessed Brownell, P. (1984) Prey detection by the sand scorpion, Scientific at:http://books.google.co.uk/books/about/Ner ve_cells_and_ American, 251 (6), 94–105. insect_behavior.html?id=TTA3AAAAIAAJ&redir_esc=y (11 April 2013). Clark, D. and Moore, A. (1995a) Variation and repeatability of the male agonistic hiss characteristics and their relationship to social Sakura, M. and Mizunami, M. (2001) Olfactory learning and memory rank in Gromphadorhina portentosa, Animal Behaviour, 50 (3), in the cockroach Periplaneta americana, Zoological Science, 18, 719–729. 21–28. Clark, D. and Moore, A. (1995b) Genetic aspects of communication dur- Schal, C., Fraser, J. and Bell, W. (1982) Disturbance stridulation and ing male-male competition in the Madagascar hissing cockroach: chemical defence in nymphs of the tropical cockroach Megaloblatta honest signalling of size, Heredity, 75, 198–205. blaberoides, Journal of Insect Physiology, 28 (6), 541–552. 6 Bioscience Horizons • Volume 7 2014 Research Schal, C., Gautier, J. and Bell, W. (1984) Behavioural ecology of cock- Sueur, J. and Aubin, T. (2006) When males whistle at females: complex fm roaches, Biological Review, 59, 209–254. acoustic signals in cockroaches, Naturwissenschaften, 93, 500–505. Snyder, W. and Wise, D. (2000) Anti predator behaviour of spotted cucum- Williams, J., Snyder, W. and Wise, D. (2001) Sex based differences in anti- ber beetles (Coleoptera chrysomelidae) in response to pr edators that predator behaviour in the spotted cucumber beetle (Coleoptera pose varying risks, Environmental Entomology, 29 (1), 32–42. chrysomelidae), Environmental Entomology, 30 (2), 327–332. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Bioscience Horizons Oxford University Press

Testing the disturbance hiss of the Madagascar hissing Cockroach (Gromphadorhina portentosa) as an anti-predatory response

Bioscience Horizons , Volume 7 – Nov 6, 2014

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BioscienceHorizons Volume 7 2014 10.1093/biohorizons/hzu010 Research Testing the disturbance hiss of the Madagascar hissing Cockroach (Gromphadorhina portentosa) as an anti-predatory response Robin Shotton* Institute of Science and the Environment, The University of Worcester, Henwick Grove, Worcester WR2 6AJ, UK *Corresponding author: 72 Pearce Close, Dudley, West Midlands DY1 2LX, UK. Email: rob.karen101112@gmail.com Project Supervisor: Dr Debbie Holmes, Institute of Science and the Environment, The University of Worcester, Henwick Grove, Worcester WR2 6AJ, UK. The display of the disturbance hiss by the Madagascar Hissing Cockroach (Gromphadorhina portentosa) is considered to be an anti-predatory response despite there being little direct evidence linking the hiss with survival. Many studies have investi- gated the roles of the aggression and courtship hisses, displayed in this social species, but few have considered the role of the disturbance hiss. This study looked at the stimulus for the disturbance hiss response by placing unfamiliar individuals into different social contexts. A total of 10 male and 10 female G. portentosa were kept separately before being placed into four different social situations for 5 min at a time. The individuals were placed into an established colony of all females, an estab- lished colony of all males and an established colony of mixed sex G. portentosa. The subjects were also placed in the presence of a predator, an Emperor Scorpion (Pandinus imperator Koch). All interactions and hisses were recorded both by video and on a sound-recording device. There was a highly significant difference in the setting in which the disturbance hiss was shown and a highly significant difference in the display rates of the disturbance hiss between the sexes in general, with most displays of the disturbance hiss being when introduced to a mixed sex colony. The findings suggest that the role of the disturbance hiss is not an anti-predatory response when presented with a predator of limited auditory senses. Further study into the behav- ioural ecology of this species is recommended to understand the range of anti-predatory responses used by this species when presented with different predators. It was also found that there is some social context for the display of the disturbance hiss which warrants further study. Key words: hissing cockroach, Gromphadorhina portentosa, disturbance hiss, anti-predator, behavioural ecology, startle response Submitted on 9 December 2013; accepted on 12 October 2014 Introduction air through the respiratory spiracles, a hiss is emitted that serves as an auditory social signal. The hiss takes three The large, wingless cockroach Gromphadorhina portentosa recognized forms: aggression, courtship and disturbance (Schaum) is a long-lived social arthropod with a lifespan of (Nelson and Fraser, 1980; Clark and Moore, 1995a). between 2 and 5 years which is endemic to the tropical low- The aggression hiss is displayed by the male during agonistic land forests of Madagascar (Clark and Shanklin, 2013). encounters which form hierarchies within the colony (Clark and The species has the unique ability among insects of being Moore, 1995b). The courtship hiss is again only displayed by able to communicate using modified spiracles on its abdomen males and is essential for successful mating (Clark and Moore, (Nelson and Fraser, 1980). Most other invertebrates commu- 1995a). It is thought that females may use the hiss to elicit pref- nicate by stridulation, rubbing body parts together. By forcing erence in mating by choosing larger, more dominant males © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Research Bioscience Horizons • Volume 7 2014 (Nelson and Fraser, 1980; Schal et al., 1984; Clark and Moore, A sample of 20 healthy adult individuals (10 male, 10 1995b). The third type of hiss, the disturbance hiss, is easily female) were purchased from Ebay.co.uk (seller zoocentre) identifiable from the others as it is both the loudest in amplitude prior to the study at the penultimate sixth instar to ensure that and shortest in frequency (Nelson and Fraser, 1980). This hiss is they were all of the same age. Differentiation between the classified as an anti-predatory response and is displayed by all sexes is relatively easy. After the fourth instar, males are larger members of this species past the fourth instar (Clark and Moore, and possess a large pair of horns on their pronotum as well as 1995a) (full maturity is reached upon the sixth instar at around hairy antennae (Clark and Shanklin, 2013). These individuals 7 months). This particular hiss was also demonstrated in a study were separated and placed in numbered plastic insect contain- by Nelson and Fraser (1980) where hissing was reported upon ers measuring 15 × 7 × 5 cm for ease of identification and han - the following stimuli: sudden onset of light, movement of shad- dling. They were kept on beech chippings with egg crates for ows, vibration of substrate and handling. The hiss was also cover, free access to food (carrot, cucumber, Pedigree mixer found to be more vigorous when in a Gecko’s mouth although original dog biscuits or Kellogg’s cornflakes) and water jelly. how much of this was as a result of the mechanical pressure of Ideally, the cockroaches would have been isolated as the Geckos jaws around the cockroach was not described. nymphs and kept individually until maturity at 8–10 months Studies into the three social hisses have shown that there is a (Clark and Moore, 1995a). This would have ensured that no noticeable difference in the frequency and amplitude between subject had experienced social encounters previously. the types of hiss, which makes hiss identification easier ( Nelson However, due to the time constraints of this study, this meth- and Fraser, 1980; Clark and Moore, 1995a). odology was not possible and sub-adults were purchased. Habituation of this species to not display the disturbance Upon purchase, the 20 individuals were marked using a hiss is possible through regular handling by the same person silver-coloured, non-water-soluble paint (Hagler and Jackson, (Davis and Heslop, 2004). It was also found that the cock- 2001). This ensured easy identification from members of the roach was able to discriminate between handlers, suggesting established colonies, while also allowing easier monitoring that by habituating the cockroach to not display the distur- under low light conditions. After marking the cockroaches, no bance hiss their study provided the first evidence of discrimi - handling took place other than to move the subject to and nation between humans by an insect species. The study by from the established colonies during the study. This reduced Davis and Heslop (2004) was the basis for a study carried out any negative effects such as habituation, which could arise by this author in 2012 looking at the habituation of this spe- from regular handling, as demonstrated by Davis and Heslop cies. The results (Supplemental Appendix S1) showed a large (2004). difference between male and female instances of the distur- bance hiss, which is interesting when looking at other species The existing colonies consisted of 17 females with numer- of arthropod and their responses to predators. A study into ous young, 1 of 5 males and a mixed sex colony of 6 male anti-predatory response to chemical detection of a predator and 6 female G. portentosa. In addition, the subjects were carried out by Williams et al. (2001) showed that in the spot- placed in the presence of a predator in the form of an Emperor ted cucumber beetle (Diabrotica undecimpunctata Linneaus), Scorpion (P. imperator Koch). High densities of male cock- the females were in fact more likely to display an anti-preda- roach lead to more aggression being displayed which poses tory response around a predator than males. risks to the health of the individuals. To reduce the risk of injury through aggression, the males in the existing colonies The role of the disturbance hiss was the main focus of this were kept in smaller groups of five and six throughout the study as although it is classified as anti-predatory, there is study (Guerra and Mason, 2005). little direct evidence linking the disturbance hiss with sur- vival in G. portentosa (Schal et al., 1984). The studies by The established colonies were kept in 8.75 l vivariums Davis and Heslop (2004) along with the author’s study in (Living world) on beech chippings with egg crates for cover, 2012 suggested that the hiss may not be an anti-predatory which were removed 1 h prior to the study each evening. This response. Thus, displays of this hiss in the presence of a made the identification of the hisser simpler and ensured that predator and in social situations with conspecifics warrant all subjects were visible during each trial. Removing the cover further examination. 1 h prior to the trials also meant that disturbance of the col- ony was kept to a minimum at the introduction of the unfa- miliar individual. Method Pandinus imperator was kept in a 30 × 15 cm glass tank The manipulative study introduced 20 novel unfamiliar sub- (Clear seal) on a mix of Exo terra plantation soil and Lucky jects to a variety of social situations and predators for 5 min Reptile humus brick at a humidity of 70–80% with two at a time with all instances of hiss recorded. The aim was to halved plant pots for shelter. Again, the plant pots were further establish that the difference in instances of distur- removed prior to each trial to enable easier monitoring of bance hissing shown by male and female G. portentosa is each subject. shared across the entire species. The study also aimed to investigate the cause of the disturbance hiss and whether it All of the subjects were kept in a room under natural should be quantified as an anti-predatory response. light:dark photoperiod conditions with a red light lamp 2 Bioscience Horizons • Volume 7 2014 Research Figure 2. T he total number of disturbance hisses displayed: males and females. Figure 1. Range of sound produced by Gromphadorhina portentosa. Hisses recorded prior to study in natural interactions. by looking at the contraction and telescoping of its abdomen (Clark and Moore, 1995a). turned on at 7 pm. Additional heating was provided via heat Initial recordings from the established colonies were made mats (ProRep 7 W), keeping a regular temperature of 26–28°C of the disturbance, aggression and courtship hisses (Fig. 1). with ambient humidity. The 20 unfamiliar individuals were Data collected during the trials were then compared with each tested over 4 days, being placed in one of the four treat- these recordings to verify the correct identification of the dis - ments each evening at 9 pm under red light conditions to best turbance hiss. replicate the natural nocturnal habits of the species involved without disturbing the subjects. Four subjects were used each The hypothesis was tested using the extended Kruskal– night to ensure that the existing colonies were only used once Wallis two-way ANOVA test for non-parametric data per day, thus reducing the chance of confounding variables (Holmes et al., 2011) with the factors being disturbance resulting from multiple introductions on one evening. hisses displayed and the setting in which the subject was placed. This was followed up by a post hoc multiple com- The subject was removed from its container and placed in parisons (Q) test. the tank of an established colony or P. imperator for 5 min at a time. A 3-mm-thick plastic screen with 2.5 mm wide by 3.5 cm high vents along it separated the novel subject from Results the colony/predator for 1 min. This reduced the chance of Figure 2 shows the total number of disturbance hisses dis- hisses occurring due to interaction with the experimenter played by males and females in each social setting. Of the 20 being included in the recording. Once the screen was removed subjects studied that showed the disturbance hiss in the pres- the trial began, although the plastic remained in place ence of a predator, the median hiss rate was zero per encoun- throughout the trials using P. imperator to keep them sepa- ter. However, the median hiss rate of the subjects that rate and eliminate any actual predation. Here the vents in the displayed the hiss when placed in mixed sex colonies was 0.5 sheet acted to keep P. imperator separate from the cockroach per encounter. while not blocking any direct sensory detection by the cockroach. The results (Table 1) showed a highly significant differ - ence (K = 12.48, P = 0.01) in the setting in which the distur- Each trial was subject to continuous monitoring from a bance hiss was shown. There was no significant difference Panasonic SDR-S45 video camera with inbuilt dynamic ste- in the display rates of the disturbance hiss between the sexes reo microphone and a sound meter from the mobile phone in general. There was also no significant difference found in application (Smart Tools Co.). This method of monitoring the interaction between the sex of the cockroach and the helped to reduce any miscounts of hiss display by enabling setting into which it was placed. The significant effect of the later referral back to the interactions. Each interaction was setting was found to be the result of a highly significant dif - recorded by Smart Tools, and the data were uploaded onto ference when females were placed in mixed colonies com- an Excel spreadsheet from which graphs were produced pared with males being placed in male colonies and with showing decibel level and the duration of each hiss (Fig. 1). females placed with female colonies (Q = 3.84, P = 0.01) The sound recordings were made from a consistent distance and when females were placed with mixed colonies com- of 10 cm to ensure that the relative amplitude displayed dur- pared with males being placed with female colonies ing each trial was constant. Conformation of which hisses (Q = 3.35, P = 0.05). were produced by just the novel cockroach was carried out 3 Research Bioscience Horizons • Volume 7 2014 Table 1. The number of Gromphadorhina portentosa displaying the disturbance hiss in various social settings with and without subject 20 which was found to be gravid with median hisses per encounter and inter-quartile ranges Social settings Test subjects Male Female Mixed Predator Males 0 1 3 2 Females 3 0 7 1 Females without subject 20 2 1 9 2 Median hisses per 0 0 0.5 0 encounter Figure 3. T he total number of disturbance hisses displayed males and females < subject 20. Inter-quartile range of 0 0 0 0 median hisses at 25% Inter-quartile range of 0 0 3 0 median hisses at 75% Subject number 20 showed a greater response than other females during the study. After the study was completed, it became apparent that the female was gravid so the analysis was carried out again with this individual removed. The rep- resentation in Figs. 3 and 4 shows the number of hisses dis- played by males and females in each social setting without taking subject 20 into account due to her condition. Results of the test showed, as in the original analysis, a highly sig- nificant difference ( K = 12.66, P = 0.01) in the setting in which the disturbance hiss was shown but no significant Figure 4. T otal results showing the social context in which the interaction between the sex of the cockroach and the setting disturbance hiss is displayed < subject 20. into which it was placed. However, there was a highly sig- nificant difference ( K = 9.49, P = 0.01) in the display rates of structure with varying levels of aggression, dominance and the disturbance hiss between the sexes in general. activity levels (Clark and Moore, 1995a). Males show terri- torial behaviour with the dominant male often defending a Discussion 2 territory within the group. This territory is less than 1 m and may simply be a piece of wood or raised ground from which There was a highly significant difference in the setting in a dominant male will chase any other invading male (Nelson which the disturbance hiss was displayed. With half of the and Fraser, 1980). It may be hypothesized that the females subjects displaying the disturbance hiss when placed in a are using the disturbance hiss in mixed sex colonies to ward mixed sex colony, the context in which the cockroach dis- off unwanted attention from unfamiliar individuals. In all played the disturbance hiss was different to what would be instances, the hiss was directed at a male cockroach of the expected. Only 10% of the subjects in this study displayed established population which was either attempting to mate the disturbance hiss when placed with the predator. With or asserting their dominance over the subject. females displaying the hiss in this situation, we are able to categorically discount this hiss being mistaken as the aggres- Pheromones play a crucial role in cockroach communica- sion response which is only displayed by males. tion and the composition of released pheromones in relation to the disturbance hiss may be worth further investigation (Sueur The study revealed a highly significant difference between and Aubin, 2006; Bell et al., 2007). Further studies may find the sexes in the display of the disturbance hiss. Females used that the pheromones accompanying the display of the distur- the disturbance hiss almost exclusively when introduced to bance hiss differ depending on its stimulus and whether it unfamiliar males, while males used other hiss responses when originates from a predator or contact with conspecifics. introduced to unfamiliar male cockroaches. The species lives in small, mixed sex colonies. Females are gregarious in their There are many anti-predatory recognition and avoidance behaviour, and they live in groups without conflict ( Nelson strategies utilized by invertebrates; the strategy employed var- and Fraser, 1980). Males, however, have a non-linear social ies from species to species (Dicke and Grostal, 2001). In the 4 Bioscience Horizons • Volume 7 2014 Research cockroach, the most common anti-predatory response is to social situations. The study found that this species had fewer turn and flee, while there is some evidence of a few species ommatidia than predatory insects such as praying mantis and using stridulation followed by the release of noxious chemicals non-predatory cockroach species Periplaneta americana but (Dicke and Grostal, 2001). If the disturbance hiss of had wider facets that enable the eye to collect a greater G. portentosa is indeed an effective anti-predatory response, amount of light at night when the species is most active. then by not showing the hiss response the females are poten- Cockroaches however have excellent olfactory learning tially at a higher risk from predators than the males that are abilities and an olfactory memory with long retention rates more likely to display these auditory responses. One explana- for scent memories. These memories form quickly and are tion could be that the hiss is a Batesian response in that the easily rewritten (Sakura and Mizunami, 2001). The subjects species is imitating a toxin-producing species. However, G. in this investigation may have detected the indirect sensory Portentosa has many natural predators across all orders: cues from P. imperator faeces indicating its presence. insects, rodents, reptiles, amphibians and mammals. As such Chemical cues can be identified directly through taste, such there is no one animal that it could mimic to deter the wide as the detection of infochemicals from a known predator, variety of predators which each has different sensory abilities. excreta, exuviae, eggs and pheromones (Herberholz and When the cockroaches were placed in the tank alongside Marquart, 2012). Another method of chemosensation used is the predator P. imperator, they moved around briefly wav - that of indirect cues detected through olfaction such as alarm ing their antennae, before stopping, placing the antennae pheromones from injured conspecifics and any scent left on laterally along the abdomen and then remaining stationary the ground by the predator (Dicke and Grostal, 2001; throughout the remainder of the trial. There can be no Herberholz and Marquart, 2012). doubt that the subjects were aware of the presence of P. Megaloblatta blaberoides (Walker) uses mechanical sen- imperator, some remained next to the vented plastic with sory cues to detect predators with the detection of air move- the scorpion directly on the other side becoming active and ment through trichoid sensilla located on the cerci which attempting to prey upon them. The disturbance hiss could indicate the approach of a nearby predator (Schal responses during this time were significantly less than in the et al., 1982). The discovery by Roeder (1963) demonstrated social, non-predator settings. The scorpion relies on olfac- that cockroaches respond to the puff of wind on the cerci that tion and basitarsal compound slit sensilla to detect its prey could represent an approaching predator by making a swift (Brownell, 1984). These mechanoreceptors are sensitive to turn followed by forward acceleration along preferred trajec- vibration but not sound, so the disturbance hiss produced tories to escape. Structures such as the fine hairs on the body by G. portentosa may not have any startle effect on this and antennae called trichoid sensilla could assist in detecting predator but would in fact give away the cockroaches loca- close field sound from conspecifics and predators through the tion. Instead, the freezing displayed in this study may offer movement of air, adding to the sensory ability of the cock- an alternative anti-predatory response to predators with roach (Sueur and Aubin, 2006). By placing the sensitive poor auditory abilities. More studies investigating whether antennae along its abdomen and remaining still, the cock- the disturbance hiss is displayed towards other predatory roaches may have then been waiting for a direct mechanore- species which have better auditory capabilities would enable ceptory cue before acting any further. us to elucidate the purpose of the disturbance hiss. The response may in fact be two different hisses used for differ- Domenici et al. (2009) showed that P. americana has ent purposes which have individual pheromones associated preferred escape trajectories in relation to the perceived with them. Alternatively, the hiss may be a single hiss that is threat indicated by puffs of air. This evolutionary response used in multiple situations. has enabled those with a quicker response to being startled to survive while those which linger do not. Active touch to Threat detection by prey is essential to ensure the survival the antennae can also result in this reaction if the object of an individual and any individual needs to learn quickly touched is unfamiliar or recognized as a predator (Comer what constitutes a threat and what does not. It is most likely and Baba, 2011). There is little direct evidence linking the that mechanical and olfactory sensory cues are used by the disturbance hiss with survival in G. portentosa (Schal et al., cockroach and other arthropods (Comer and Baba, 2011). 1982) and examples of the escape response displayed by This was demonstrated to be the case in the spotted cucum- other non-toxin-producing species such as P. americana ber beetle (D. undecimpunctata Linneaus.), which was found (Schal et al., 1984; Domenici et al., 2009; Comer and Baba, to use both chemosensory and mechanical cues to help them 2011) are a more likely response to the indirect cue of a recognize and differentiate between the most dangerous predator. predators and other similar but less harmful species (Snyder and Wise, 2000). Finally, the behaviour of subject 20 in the study was very interesting and may shed some light on the reason for the Findings by Mishra and Meyer-Rochow (2008) suggest display of the disturbance hiss. This female was the only that vision is of lesser importance to the nocturnal scavenger female subject to display the disturbance hiss and was later G. portentosa than other senses and, as such, it is unlikely to found to be gravid, perhaps indicating that tolerance levels be the sense used by this species for predator detection or in 5 Research Bioscience Horizons • Volume 7 2014 Clark, D. and Shanklin, D. (2013) Madagascar hissing cockroach, accessed are reduced when in this condition as the effectiveness of at: http://www.ca.uky.edu/entomology/entfacts/ef014.asp (8 March flight behaviour may become impaired in gravid females. 2013). This results in reduced locomotor performance leaving the female at a greater risk from predation (Pruitt and Troupe, Comer, C. and Baba, Y. (2011) Active touch in orthopteroid insects: 2010). As a result, the anti-predatory strategies of females of behaviours, multisensory substrates and evolution, Philosophical many species alter when gravid. Transactions of the Royal Society B, 366, 3006–3015. Davis, H. and Heslop, E. (2004) Habituation of hissing by Madagascar Conclusion hissing cockroaches (Gromphadorhina portentosa): evidence of discrimination between humans? Behavioural Processes, 67, The results of this study allow us to challenge the hypothesis 539–543. that the disturbance hiss is an anti-predatory response. Instead, there appears to be some social aspect to the distur- Dicke, M. and Grostal, P. (2001) Chemical detection of natural enemies bance hiss in that it is readily displayed in other situations by arthropods: an ecological perspective, Annual Review of Ecology and, most likely, as a warning resulting from unwanted direct and Systematics, 32, 1–23. contact with conspecifics. Further investigation into the use of the disturbance hiss by G. portentosa in social situations Domenici, P., Booth, D., Blagburn, J. et  al. (2009) Escaping away from would help us to better understand the behavioural ecology and towards a threat, Communications and Integrative Biology, 2 (6), of the species. 497–500. Guerra, P. and Mason, A. (2005) Information on resource quality medi- Author biography ates aggression between male Madagascar hissing cockroaches, Gromphadorhina portentosa (Dictyoptera: Blaberidae), Ethology, 111, I am a mature student and have just completed the Animal 626–637. Biology degree at Worcester University as a top-up student after completing an HND at Pershore College in 2012. I cur- Hagler, J. and Jackson, C. (2001) Methods for marking insects: current rently work at Pershore College as both Lecturer in animal techniques and future prospects, Annual Review of Entomology, 46, care and instructor technician. I designed the study as my 511–543. final year study. I purchased the insects used, conducted the Herberholz, J. and Marquart, G. (2012) Decision making and behavioural experiments, analysed the data performing all statistical anal- choice during predator avoidance, Frontiers in Neuroscience, 6 (125), ysis and wrote up the paper. I have sole responsibility for the 1–15. study’s final content. Holmes, D., Moody, P. and Dine, D. (2011) Research Methods for the Biosciences, 2nd edn, Oxford University press, Oxford, UK. Supplementary material Mishra, M. and Meyer-Rochow, V. (2008) Fine structural description of Supplementary Material is available at BIOHOR online. the compound eye of the Madagascar “hissing cockroach” Gromphadorhina portentosa (Dictyoptera: Blaberidae), Insect Science, Acknowledgements 15, 179–192. I extend my thanks to Dr Debbie Holmes for her patience, Nelson, M. and Fraser, J. (1980) Sound production in the cockroach assistance and support provided to me throughout my study. Gromphadorhina portentosa: evidence for communication by hiss- ing, Behavioural Ecology Sociobiology, 6, 305–314. 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(2001) Sex based differences in anti- ber beetles (Coleoptera chrysomelidae) in response to pr edators that predator behaviour in the spotted cucumber beetle (Coleoptera pose varying risks, Environmental Entomology, 29 (1), 32–42. chrysomelidae), Environmental Entomology, 30 (2), 327–332.

Journal

Bioscience HorizonsOxford University Press

Published: Nov 6, 2014

Keywords: hissing cockroach Gromphadorhina portentosa disturbance hiss anti-predator behavioural ecology startle response

References