Behav Ecol Sociobiol (2015) 69:1879–1896 DOI 10.1007/s00265-015-2000-3

ORIGINAL ARTICLE

Collective resilience in a disturbed environment: stability of the activity rhythm and group personality in Periplaneta americana

1 1 1 Michel-Olivier Laurent Salazar & Isaac Planas-Sitjà & Jean-Louis Deneubourg & Grégory Sempo1

Received: 14 July 2015 /Revised: 21 August 2015 /Accepted: 24 August 2015 /Published online: 4 September 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Studies on the use of aggregation sites, or commu- and induce migration to an undisturbed shelter site, the distur- nal roosts, found that these roosts have high stability but that bance did not influence the group’sglobalactivityrhythm. individuals will migrate to other sites when the original site is disturbed or otherwise no longer suitable. In this study, the Keywords Domiciliary cockroaches . Sleeping aggregation dynamics of groups of Periplaneta americana aggregations . Communal roosting . Crowding . Aggregation were examined without interruption for 5 days and 4 nights. sites . Disturbances . Group personality Our results showed that groups inside an undisturbed aggre- gation site presented stable group personalities and choice in aggregation site. The individuals that were aggregated in a site Introduction that was repeatedly disturbed by a lighting stimulus during their resting period not only exhibited stability in their group Numerous studies dedicated to the study of group living, have personalities but also a resistance to the disturbance, which found that the costs of living in groups, such as parasitism and allowed the initial aggregation site to remain the site of choice increased competition, are outweighed by the benefits, such as for a few days. Regarding the group personalities, we showed the increased probability of finding a mate (Krause and that the groups had distinct personalities with respect to the Ruxton 2002); the correct development of individuals total amount of time spent outside of aggregation sites and at (Lihoreau et al. 2012); waste reuse by group members (Mira the sources during their active period and the time spent shel- 2000; Rychtár et al. 2014); protection from the environment, tered during their resting period. For the reaction to the distur- including from desiccation or waves (Bell and Adiyodi 1982; bances, we found that the groups showed distinct personalities Focardi et al. 1985; Yoder et al. 2005;Benoitetal.2007;van between the fraction that fled and the fraction that migrated to de Koppel et al. 2008; Rojas et al. 2013; Broly et al. 2014); the undisturbed site. Our study also showed that although the possibility to hunt larger prey and better protect a food source disturbances were strong enough to trigger fleeing behaviour from competitors (Krause and Ruxton 2002;Beauchamp 2014); and protection from predators and parasitoids (Vulinec and Miller 1989;Vulinec1990;Alcock1998; Communicated by L. Keller Krause and Ruxton 2002;AggioandDerby2011;Ley- Cooper et al. 2011;KlompmakerandFraaije2012; Electronic supplementary material The online version of this article Beauchamp 2014). (doi:10.1007/s00265-015-2000-3) contains supplementary material, which is available to authorized users. The fact that these benefits generally outweigh the costs is highlighted by the wide variety of group living species. * Michel-Olivier Laurent Salazar Indeed, group living is widespread taxonomically, with many [email protected] species living in groups at various timescales and with varying degrees of interaction. For example, there are animals with 1 Unit of Social Ecology, CP 231, Université libre de Bruxelles, solitary forms and gregarious forms, and the most famous Campus Plaine, Boulevard du Triomphe, Building NO level 5, example is the desert locust Schistocerca gregaria Brussels, Belgium (Forsskål), in which the presence of one form or the other 1880 Behav Ecol Sociobiol (2015) 69:1879–1896 depends on the local population density (e.g. Maeno and sites possibly because using alternative roosting sites farther Tanaka 2011). Other animals spend only some parts of their from foraging areas would prove too costly (e.g. risk of heat life cycles in groups, with some of them spending their gre- stress) (Rogers et al. 2006). Similar results were found for garious phase in a stable site. For instance, numerous studies harvestmen, which keep using unsuitable sites in the absence have focused on the case of typically solitary species that of close alternatives (Grether and Donaldson 2007), indicating gather at specific sites for hibernation or for reproduction that a disturbed aggregation site is not necessarily abandoned (e.g. certain snakes (Gregory 1974; Shine et al. 2001;Ajtić (e.g. Parsons and Eggleston 2006) but may continue to be et al. 2013;Zappalortietal.2014), insects (Thornhill 1980; used. Although the aggregation sites themselves can be stable, Raak-Van Den Berg et al. 2013;DublonandSumpter2014; individuals can move between different aggregation sites. Durieux et al. 2014; Turner 2015) and birds (Gibson et al. Studies on the aggregation behaviour of different species 1991; Höglund and Alatalo 2014)). Other studies have fo- have shown that site fidelity is variable, with some indi- cused on the many species that form aggregations only at viduals joining aggregates at different aggregation sites certain times of the day, while inactive, and disaggregate into from 1 day to another (e.g. Heinrich and Vogt 1980; small groups or solitary individuals during their periods of Lewis 1995;Kerth2010). activity. At the beginning of the inactive period, the indi- The focus of the current study is to analyse the stability of viduals aggregate in specific sites whose use is stable shelter site choice by groups of individuals that present soli- through time, with sites used for consecutive days to years tary and gregarious periods that are closely linked to a day/ (Lewis 1995;Silvaetal.2011;Laughlinetal.2014). This night cycle under calm and disturbed conditions. Since these type of aggregation, for example, is exhibited by birds aggregation/disaggregation processes are carried out by (Beauchamp 1999), bats (Lewis 1995;Kashimaetal. groups of individuals, we analyse if it is possible to dis- 2013), gregarious caterpillars (Fitzgerald and Costa tinguish different group behaviours. This pattern of soli- 1999;Spechtetal.2007), lobsters (Aggio and Derby tary and gregarious periods is notably exhibited by domi- 2011;KlompmakerandFraaije2012), molluscs (Focardi ciliary cockroaches which are model organisms for many et al. 1985), harvestmen (Machado et al. 2000)anddomi- studies in biology, including research on aggregation (Bell ciliary cockroaches (Lihoreau et al. 2012). and Adiyodi 1982;Lihoreauetal.2012). Domiciliary If these aggregation sites are typically used as long as the cockroaches, e.g. Blattella germanica (Linnaeus) and sites are suitable, they will stop being used when disturbances Periplaneta americana (Linnaeus), are nocturnal foragers appear, either from predators or from anthropomorphic origin and form resting aggregates inside shelters during the day (e.g. Parsons and Eggleston 2006; Grether and Donaldson (Lihoreau et al. 2012). 2007). Concerning this last point, several authors have devot- Studies performed on the aggregation and on the activity ed their studies to understanding the effects of anthropogenic rhythms of domiciliary cockroaches have been mostly carried disturbances on the behaviour of species that roost near urban out with isolated or small groups of individuals for periods or anthropogenic landscapes (Carrete and Tella 2011; less than 24 h (e.g. Harker 1956;LiptonandSutherland1970; Shamoun-Baranes et al. 2011;Chudzinskaetal.2013; Roberts 1982; Rivault 1985;Belletal.2007; Canonge et al. Pirotta et al. 2015). It was notably shown that living in such 2011). These studies have shown that the collective decision environments can result in a differentiation between popula- making guiding the aggregation process is mediated by cutic- tions. For instance, bird and mammal populations living in ular hydrocarbons (Saïd et al. 2005; Sempo et al. 2006)andby their natural environment differed significantly from the urban the amplification that results from the inter-attractions among populations in their personalities, circadian rhythms and sed- individuals in a situation in which each individual has limited entary levels (Ditchkoff et al. 2006;Parteckeetal.2006; environmental information (Parrish and Edelstein-Keshet Atwell et al. 2012; Evans et al. 2012; Dominoni et al. 2014). 1999;Halloyetal.2007; Sumpter 2010). In addition, individ- Despite the obvious effects of urban environments on wild- ual survival, growth and likelihood of response to environ- life, it remains unclear why and how some species adapt to mental heterogeneities and even fleeing behaviour are linked urban settings (Carrete and Tella 2011). Indeed, anthropogenic to the size of the aggregate in domiciliary cockroaches perturbations affect foraging activity (Chudzinska et al. 2013; (Wharton et al. 1968;Sempoetal.2009;Lihoreauetal. Pirotta et al. 2015), flight distance (Carrete and Tella 2011; 2012). Moreover, regarding the behaviour of P. americana Price et al. 2014) and alarm or vigilance behaviour (Wright when confronted with a disturbance, Laurent Salazar et al. et al. 2010; Price et al. 2014). For example, studies on the great (2013) analysed the effect of group size on the group-fleeing knot (Calidris tenuirostris (Horsfield)) and the red knot dynamics of a group of P.americana inside a shelter and noted (Calidris canutus (Linnaeus)) have found that individuals that positive feedback accelerated the fleeing process; there- may keep using roosting sites even when they become unsuit- fore, the fleeing process was more important in larger groups. able due to an increase in disturbances. These shorebirds keep Nevertheless, the studies concerning aggregation and fleeing using such highly disturbed (by predators or humans) roost dynamics could not examine the long-term stability, Behav Ecol Sociobiol (2015) 69:1879–1896 1881 particularly when the aggregate was periodically modulated concerning their migration rate. This group personality may by activities such as foraging. result from the interaction between insects and individual per- There has been a surge of interest on the factors that influ- sonality, the individuals being different with respect to the ence group dynamics and collective behaviour in general. For light stimulus. This means that groups where more individuals instance, recent studies have shown that individual and group migrated during the first disturbances might go below a quo- personalities (consistent inter-individual and inter-group be- rum (Sempo et al. 2009) and the group fastly migrates. On the havioural differences across time or situations) modulate col- contrary, if individuals do not migrate easily during the first lective behaviour (Webster and Ward 2011; Jandt et al. 2013; disturbances, coupled with an increased cuticular hydrocarbon Bengston and Dornhaus 2014; Jeanson and Weidenmüller marking, the migration will be slow. These group personalities 2014; Modlmeier et al. 2014b; Cronin 2015). For example, can arise even if all the individual among the groups are iden- studies on bats have shown that the personality of each indi- tical with respect to the light stimulus but present different vidual influences the fission-fusion of groups among aggrega- social interactions within each group. It is also possible that tion sites (Kerth 2010). In the case of arthropods, for instance, these group personalities are due to the different composition Planas-Sitjà et al. (2015) have shown that the aggregation of the groups in terms of individual personalities and their dynamics are influenced by individual and group personalities sheltering dynamics (Planas-Sitjà et al. 2015). Therefore, we in P. americana. Additionally, recent studies on social spiders hypothesise that the level of nocturnal activity will also show have shown that individual and group personality are strongly similar group personalities. We further discuss the origins of influenced by the social context of the individuals and the this group personality and how it can be affected by the syn- environment itself (Keiser et al. 2014;Modlmeieretal. ergies between social interactions, individual differences and 2014a) and that familiarity between members of a group in- also habituation and learning. creases the personality difference between individuals (Laskowski and Pruitt 2014;Modlmeieretal.2014c). However, besides these examples on the influence of environ- Materials and methods mental and group stability on personality, there is a lack of studies on the long-term effects of disturbances on aggrega- Biological model tion sites and the relation between fleeing dynamics and group personalities. P. americana is a reddish brown, nocturnal domiciliary cock- In the current research, we study the selection of aggrega- roach of the family Blattidae that forms aggregates in dark, tion sites, the long-term stability of the activity rhythms and warm and damp places during the daylight hours. The adults group personalities of P. americana under undisturbed and measure from 35 to 50 mm in length, with a maximum width disturbed (with severe white light disturbances) conditions. of 10 mm (Bell and Adiyodi 1982). These groups were free to roam and aggregate in two shelters The cockroaches used were from the rearing room of the in a simple environment of comparable size with that found Université libre de Bruxelles (ULB). The P. americana were for natural populations of cockroaches in human dwellings reared in the ULB beginning in 2002 in five Plexiglas vivaria (Bell and Adiyodi 1982;Rivault1989; Lihoreau et al. 2012; that were 80×40×100 cm in size in which cardboard tubes our personal observation). We expect that in both conditions were hung from the walls to serve as shelters. Each vivarium (undisturbed and disturbed), individuals will choose an initial had about 1000 individuals of both sexes and of all develop- shelter at the beginning of the trial. Initial shelter choice is well mental stages. The cockroaches were provided with dog pel- known in domiciliary cockroaches (Saïd et al. 2005; Sempo lets and water ad libitum. The rearing room was maintained at et al. 2009; Lihoreau et al. 2012). We hypothesise that, due to 25±1 °C under a 12:12 h light/dark (L/D) cycle. the increased shelter marking with cuticular hydrocarbons, the initial choice will remain stable through the long term (5 days) Experimental setup in the absence of disturbances (undisturbed condition) and despite their nocturnal foraging and disaggregation. In the The experiments were conducted in a circular arena 4 m in disturbed condition where the initially chosen shelter is dis- diameter, limited by a Plexiglas strip at 20 cm high with an turbed with a light, we expect that groups will migrate from electric fence (19 V, 0.2 A) composed of three aluminium the disturbed shelter to the undisturbed shelter. Indeed, light bands with alternate charges to prevent the escape of the cock- disturbance induces a clear collective fleeing behaviour in roaches (Fig. 1). The shelters were constructed of two plastic P. americana (Laurent Salazar et al. 2013), and after each rings 19 cm in diameter and 4.5 cm in height that were placed fleeing event, individuals have two choices, migrate to the 40 cm from the Plexiglas and on opposite sides of the arena. undisturbed shelter or come back to the initial, disturbed, The shelters had two openings of 3×1.5 cm that were opposite one. However, we hypothesise that groups will show consis- one another and that faced away from the food and water tent behavioural differences (Planas-Sitjà et al. 2015) sources, which were placed in the centre of the arena. A glass 1882 Behav Ecol Sociobiol (2015) 69:1879–1896

Fig. 1 Experimental setup. The Water and f ood uos rce Plexiglass strip shelters were placed 40 cm from with electric b ra rier the Plexiglas strip. The two openings in the shelter were opposite one another and faced away from the water and food source Paper

She 4 m lter

Openings c 91 9 mc

top covered with one sheet of red-coloured filter (Rosco col- of cotton soaked in water and dog pellets (Tom & Co. ®, our filter, E-Colour no. 19; Rosco Ltd., London, UK) was Delhaize Group, Brussels, Belgium). placed on top of the shelter to darken the shelters for the To exclude any behavioural variations related to the cockroaches (wavelength accuracy (λd), 608.9 nm; illumi- ovarian cycle (Paterson and Weaver 1997), only the male nance accuracy (Ev), 22.4 lx) in comparison with the outside adults were tested. Individuals with any injury or damage light during daylight hours (λd, 585.8 nm; Ev, 250.3 lx). This (e.g. missing leg segments) were rejected. On the eve- allowed us to observe the interior while maintaining the shel- ning preceding the start of the experiment, we tagged 20 ter dark for the cockroaches (Mote and Goldsmith 1970; Bell individuals from these cohorts with an RFID chip, and and Adiyodi 1982). White paper (120 g/m2) was placed under these individuals were introduced into the arena 1 h after the shelters to prevent any chemical marking (Saïd et al. tagging, at approximately 1900 hours. The group size we 2005), and the papers were changed after each experiment. used was consistent with the group sizes reported in the The interior face of the glass covers was lined with diffuse literature (e.g. Wharton et al. 1968;BellandAdiyodi white LEDs. When these lights were turned on, only the inte- 1982). Although studies on aggregations in natural envi- rior of the shelters was illuminated (λd, 468.3 nm; Ev, ronments were not conducted, empirical observations 308.41 lx), which forced the individuals to flee the shelter. showed that the number of individuals in an aggregation The light measurements were performed with an illuminance varied greatly, from half a dozen to several dozens spectrophotometer (Konica Minolta CL-500A, Konica (Lihoreau et al. 2012,pers.obs). Minolta, Inc. Marunouchi, Chiyoda, Tokyo, Japan; λd, The experiments began at 0800 hours the next day and ±0.3 nm; Ev, ±2 % of ±1 digit of the displayed value). continued for 5 days and 4 nights, which allowed for any The experiments were conducted in a room maintained at unusual behaviours caused by our handling and the introduc- 25±1 °C under a 12:12 h L/D cycle (0800–2000 L; 2000– tion to a novel environment to be minimised. In one series of 0800 D). To detect the cockroaches, whether inside a shelter experiments (the disturbed experiments), we disturbed the or on the food and water source, we tagged each individual on shelter in which the majority of the individuals were aggregat- the pronotum with a radio-frequency identification chip ed at 0800 hours the first day (more than half of the individuals (RFID; diameter, 7.1±0.2 mm; weight, 107±3 mg; in the aggregation). Hereafter, this shelter will be referred to as Spacecode, Verrières-le-Buisson, France) using a drop of latex the selected shelter (S) and the other one as the nonselected (Winsor & Newton ®). A circular RFID lecture panel was shelter (NS). For example, we have the Bleft^ and Bright^ placed under each shelter and under the food and water source. shelters; if the majority of individuals had aggregated inside To complement the RFID recordings, we used two security the Bleft^ shelter, this shelter would be called the Bselected^ video cameras that also recorded in the dark (Monacor ® shelter throughout the experiment and would be the only shel- DMR-188). ter disturbed, regardless on the number of cockroaches aggre- gated there through the rest of the trial. The Selected shelter was disturbed 6 times/day at 0830, 1030, 1230, 1430, 1630 Experimental procedures and measurements and 1830 hours. At those times, the exterior lights were turned off to leave the arena in the dark and the LEDs of the shelter Collected from the rearing room, we isolated in plastic con- were turned on for 5 min, after which the setup was returned to tainers (36×24 and 14 cm in height) around 70 adult male the original state of illumination (N=6). In another series of cohorts of the same age that completed the imaginal moult experiments (the undisturbed experiments), the selected shel- within the same month. The cockroaches had access to a piece ter was not disturbed. However, to minimise the differences Behav Ecol Sociobiol (2015) 69:1879–1896 1883 between experimental conditions, the exterior lights were level of 0.05. The expected distributions were calculated using turned off for 5 min (N=7). abinomialdistribution(Eq.1; Sempo et al. 2009).

Analyses N! PN; n 0:5N 1 ðÞ¼n! N−n ! ð Þ We analysed the aggregation dynamics for 5 days and 4 ðÞ nights. The comparison of the disturbed and undisturbed ex- periments allowed us to highlight the influence of distur- where n is the number of individuals inside a shelter and N is bances on the aggregation dynamics of the cockroaches. the number of individuals in both shelters. For our analysis, we used parametric tests whenever the This allowed us to see the fraction of groups where a data met normality and homogeneity of variance assumptions, statistically significant shelter choice was made through otherwise nonparametric tests were used. For the analysis of the days. To verify that the fraction of groups where a linear regressions, we used F tests. For more information of statistically significant shelter choice was made did not the statistical tests used, see below. vary through the days, we realised a Cochran’s Q test. For the undisturbed condition where there was no mi- Sheltering and migration gration during the day due to a lack of disturbance, we used McNemar’stestwhentheproportionsbetween To confirm that cockroaches aggregated inside the shel- 0830 and 1900 hours were not the same to verify that ters, we used Wilcoxon signed-rank tests to compare the the fraction of groups whereastatisticallysignificant observed number of individuals inside the shelters with a shelter choice was made was stable. theoretical number of individuals randomly distributed in Throughout the experiments, individuals could change the arena. The diameter of the experimental arena was shelters. To analyse this change and to determine wheth- 400 cm, and the diameter of each shelter was 19 cm. er the selected shelter remained as such throughout the Therefore, if assumed that individuals were randomly week, we counted the individuals aggregated in each distributed within the experimental arena, we obtained a shelter at 0830, 1030, 1230, 1430, 1630 and 1830 hours density per square centimetre of 0.0002. Taking into ac- daily. We analysed the difference between the selected count the diameter of each shelter, we arrived at an ex- and the nonselected shelters at those respective hours pected mean number of individuals of 0.09 (density×(2× and then divided the difference by the number of indi- shelter surface)=0.09). To test if there was a choice bias viduals inside both shelters (hereafter, the relative shelter towards one shelter, we used a binomial test on the frac- difference (RSD)). Values of RSD close to 1 indicated tion of times the Bleft^ shelter had more individuals than that most individuals were sheltered inside the Selected the Bright^ one. shelter, values close to 0 indicated that both shelters were The fraction of the total time that each group spent equally occupied, and values close to −1indicatedthat inside both shelters during the daytime (or outside and most individuals were inside the nonselected shelter (in at the sources at night) was also a measure of the shel- this case, the shelter choice changed because the choice tering behaviour. The fraction of the time was calculated was always the selected shelter at the start of the by the total amount spent inside the shelters (or outside) experiment). divided by the total amount of time possible for each As noted above, each disturbance continued for 5 min. The group (14,400 min was the total amount of time possi- effect of these disturbances on the sheltering behaviour of the ble for a group of 20 individuals who spent 720 min cockroaches was quantified with the measurement of the flee- inside (or outside) the shelters). To compare the fraction ing fraction of individuals, which was the proportion of shel- of the total times between conditions and between tered individuals in the selected shelter before (T0) and after nights, we used repeated measures two-way analysis of (T5)eachdisturbance: variance (ANOVA) tests (see BNight occupations^). To conduct multiple comparisons, we used the Holm-Sidak T −T Fleeing fraction 5 0 2 multiple comparisons test when applicable (Glantz ¼ T 0 ð Þ 2011). To compare each 15-min block between nights, we used Kruskal-Wallis test followed by a Dunn’stest (Broly et al. 2012). We used a two-way ANOVA with two repeated measures To determine whether the choice of one shelter over the to compare the fleeing fraction between days and other by the group of cockroaches was statistically significant, disturbances. we compared the number of sheltered individuals in the se- After each disturbance, a fraction of the individuals who lected shelter with the expected distribution at a significance fled from the selected shelter (S) returned to it, whereas the 1884 Behav Ecol Sociobiol (2015) 69:1879–1896 other fraction migrated to the nonselected shelter (NS); the behavioural traits we analysed were, for both conditions, the fraction that returned to S was the returning fraction. total time spent outside and at the sources during the night, the RSD, and the total amount of time sheltered during the day. Night dynamics For the disturbed condition, we also analysed the fleeing and returning fraction. The night hours were from 2000 to 0800 hours, and we divid- We compared the total amount of time spent outside as a ed the night into 15-min blocks. We counted the individuals in function of the moment each trial was conducted with a each shelter and outside of the shelters at the start of each time Kruskal-Wallis test to verify that our observations were not a block. We also counted the sheltered individuals that left the result of any tendency caused by the period of time during shelter at least once during each time block and the individuals which a trial was conducted. that were outside that entered a shelter at least once during each time block. With these data, we calculated the probability of leaving Results and entry for each 15-min block as the number of individuals that left (entered) divided by the number of individuals shel- Daytime occupation tered (outside). To determine the probability per minute, the values were divided by 15. Shelter use

Presence in the shelters Our observations confirmed that the presence of P. americana individuals inside the shelters during the day (at 0830 hours We calculated, for each night and day, the relative presence in before any disturbance) was not caused by a random process. a shelter by dividing the number of presences inside a given Indeed, the theoretical number of individuals inside both shel- shelter by the total number of presences in both shelters. This ters was significantly lower than that observed for both sets of calculation used Eq. 3, where s is one of the shelters, ni is the experimental conditions (Table 1 (Mean number of individ- number of individuals inside the considered shelter at the i 15- uals (±SD) inside the shelters at 0830 hours)). min interval and mi is the number of individuals inside the This sheltering behaviour was stable during the day; the other shelter at the i 15-min interval (there are 48 fifteen- individuals did not leave the shelter during this period or left minute intervals per day and 48 per night). for only short periods of time. The fraction of the total time each group spent inside both shelters during the day (see i 48 ni BMaterials and methods^) was close to 1 (Table 1 (Mean frac- Relative presence ¼ 3 i 0 ¼ ni mi ð Þ tion of the total time sheltered (±SD))), even with the distur- ¼ þ X bances. Indeed, during the day, the individuals that left the shelter during the disturbance did not remain outside the shel- Personality assessment ter long enough to cause a decrease in the mean fraction of the total time sheltered. To analyse for different group personalities and the stability and repeatability of behavioural traits of the group, we used Fleeing and migration the Kendall’s coefficient of concordance (W) for concordance assessment (Kendall 1938; Kendall and Smith 1939). The W In addition to this sheltering behaviour, we observed the se- for concordance assessment compares the stability of rank lection of one shelter after the first night (observation at 0830 positions for each group during the trials and results in the hours of day 1, no selection bias: Bleft^ shelter=8 times out of coefficient W. The values of W range from 0 (no concordance 13; binomial test, p value=0.58), and a statistically significant of ranks) to 1 (complete concordance). Because there is no selection of only one shelter by the group was observed in 71 general qualitative threshold of significance for all situations and 100 % of experiments in the undisturbed and disturbed (Napolitano et al. 2005), we compared the observed W coef- conditions, respectively (undisturbed: binomial test (five out ficients with the BKendall Groups Random Distribution^ of seven groups), p value <0.05; disturbed: binomial test (six (KGRD) as previously explained (Planas-Sitjà et al. 2015). out of six groups), p value <0.05; see the BMaterials and The KGRD is the theoretical distribution of the W coefficients methods^ (Eq. 1); Table 2). At the time of this observation, for random rank orders of the same number of experimental no disturbance had yet been applied in the disturbed condition. groups and repetitions (e.g. seven groups and four nights and In the undisturbed condition, the comparison between shelter N=1000).Weperformeda Z test to test the significance of the selection at 0830 and 1900 hours revealed a very stable col- 2 difference between the observed W coefficients and the corre- lective choice (McNemar’stest:X1=0, p value=1; Table 2). sponding KGRD (Zar 1998; Planas-Sitjà et al. 2015). The Moreover, for each group, we compared each day at 0830 Behav Ecol Sociobiol (2015) 69:1879–1896 1885

Table 1 Shelter occupation a during the day Condition Mean number of individuals (±SD) inside the shelters at 0830 hours Mean fraction of the total time sheltered (±SD)b Observed Theoretical value Wilcoxon signed-rank tests (p values)

Undisturbed (n=7) Day 1 19.6±1.13 0.09 0.016 0.99±0.02 Day 2 19.9±0.38 0.09 0.016 1±0.002 Day 3 19.3±0.95 0.09 0.016 0.98±0.04 Day 4 19.3±0.95 0.09 0.016 0.98±0.03 Day 5 19.3±0.95 0.09 0.016 0.98±0.04 Disturbed (n=6) Day 1 19.17±0.75 0.09 0.031 0.968±0.02 Day 2 18.33±2.25 0.09 0.031 0.96±0.04 Day 3 19.83±0.41 0.09 0.031 0.98±0.02 Day 4 19.83±0.41 0.09 0.031 0.98±0.02 Day 5 19±1.26 0.09 0.031 0.95±0.05

a Mean number of individuals inside the shelters at 0830 hours compared with the expected mean number from a theoretical distribution of individuals b The experimental mean fraction of the total time spent inside the shelters during the daytime hours the presence or absence of a statistically significant day at 0830 hours the presence or absence of a statistically shelter choice. Our results showed that there was no difference significant shelter choice. Our results showed that there was a between days (Cochran’s Q test: Q4=2.9,p value=0.57). This significant difference between days (Cochran’s Q test: Q4= meant that in the undisturbed condition, the fraction of groups 14.46, p value=0.006). Moreover, this difference between where a statistically significant shelter choice was made did days was due to a decrease of the selection rate through time, not vary for the 5 days of the experiment. Notably, in the contrary to the undisturbed condition. This decrease continued undisturbed condition, the S remained the shelter with the until the fifth day, when we observed an increase. This increase most aggregated individuals throughout the 5 days, regardless on the last day resulted from the progressive migration of in- of the statistical significance of the shelter choice (S and NS dividuals from the selected to the nonselected shelter. were, respectively, the shelters with the most individuals and As noted above, the individuals in the disturbed experiments the least individuals on the first day of the trial; see the fled during a disturbance. The effect of each disturbance was BMaterials and methods^ for the definition of S and NS and calculated using Eq. 2 (see the BMaterials and methods^). The the difference between a significant shelter choice). fraction that fled was significantly different between distur- The individuals in the disturbed experiments fled during a bances and days (two-way ANOVA with two repeated mea- disturbance. We analysed whether the shelter choice of the sures; day: F4, 20=9.84, p value=0.0001, disturbance: F5, 25= group of cockroaches was influenced by the migration of in- 26.27, p value <0.0001, day×disturbance: F20, 100=0.83, p val- dividuals from the S towards the NS due to the disturbances. ue=0.68). Multiple comparisons test on the fraction that fled We observed a decrease in the selection rate between the morn- between days showed that, overall, the main difference was ing and the afternoon of the first day. We also compared each between day 1 and the rest (Holm-Sidak’smultiplecomparisons test: p value <0.01) and mostly due to the differences between the disturbances 3 and 6 between days (Holm-Sidak’smultiple Table 2 Fraction of trials in which a non-random shelter choice was observed comparisons test: p value <0.05). Our methodology included six disturbances each day, for 5 days, for a total of 30 disturbances. Undisturbed (N=7) Disturbed (N=6) The mean fraction of fleeing cockroaches decreased exponen- 0830 hours 1900 hours 0830 hours 1900 hours tially with successive disturbances and reached a plateau (0.3) after 2 days according to the following equation: Day 1 0.71 0.71 1 0.50 Day 2 0.86 0.86 0.33 0.33 Fleeing fraction 0:53e−0:17D 0:3 4 Day 3 0.86 0.71 0.33 0.33 ¼ þ ð Þ Day 4 0.86 0.71 0.17 0.17 where D is the number of disturbances (Fig. 2a; R2=0.21, n= Day 5 0.57 0.57 0.83 0.67 180). Of the individuals that fled, we observed that most of them 1886 Behav Ecol Sociobiol (2015) 69:1879–1896

Fig. 2 a Mean fraction of a individuals fleeing (± SD) after each disturbance. b Mean fraction 10 of individuals that return to S after 08 having fled. c Mean RSD (±SD) 06 for the undisturbed and d 04 disturbed experiments before each disturbance. The dotted lines 02 mark the end of 1 day and the Fleeing fraction 00 beginning of the next day b 1 2 10 08 06 04 02 00 Returningc fraction 1.0 0.5 0.0 RSD -0.5 d 1.0 0.5 0.0 RSD -0.5 1 2 4 3 5 6 7 8 9 11 12 14 21 22 24 10 13 15 16 17 18 19 20 23 25 26 27 28 29 30 Disturbance

returned to the selected shelter after the disturbance. This Night occupations returning fraction (see the BMaterials and methods^;Fig.2b) was constant (approximately 0.9 of the individuals that fled) The disturbances did not have a major effect on the other over time, and most of the variability occurred during the first aspects of the group dynamics. Moreover, during the night, six disturbances. we found no differences between the undisturbed and dis- To better observe the migration of individuals towards turbed groups in the measured parameters. the NS from the S one in response to the disturbances, We analysed the total fraction of time each group spent we compared the relative shelter difference (RSD) of outside of the shelters and on the sources of food and water both conditions (see the BMaterials and methods^; through the nights (see the BMaterials and methods^). We Fig. 2c, d). Individuals had the choice to return to their found no significant differences between the undisturbed and original shelter or to migrate to the other one after a disturbed conditions for either measurement (two-way disturbance, and the decrease in the RSD values over ANOVA with repeated measures: time outside: condition: F1, time showed that the individuals migrated from the S to 11 =3.53, p value=0.09, night: F3, 33=7.21, p value=0.0007, the NS. The majority of this decrease occurred during condition×night: F3, 33=1.97, p value=0.14; Time sources: the first day. In the case of the undisturbed condition, condition: F1, 11=0.072, p value=0.79, night: F3, 33=1.77, p our results showed clearly that in the absence of any value=0.17, condition×night: F3, 33=0.73, p value=0.54). A disturbance, the initial shelter retained the selected status multiple comparisons test on the total time spent outside for at least 5 days and no migration from the S to the NS showed that the main difference was between night 1 and was observed. nights 3–4(Holm-Sidak’smultiplecomparisonstest:p value Behav Ecol Sociobiol (2015) 69:1879–1896 1887

<0.05). Since the experimental conditions did not have an ef- a fect, we pooled the data for the two conditions to increase the 10 numberof trials for the analysis of the global behaviour (N=13, Fig. 3). 08

06 Night sheltering dynamics 04 To analyse the sheltering dynamics during the night, we pooled 02

the data for the four nights. The above result indicated that there Mean fraction of individuals was a difference between nights (nights 1 and 3, nights 2 and 4); however, the difference was quantitative not qualitative (see 00 b Fig. S1). Similar to the method used by Broly et al. (2012), 0 10 we used a Kruskal-Wallis test followed by a Dunn’s test to Leaving probability Entry probability compare each 15-min block between nights and we found that 008 6 hour mark there was no significant difference between corresponding time blocks (Dunn’stest:p value >0.99). In other words, the curve 006 shape of each night was similar and we thus pooled the data to increase our number of trials and study the global dynamics 004 which was applicable to all nights. During the night, the number Probabilities of sheltered individuals decreased drastically in the first 002 100 min after the start of the night (Fig. 4a). In Fig. 4b,we show the probabilities of leaving and entry, which are explained 000 in the BMaterials and methods^.Forourfirstapproximation,we 0 100 200 300 400 500 600 700 assumed that there were no social influences during the night. Time from start of the night (min) Therefore, the number of sheltered individuals must be de- Fig. 4 a Mean (±SD) fraction of sheltered individuals every 15 min from the start of the night (0 min) for all four nights and for both conditions scribed by Eq. 5 as follows: (N=13). b The probabilities of leaving and entry as a function of time. The number of sheltered individuals during the night is the The dotted line represents the middle of the 12-h dark period result of two probabilities through time (t). Cockroaches will leave the shelter with a probability l (Eq. 6; R2=0.81) and 0:014 2 e 0:012 7 enter the shelter with a probability e (Eq. 7; R =0.92). The −0:037 t−330:6 ¼ 1 e ðÞþ ð Þ number of individuals that leave will depend on the number of þ individuals sheltered (x), and the number that enter will de- pend on the number of individuals outside the shelter (N−x, The probability of leaving was constant throughout the where N is the total number of individuals) night, with two thresholds at 12 and 660 min, which corresponded to the beginning of the night with the increase dx −ltx et N−x 5 when individuals started to leave the shelters and to the end of dt ¼ ðÞ þ ðÞðÞ ð Þ the night when individuals started to enter the shelters to spend the day inside, respectively. 0:039 l 6 The probability of entering the shelters had a threshold at ¼ 1 e0:06 11:71−t 1 e0:06 t−664 ð Þ ðÞþ ðÞðÞþ ðÞ 330 min when the probability increased, corresponding to the

Fig. 3 Mean fraction of the total 0.7 0.05 time (±SD) spent outside the Outside 0.6 shelters and at the source each Source 0.04 night 0.5 0.4 0.03

0.3 0.02 0.2 0.01 0.1 Fraction of total time source Fraction of total time outside 0.0 0.00 123 4 Night 1888 Behav Ecol Sociobiol (2015) 69:1879–1896 beginning of the second half of the night, which was in accor- Presence in the shelters dance with the time that the cockroaches entered the shelters in massive numbers to spend the daylight period sheltered. During the night, cockroaches could freely visit the source of The probability of entering NS was proportional to the food and water and the shelters. Therefore, for each night, we probability of entering S with ratios of 0.15 and 0.29 for the analysed the presence of individuals in both shelters during undisturbed and disturbed conditions, respectively (undis- the night as a function of their presence during the day. turbed: slope=0.15, R2=0.59, F test for slope significantly In both conditions, our results (Fig. 7) from the linear re- nonzero: F1, 46=73.38, p value <0.001; disturbed: slope= gressions indicated that the presence of individuals in a given 2 0.29, R =0.32, F test for slope significantly nonzero: F1,46= shelter during the day had an important influence on their 24.08, p value <0.001; Fig. 5a, b). The ratios between the presence in that shelter during the night (undisturbed: relative probability of leaving NS and the probability of leaving S presence S: y=0.8x+0.17, R2=0.52, n=28, F test for slope were 0.06 and 0.37 for the undisturbed and disturbed condi- significantly nonzero: F1, 26=28.66, p value <0.0001; relative tions, respectively (undisturbed: slope=0.06, R2=0.018,F test presence NS: y=0.8x+0.05, R2=0.53, n=28, F test for slope for slope significantly nonzero: F1, 46=0.84, p value=0.36; significantly nonzero: F1, 22=68.26, p value <0.0001; regres- 2 disturbed: slope=0.37, R =0.36, F test for slope significantly sions were not significantly different: F2, 52=1.19, p value= 2 nonzero: F1, 46=25.56, p value <0.001; Fig. 5c, d). In both 0.31. Disturbed: relative presence S: y=x−0.03, R =0.76, n= conditions, the graphs of the probabilities in both shelters had 24, F test for slope significantly nonzero: F1, 26=29.12, p the same shape (Fig. 6). These results suggest that although value <0.0001; relative presence NS: y=x+0.01, R2=0.76, the selected shelter had higher probabilities in both conditions, n=24, F test for slope significantly nonzero: F1, 22=68.26, p the migration of individuals to the non-selected shelter value <0.0001; regressions were not significantly different: changed the composition of the aggregations, therefore de- F2, 44=0.98, p value=0.38). We compared these relative pres- creasing the difference between both probabilities and leading ences between conditions to see if disturbances had an influ- to an increase in their ratio. ence, and the results showed that this was not the case for

a Undisturbed b Disturbed 0 006 0 014

0 005 0 012 0 010 0 004 0 008 0 003 0 006 0 002 0 004

0 001 0 002

Non-selected: Entry probabilities 0 000 Non-selected: Entry probabilities 0 000 0 000 0 005 0 010 0 015 0 020 0 025 0 030 0 000 0 005 0 010 0 015 0 020 0 025 Selected: Entry probabilities Selected: Entry probabilities c d 0 035 0 030

0 030 0 025 0 025 0 020 0 020 0 015 0 015 0 010 0 010

0 005 0 005

0 000 0 000 Non-selected: Leaving probabilities 0 00 0 02 0 04 0 06 0 08 0 10 Non-selected: Leaving probabilities 0 000 0 006 0 012 0 018 0 024 0 030 0 036 Selected: Leaving probabilities Selected: Leaving probabilities Fig. 5 Relationship between probabilities. a Entry probabilities for the undisturbed and b disturbed conditions. c Leaving probabilities for the undisturbed and d disturbed conditions Behav Ecol Sociobiol (2015) 69:1879–1896 1889

Fig. 6 Entry and leaving a Undisturbed b Disturbed probabilities for the undisturbed 0 040 (a, c) and disturbed (b, d) 6 hour mark conditions. The probabilities of 0 035 the selected shelter is represented Probability of Selected shelter by black dots and of the Non- 0 030 Probability of Non-selected shelter selected by grey dots.Inthe disturbed condition, the selected 0 025 shelter was the shelter that was 0 020 disturbed 0 015

Entry probabilities 0 010

0 005

0 000 c d 0 10

0 08

006

0 04

Leaving probabilities 002

000 0 100 200 300 400 500 600 700 0100200300400500600700 Time from start of the night (min) either shelter (relative presence S between conditions: regres- experiments, we also analysed the group personality for the sions were not significantly different: F2, 48=1.05, p value= fraction that fled and the fraction that returned (Table 3). For 0.36; relative presence NS between conditions: regressions the returning fraction, we accounted for only the first six dis- were not significantly different: F2, 48=1.1, p value=0.34). turbances because after those, there were cases in which no individual fled, making it impossible to calculate the W. Group personalities To ensure that these personalities were not a result of any tendency caused by the period of time during which a trial was Using the W for concordance assessment (see the BMaterials conducted, we compared the total amount of time spent out- and methods^), we analysed the presence of group personality side as a function of the moment each trial was conducted. The for both conditions as defined by the total time spent outside result (Kruskal-Wallis test: H3=2.9, p value=0.45) confirmed and on the source during the night and by the time spent inside that the group personalities were not caused by the period of both shelters during the day. In the case of the disturbed time during which a trial was conducted but, instead, were

Fig. 7 Presence of individuals a b 1 2 Selected shelter inside a given shelter during the night as a function of the presence 10 Non-selected shelter of individuals inside that shelter during the day for the a 08 undisturbed and the b disturbed 06 conditions 04

02

Relative presence during00 the night 00 02 04 06 08 100 00204060810 Relative presence during the day 1890 Behav Ecol Sociobiol (2015) 69:1879–1896

Table 3 Summary of the group personality assessment Condition Measurement Repetitions Kendall coefficient for concordance assessment

WZ pvalue

Undisturbed (N=7) Time outside 4 nights 0.94 5.42 <0.0001 Time sources 4 nights 0.5 2.00 0.0453 Time sheltered 5 days 0.61 2.85 0.0044 RSD 30 0.67 35 <0.0001 Disturbed (N=6) Time outside 4 nights 0.82 4 <0.0001 Time sources 4 nights 0.73 3.37 0.0008 Time sheltered 5 days 0.6 2.45 0.0142 RSD 30 0.67 33.8 <0.0001 Fleeing fraction 30 disturbances 0.22 9.94 <0.0001 Returning fraction 6 disturbances 0.51 3.56 0.0004

attributed to the stability of the group behaviours throughout temporal patterns of exploration and foraging. We also the experiment. showed, for both conditions, that the fraction of individuals We highlighted the presence of personalities at the group aggregated in each shelter during the day was correlated with level for all our measurements (Table 3). However, the differ- the presence of individuals in the corresponding shelter during ent behaviours that we measured did not have the same level the night. of stability and repeatability, as observed with W.Weobserved These results highlight that aggregations of cockroaches clearly, for example, that the time spent outside and at the are stable at different timescales and that they are modulated sources was not at the same level; the time spent at the sources during the day- and night-time. Three mutually nonexclusive had a lower level of stability and repeatability than the time hypotheses acting in synergy, applied at different timescales, spent outside. Overall, the behaviours that presented the could explain our observations, namely, habituation and learn- highest level of stability and repeatability, for both conditions, ing, social interactions, and individual differences in response were the time the group spent outside during the night and the thresholds. We hypothesise that social interactions are the pri- RSD. mary factor influencing the formation of aggregates during the Surprisingly, when we studied all paired correlations day and their disaggregation during the night. among the different group personalities, we only observed a Indeed, during the day, direct (contact among individuals) correlation between the fraction that fled and the RSD, which and indirect (substrate marking with cuticular hydrocarbons) indicated that the groups with fewer individuals inside the S social inter-attractions are necessary to accurately describe the shelter had a lower fraction of individuals that fled during a observations of shelter selection when individuals are faced disturbance (R2=0.08; F test for slope significantly nonzero: with multiple shelter choices (Rivault et al. 1998; Ame et al.

F1, 178=16.02, p value <0.0001). 2004; Saïd et al. 2005; Sempo et al. 2009; Lihoreau et al. 2012). The stability of the shelter choice was evident when the aggregate was not disturbed: individuals did not Discussion leave the shelter during the day. Moreover, when the aggregate was disturbed, we observed a resistance to Resilience and stability of the choice disperse (see BMigration^ below). During the night, individuals inside both shelters disaggre- Our experiments, conducted for 5 days and 4 nights without gated, and we showed that the total sheltered population could interruptions, allowed us to study the day and night rhythms of be described without the necessity to include social interac- aggregation and foraging of the cockroach. First, we tions. This is in agreement with Knadler and Page (2009), highlighted that, in the absence of any disturbance, a collec- which showed that entrainment was influenced more by the tively chosen sheltering site continued to be used by a group photoperiod than by the social interactions. The total popula- of cockroaches for at least 5 days. Second, we showed that the tion inside or outside the shelters depended on the probability stress caused during the day (light disturbance) had no effects of an individual entering or leaving a shelter. The decrease in on shelter use and feeding behaviour of the cockroaches dur- the number of sheltered individuals at the beginning of the ing the night. Indeed, there were no significant differences night occurred because of the increase in their probability of between the disturbed and undisturbed conditions for the leaving the shelter, whereas their probability of entering was Behav Ecol Sociobiol (2015) 69:1879–1896 1891 weak and constant. Later during the night, we observed an find any behavioural syndromes at the group level (Sih et al. increase in the number of sheltered individuals, which 2004; Jandt et al. 2013). corresponded to an increase in the probability of entering the shelter after midnight (6 h after the start of the night), and last, we observed an acceleration in the number of sheltered indi- Migration viduals closer to the resumption of daytime conditions that was explained by the abrupt decrease in the probability of For the disturbed condition, the disturbances were applied leaving the shelter. only to the initially selected shelter (selected) throughout the Nonetheless, at the level of the shelters, we observed a experiments. We observed that when the initially selected social influence. The probabilities of leaving and entering shelter was disturbed, a migration of individuals towards the the shelters with the most individuals during the day were undisturbed shelter occurred during the day. Frequent light higher than the probabilities of leaving and entering the shel- disturbances may decrease the individual fitness of cock- ters with fewer individuals. This result strongly suggests that roaches by interrupting their sleep-like state and increasing social interactions modulate the dynamics during the night. stress (Bell and Sams 1973; Stephenson et al. 2007). These Indeed, some authors have demonstrated that the sensitivity disturbances were sufficient to force most individuals to flee to odours varies from day to night in cockroaches (Page and the first time (Fig. 2a), although the fraction that fled during a Koelling 2003;Deckeretal.2007). This change in sensitivity disturbance decreased with successive disturbances. may diminish the social inter-attraction among cockroaches However, the fraction of the fleeing individuals that entered and induce disaggregation during the night. Moreover, these the undisturbed shelter was low and constant throughout the loose inter-attractions during the night might increase agonis- disturbances. This progressive migration could be explained tic behaviours, leading to an increased probability of leaving by the synergy among the three mutually nonexclusive hy- the shelter. To summarise, the shelter that has more individuals potheses discussed above (habituation and learning, social will have more agonistic behaviours, and therefore, that shel- interactions and individual differences in response thresholds) ter will have a higher probability of cockroaches leaving than but on a different timescale. shelters with fewer individuals (Bell and Sams 1973). First, we cannot exclude habituation to the disturbances. We also observed how the choice of a shelter during the Individuals that did not migrate during the first disturbance day influenced the shelter that was the most visited during the could habituate to the disturbances, decreasing the fraction night. One possible reason for this finding is that shelters with that fled through time. As we noted above, other studies have more individuals during the day are marked more with cutic- demonstrated that cockroaches could memorise the position of ular hydrocarbons (Rivault et al. 1998;Saïdetal.2005)than their shelter and navigate a return, even when they were dis- shelters with fewer individuals, and the increased marking turbed during feeding outside of the shelter (Rivault and would lead to longer visits during the night, without reaching Durier 2004). This behaviour might explain why most indi- a level of attraction that would induce an aggregation during viduals returned to the disturbed shelter once the disturbance the night. The second possible reason is that individuals re- was over and the external lights were turned on. membered the shelter they were in during the day, and there- Second, regarding social interactions, previous studies fore, the cockroaches visited it more during the night (Rivault demonstrated that disturbances of light increased the ag- and Durier 2004). onistic behaviours among cockroaches and induced dis- We also observed an intragroup behavioural stability persion until individuals were no longer in contact with throughout the week that allowed us to highlight group per- one another (Bell and Sams 1973). Moreover, the move- sonalities. The ability to identify personalities at the group ment of individuals fleeing within a group accelerated level is in accordance with previous works in which the con- the fleeing process of the group (Laurent Salazar et al. sistency of cockroach behaviours was tested three times in a 2013). Both studies showed that larger groups resulted week (Planas-Sitjà et al. 2015). However, in our study, we in a larger fraction of individuals that flee and a greater identified group personalities during both the day and the dispersal of individuals during a light disturbance than night. Indeed, group personalities were observed for the total smaller groups. In our experiment, with the decrease in sheltering time during the day and the night and in the time the population in the disturbed shelter after successive they stayed outside the shelter during the night and in the disturbances, the fraction of individuals fleeing de- migration rate during the day. A notable aspect of the group creased. Indirect social interactions may also play a personalities was found in the absence of correlations among role. Indeed, because the group members did not all the measurements of behaviour. For example, we expected migrate to the undisturbed shelter after the first distur- that groups that spent more time outside the shelters during bance, the disturbed shelter could be increasingly the night would also spend more time at the source of food and marked with cuticular hydrocarbons, which might have water. These absences of correlation indicated that we did not aroleinretentionduringadisturbance. 1892 Behav Ecol Sociobiol (2015) 69:1879–1896

Table 4 Examples of species that aggregate during the resting period and that disaggregate during the active period

Species studied Cycle type Example adaptive value References

Molluscs Nerita textilis Tidal Protection against waves, overheating Chelazzi et al. (1984), Focardi et al. (1985) and dehydration. Crustaceans Clibanarius spp. Tidal Protection against predators and Snyder-Conn (1980), Turra and Leite dehydration. (2000) Ligia exotica Tidal Protection against dehydration. Farr (1978) Spiny lobsters Nychthemeral Protection against predators. Aggio and Derby (2011); Ley-Cooper et al. (2011) Porcellio scaber Nychthemeral Protection against dehydration. Broly et al. (2014) Arachnida Prionostemma spp. Nychthemeral Protection against predators Grether and Donaldson (2007) Goniosoma longipes Nychthemeral Protection against predators and Machado et al. (2000) dehydration. Insects Idiomelissodes duplocincta Nychthemeral Protection against predators. Alcock (1998) Triatoma spp. Nychthemeral Protection against predators, Lazzari (1992), Lorenzo Figueiras and Lazzari (1998), Barrozo et al. (2004), Minoli et al. (2007) Whirligig beetles Nychthemeral Protection against predators Heinrich and Vogt (1980), Vulinec and Miller (1989) Hetaerina americana Nychthemeral Protection against predators Grether and Switzer (2000), Switzer and Grether (2000) Taeniopoda eques Nychthemeral Thermoregulatory and protection Alcock (1972) against predators Various butterfly species Nychthemeral Protection against predators, Fitzgerald and Underwood (1998), (caterpillar) thermoregulation, and moulting Fitzgerald and Costa (1999), Fitzgerald and Pescador-Rubio (2002), Specht et al. (2007) Birds Various species Nychthemeral Thermoregulation, protection against Eiserer (1984), Rogers et al. (2006) predators, increased feeding efficiency, and preparation for migration Bats Various families Nychthemeral Information transfer, maintenance Lewis (1995), Willis and Brigham (2004), of social relationships predator Kerth (2010) and parasite avoidance. Primates Microcebus murinus Nychthemeral Minimise resting metabolic rate Perret (1998), Schülke and Ostner (2005) Rhinopithecus roxellana Nychthemeral Protection against predators and Zhang et al. (2011) thermoregulation Papio hamadryas Nychthemeral Protection against predators Hamilton (1982), Swedell (2002) Reptiles Christinus marmoratus, Nychthemeral Protection against predators and Kearney et al. (2001), Shah et al. (2003) Nephrurus milii thermoregulation

Third, we observed group personalities in all the measured Perspectives parameters, including in clearly stressful situations such as in fleeing and migration. Although personalities may disappear As in other gregarious species, aggregation in domiciliary in cases of extreme stress (Sih et al. 2004; Niemelä et al. cockroaches is the keystone for other adaptive strategies such 2012), in our study, individuals differed in their response to as the use of social information (Sumpter 2010;Grüterand the disturbances, as we observed group personalities for the Leadbeater 2014), reduction of physical stress (Focardi et al. fraction that fled the disturbances and for the fraction that 1985;Benoitetal.2007; Broly et al. 2014) and anti-predator returned to the disturbed shelter after each disturbance. It is behaviours (Vulinec and Miller 1989; Machado et al. 2002; possible that individuals with a lower fleeing threshold were Beauchamp 2014). After an aggregation phase during the rest- the first to leave the disturbed shelter and migrate. Hence, after ing period, these species are characterised by a dispersion each disturbance, the composition of the group sheltered in the phase associated with individual (or in small groups) foraging disturbed shelter would change. After each disturbance, the activities during the active period; this characteristic is shared more resilient individuals would stay in the disturbed shelter by many gregarious species (Table 4). and thereby decrease the fraction that flees in subsequent The disaggregation of aggregates can be induced by distur- disturbances. bances during the resting period. The disturbance of Behav Ecol Sociobiol (2015) 69:1879–1896 1893 aggregates caused by predator attacks or the presence of par- Pruitt 2014; Planas-Sitjà et al. 2015). Hence, we encourage asites is the subject of a number of studies (Davis 1975; Lewis further studies to clarify the involvement of individual person- 1996; Hilton et al. 1999; Beauchamp 2012). These distur- ality in collective decision-making processes such as fleeing bances occur because the presence of the aggregates attracts behaviour and its synergy with memory and social behaviour. predators, for example. However, numerous types of distur- bances are not the direct result of the presence of the aggre- Acknowledgements M-OLS and IP-S were funded by a PhD grant gates. Depending on the intensity, duration, and frequency of from Fonds pour la Recherche dans l’Industrie et dans l’Agriculture (FRIA). JLD is Research Director from the Belgian National Fund for such disturbances, the typical environment of the aggregates Scientific Research (F.N.R.S). can be mildly affected (e.g. when a roosting tree is disturbed by sounds (Mott 1980)) or rendered permanently unavailable Compliance with ethical standards (e.g. when a roosting tree is no longer safe from predators (Grether and Donaldson 2007)). Only a few studies have fo- Ethical approval Our observations were carried out in full accordance with the ethical guidelines of our research institution and comply with the cused on the collective migration behaviour caused by distur- European legislation. bances of aggregation sites. For example, the migration to- wards an undisturbed shelter was similar to that observed in Conflict of interest The authors declare that they have no conflict of harvestmen, which completely migrated to better shelters only interest. when their original shelter no longer offered protection against predators (Grether and Donaldson 2007). Similar migration patterns with variable levels of site fidelity apply for certain References shorebirds (Pfister et al. 1992; Rogers et al. 2006), starlings and blackbirds (Brough 1969;Mott1980) and Brent geese Aggio J, Derby CD (2011) Chemical communication in lobsters. In: (Owens 1977). Breithaupt T, Thiel M (eds) Chem Commun Crustac. Springer, pp 239–256 Over the long term, living in a constantly disturbed envi- Ajtić R, Tomović L, Sterijovski B et al (2013) Unexpected life history ronment can lead to a differentiation among populations. traits in a very dense population of dice snakes. Zool Anz 252:350– Indeed, this process of differentiation has been observed in 358 species living in urban environments with frequent anthropo- Alcock J (1972) Observations on the behaviour of the grasshopper genic disturbances. For example, among house sparrows, Taeniopoda eques (Burmeister), Orthoptera, Acrididae. Anim Behav 20:237–242 European blackbirds and raccoons, populations that lived in Alcock J (1998) Sleeping aggregations of the bee Idiomelissodes their natural environment differed significantly from the urban duplocincta (Cockerell) (Hymenoptera: Anthophorini) and their populations in their personalities, circadian rhythms and sed- possible function. J Kansas Entomol Soc 71:74–84 entary levels (Ditchkoff et al. 2006;Parteckeetal.2006; Ame J-M, Rivault C, Deneubourg J-L (2004) Cockroach aggregation Atwell et al. 2012; Evans et al. 2012;Dominonietal.2014). based on strain odour recognition. 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