Research Article |
Corresponding author: Ivan Hadrián Tuf ( ivan.tuf@upol.cz ) Academic editor: Elisabeth Hornung
© 2015 Ivan Hadrián Tuf, Lucie Drábková, Jan Šipoš.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Tuf IH, Drábková L, Šipoš J (2015) Personality affects defensive behaviour of Porcellio scaber (Isopoda, Oniscidea). In: Taiti S, Hornung E, Štrus J, Bouchon D (Eds) Trends in Terrestrial Isopod Biology. ZooKeys 515: 159–171. https://doi.org/10.3897/zookeys.515.9429
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We evaluated individual behavioural patterns of isopods expressed as tonic immobility following some intrusive treatments. Common rough woodlice, Porcellio scaber, were kept individually in plastic boxes and tested for tonic immobility repeatedly. Reactivity, sensitivity (number of stimuli needed to respond), and endurance of tonic immobility (TI) according three types of treatments (touch, squeeze, drop) were evaluated. Touch was the weakest treatment and it was necessary to repeat it a number of times to obtain a response; while squeeze and drop induced TI more frequently. Nevertheless, duration of the response persisted for a longer time with the touch treatment. Within each set of the three treatment, the strongest response was the third one, regardless of treatment type. Duration of reaction was affected by the size of the woodlouse, the smallest individuals feigning death for the shortest time. Despite body size, we found a significant individual pattern of endurance of TI among tested woodlice, which was stable across treatments as well as across time (5 repetitions during a 3 week period). Porcellio scaber is one of the first species of terrestrial isopods with documented personality traits.
Anti-predatory behaviour, death feigning, thanatosis, predation, behavioural trait
Generally, when animals encounter their predator they (1) run away, (2) attack it or (3) stay invisible and/or look unpalatable.
Anti-predatory behaviour including boldness can be a part of animal personality. Personality of animals has been routinely studied during the last twenty years, although the study of personality in vertebrates prevails. Behavioural traits, which are consistent over time in individuals and as a response to different situations, have been described as a personality (
Change in anti-predatory behaviour during growth and development of animal can challenge stability over time of the behavioural traits mentioned above. Examination of animal personality traits must consider consistency over two different time intervals: short intervals to determine whether behaviour is sufficiently consistent to be included in a study of personality, and longer intervals to determine how behaviour changes over the course of a lifetime (
During their evolution, terrestrial isopods colonised land and they were faced with new types of stresses, including new types of predators (
Terrestrial isopods developed behavioural protection known as tonic immobility or death feigning, which is related also to behaviour known as “taking specific posture”. In general, the main difference between these categories is that “taking posture” is aimed for protection against being swallowed by a predator (e.g.
The usefulness of feigning death as an anti-predatory behavioural strategy can theoretically be dependent on body size of an animal. If smaller animals can be easily overlooked by predator, the frequency of using this strategy by small animals can be higher than by bigger animals. This pattern was confirmed in some studies (
We studied anti-predatory behaviour of the Common rough woodlouse Porcellio scaber Latreille, 1804, and we added a new parameter to standard experimental design – repetitions at the individual level. With this modification we were able to study the stability of behavioural traits, i.e. animal personality. The main aims of this research were: Are there any patterns in death feigning (tonic immobility, TI) behaviour? Is TI affected by type of treatment or its order? Is there a body-size pattern of behaviour among woodlice suggesting any developmental changes of its behaviour? Despite size of body, is there an individual specific pattern of behaviour among woodlice, i.e. are we able to evaluate their boldness on personal level?
Several hundreds of Common rough woodlice, Porcellio scaber, were collected in the environment of Kutna Hora, Czech Republic (urban green areas and gardens) during June 2013. Following transport to laboratory, they were not sexed, but sorted in three size categories by length (small < 7 mm, medium 7–12 mm, and large > 12 mm). Size of woodlouse is related to its age (
Behavioural experiments followed the design used by
The first treatment was applied and if TI was induced, its duration was measured. If necessary, the stimulus was repeated up to 5 times in order to induce TI. If TI was not induced, lack of reaction was recorded. We let individual woodlouse rest for approximately 30 minutes and applied the second treatment in the same way and the third treatment after a further half hour, respectively (Fig.
We tested the effects of the three types of treatment (touch, squeeze and drop) on reactivity (presence/absence of reaction to stimulus, i.e. probability of inducing TI), sensitivity (number of stimuli needed to induce TI) and endurance of TI. Experimental sets which failed to induce TI were excluded from next data analyses. To determine the effect of different types of treatments we conducted repeated measures ANOVA. The error term of ANOVA reflects that we had the type of treatment nested within individuals of woodlice (ID). Data were not normally distributed therefore we transformed data by decimal logarithm. For multiple comparisons we used a pairwise t-test with adjusted p-values by the Holm correction. We used the F test to check the significance of the explanatory variables. Kendall’s coefficient of concordance was computed in order to determine the consistency of between-individual differences in the three types of treatment. We also used the correlation of TI endurance among different type of treatment. Significance of correlations was tested by using Kendall method with Bonferroni correction.
Three isopods died after the first experimental set, but data are available to evaluate from 738 experimental sets; TI as a reaction to at least one treatment was recorded in 334 sets (45% of sets) in 35 woodlice (23% of individuals). TI was induced by all treatments during the same experimental set in 41 experiments (6%) in 25 woodlice, with only one individual showing TI at each of the 15 treatments (i.e. through all five experimental sets).
If a woodlouse reacted to a treatment in an experimental set, the probability of reaction was influenced by type of treatment (F2,298 = 1165.00, p < 0.001, Fig.
Tonic immobility of Porcellio scaber induced by different treatments: a probability of inducing TI by the first, the second and the third treatment b probability of inducing TI by different treatments c endurance of TI following the first, the second and the third treatment d endurance of TI following different treatments e sensitivity, i.e. promptness of inducing TI by the first, the second and the third treatment f sensitivity, i.e. promptness of inducing TI by different treatments. (*** p < 0.001; ** p < 0.01; * p ≤ 0.05)
To avoid misunderstandings relating to the effect of treatment type and its order in the experimental set, the order of the applied treatments was changed. Without respect to type of treatment, the third treatment was the most probable to be followed by TI (F2,298 = 81.00, p < 0.001, Fig.
Although there were no significant differences among body-size categories of P. scaber in the probability of inducing TI (F1,148 = 0.73, p = 0.395), the longest TI duration was performed by medium body sized woodlice (F1,148 = 6.75, p < 0.05, Fig.
Personality, i.e. individual stability of duration of TI was confirmed by Kendall’s concordance analysis for the whole reactive group of isopods (W = 0.73, p < 0.001); there were individual patterns of endurance of TI irrespective of type of treatment or its order. To avoid obfuscation of personality and size-dependent differences in behaviour, concordance analyses for individual size categories were calculated and revealed significant stability of endurance of TI inside all body-size categories (large size: W = 0.68, p < 0.001; medium size: W = 0.82, p < 0.001; small size: W = 0.65, p < 0.001). Stability of patterns of durations of TI can be visualised by correlations between endurances of different TI values (Fig.
Correlations between duration (in seconds) of TI of Porcellio scaber induced by the different treatments: a correlation between duration of TI induced by squeeze and drop b correlation between duration of TI induced by touch and drop c correlation between duration of TI induced by touch and squeeze. Data were transformed by decimal logarithm.
Correlations between durations of TI of Porcellio scaber induced by different treatments: D – drop, S – squeeze, T – touch. (*** p < 0.001; ** p < 0.01; * p ≤ 0.05)
all animals | large-size animals | medium-size animals | small-size animals | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
D | S | T | D | S | T | D | S | T | D | S | T | |
D | - | 0.55*** | 0.45*** | - | 0.40* | 0.32* | - | 0.71** | 0.56** | - | 0.44* | 0.44* |
S | - | 0.49*** | - | 0.61* | - | 0.52** | - | 0.32** | ||||
T | - | - | - | - |
We evaluated reactivity, sensitivity, and duration of tonic immobility of Porcellio scaber. It is difficult to evaluate the functional significance of anti-predatory behaviour, as there are several interfering behaviours which affect probability of an animal being recognized, captured and consumed by predators (
Generally, the reactivity was relatively low (23% of isopods). It is known that tonic immobility is not the main anti-predatory strategy for P. scaber, as a clinger ecomophological type (
Reactivity of isopods was affected by the type of treatment. Whereas drop and squeeze were followed by TI regularly, touch was not an effective treatment for TI in some specimens. The explanation can be found in the manipulation of isopods by different kinds of predators (e.g.
It is necessary not to forget that P. scaber is strongly thigmotactic (e.g.
Another advantage of aggregates is the higher probability of being passed over by a predator among running conspecifics (
Studies have shown changes in behaviour according to the type of disturbing treatment.
Although our research is not the first to look into TI in terrestrial isopods, the results presented here enable to test repeatability of responses of individual isopods, i.e. its personality. The concept of personality was used for behavioural studies of some Crustacean species, mainly Decapoda, i.e. in crabs, hermit crabs, crayfishes (e.g.
Correlations between length if TI, even if there is a decrease of endurance of TI during one experimental set, can be caused by habituation of isopods to repeated treatment as well as their sensitivity to new type of treatment.
Documented “boldness”, as a parameter of personality of P. scaber, is independent of size (age) of specimen.
Besides finding differences in endurance of TI between body size groups, we also identified personal behavioural patterns in all tested individuals, as well as variation within these body-size groups. These findings are not able to resolve if personality is changing during individual development or not. Although behavioural traits can be stable across short time intervals, changes to personality due to development can cause inconsistency in responses to stimuli over longer time intervals (
We are grateful to Elisabeth Hornung and two anonymous reviewers for their valuable comments and suggestion. Megan Short (Deakin University, Australia) kindly improved the English of the manuscript.