Review Article |
Corresponding author: Ivan Hadrián Tuf ( ivan.tuf@upol.cz ) Academic editor: Pallieter De Smedt
© 2022 Ivan Hadrián Tuf, Barbora Ďurajková.
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, Ďurajková B (2022) Antipredatory strategies of terrestrial isopods. In: De Smedt P, Taiti S, Sfenthourakis S, Campos-Filho IS (Eds) Facets of terrestrial isopod biology. ZooKeys 1101: 109-129. https://doi.org/10.3897/zookeys.1101.76266
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Terrestrial isopods (Oniscidea) represent a widespread group of land Crustacea that have been able to successfully adapt to the terrestrial environment and occupy newly formed ecological niches. During the colonisation of land, they faced numerous challenges, including finding an effective way to avoid their new terrestrial predators. In response to predation pressure, they have developed various behavioural and morphological adaptations. These include tonic immobility, conglobation, clinging to the ground, releasing strongly acidic secretions, jumping, and efficient running away. Furthermore, terrestrial isopods can aggregate with other individuals, use stridulation, or change their typical activity time. Some of them also developed spiny tergites and aposematic colouration or posture. The majority of these strategies have not yet been studied.
Aggregation, aposematism, behavioural traits, death feigning, defence, mimicry, Oniscidea
Oniscidea, commonly called terrestrial isopods, woodlice or pill bugs, represent one of the eleven suborders belonging to the order Isopoda (Pericarida, Crustacea) that first appeared on land during the lower Carboniferous (
As terrestrial isopods colonised land some 300 MA, they faced several predators, such as centipedes, spiders, amphibians, and reptiles. Predator pressures caused Oniscidea to develop various morphological and behavioural adaptations. The lifespan of terrestrial isopods ranges from 1 to ~ 10 years. The highest mortality rate is within the first month of their life outside the brood pouch; this is most frequently due to climate factors, such as high temperatures, drought, and floods, as well as due to cannibalism of different ontogenetic stages (
Predators keep up with antipredator adaptations of prey and improve their own hunting techniques accordingly. This never-ending struggle causes the creation of numerous adaptations of both predators and prey, i.e., terrestrial isopods. Although the various types of antipredation strategies among animals are well known, a comprehensive overview on the subject concerning terrestrial isopods is lacking. Therefore, this text provides a systematic review of currently known information regarding the antipredation strategies of terrestrial isopods. The known methods of terrestrial isopod defence against predators, both behavioural as well as morphological, are summarised below, including tentatively proposed strategies.
The simplest strategy to defend oneself against a predator is to keep one’s distance from it, and to avoid an encounter with it. A useful strategy is to avoid staying in places where other individuals were killed. Supporting a necromone hypothesis,
In general, movement in a linear path represents the most efficient adaptive escape strategy when precise information about environmental risks for an animal is lacking (
As terrestrial isopods usually live on the soil surface, it is difficult for them to walk straight and maintain their direction while walking around numerous obstacles (e.g., stones, pebbles, and vegetation stems). The most effective way for them to keep a straight-forward direction is through systematic turn alternations (
A sophisticated method for testing the stress of terrestrial isopods is by keeping track of their movements through a T-maze (
Terrestrial isopods not only engage in spatial predator avoidance, but they also engage in temporal predator avoidance. Terrestrial isopods can avoid encounters with a predator by changing the time range in which they are active. For example, while most terrestrial isopods are nocturnal, the burrowing isopods H. reaumurii, from the arid regions of North Africa, the Middle East, and Central Asia, are active in the colder season during full daylight (
The tendency “not to be seen” can be an escape mechanism from predators. Some terrestrial isopod species, the so-called “runners” group according to the ecomorphological classification of
A jumping strategy is more unpredictable than a running strategy for a hunter. For several species of Philoscia (Ischioscia), jumping, akin to springtails (Collembola), was reported (
Visually oriented larger predators, such as amphibians, lizards, or birds, are attracted by the movement of prey. A very simple strategy related to “to not be seen”, not only used by terrestrial isopods, is to stay inactive when disturbed. When A. vulgare and P. laevis detect a predatory spider, they reduce their activity as a response (
The tendency of terrestrial isopods to not instigate predators by their movement can also be related to “tonic immobility”. This is the state of reversible physical immobility and muscle hypertonicity during which the animals do not respond to external stimuli (
While adopting a posture increases the protection of an animal against being swallowed by a predator (
The soft vulnerable ventral surface of any terrestrial isopod is best protected during conglobation, which allows them to survive in conditions that may be lethal to other species (
The ability to conglobate depends on several body characteristics. The bend of the tergites and the ventral muscles are the most important features that enable conglobation. Aside from an animal’s arched shape, there are a wide range of additional body part adaptations common for species capable of conglobation. These include the shape of the head, the shape and length of the antennae, the shape of the epimers of the pereonites, and the shape of the pleon, telson, and uropods. Species with the ability to roll up have often developed head grooves in which the antennae can fit (
Conglobation is usually triggered by external stimuli, such as strong vibrations or pressure (
Although intraspecific variability in the use of tonic immobility in the “clinger” species P. scaber is high (
If a prey species is distributed homogenously, it is easier for a predator to encounter prey frequently and eat ad libitum; therefore, a very simple antipredatory strategy is for prey to be grouped together. Aggregation into groups is considered an evolutionarily successful response to predator pressure, ambient temperature, and water deficits (
One of the basic characteristics of this type of defensive behaviour is the predator confusion. People who have tried to collect aggregated isopods can confirm that individually handling them can give the majority of isopods enough time to disappear. Even a skilled predator is not capable of eating all individuals in a group. The size of the group has an inverse correlation with the probability that a particular individual in the group will be attacked; i.e., the larger the group, the less likely it is for an individual to be attacked. Actually, a higher visibility of large groups of prey, i.e., a higher attack rate per group, is less important for each individual than is the much lower probability of being eaten while “hiding” in large groups (
In aggregations, information about an approaching attack can be transmitted from individuals who did observe the danger to those who have not yet noticed it. Such behaviour was documented in A. officinalis, which can produce substrate vibrations to warn neighbouring individuals (
Only one terrestrial isopod, A. officinalis, is known to produce sounds that are audible to humans. This sound is produced by stridulation through a ledge of scales situated on the propodus of the fourth and fifth pereopod (
Additionally, substrate-borne vibrations induced by stridulations can be a strategy of intraspecific communication. The pill bug A. officinalis can probably warn other individuals of imminent danger and adverse conditions, and thus ensures a higher survival rate of neighbouring individuals (
Stridulation could also work as an antipredatory strategy. In giant pill millipedes (Sphaerotheriida) this function of stridulation was reported more than a hundred years ago (
Defensive sounds could similarly be aposematic; that is, they could be the acoustic counterparts of visual aposematic signals, differing only in the way that they can fulfil their function both in daylight and in darkness. Defensive stridulation is known from many species of arachnids, myriapods, insects, as well as crustaceans. Usually, these species use stridulation to warn predators against inflicting an attack on poisonous scorpions, spiders, harvestmen, centipedes, or mutilid wasps (
When a terrestrial isopod is found and recognised by a predator, there are some other possible strategies it can use to avoid being consumed. A widespread strategy to repulse predators is the use of excretions from the defensive glands. A detailed description of the glands of terrestrial isopods, which are diverse and numerous, was done by
The substance of lobed glands has a proteinaceous composition with a secretion that is not associated with the hormonal or nervous system; it is instead probably caused by the contraction of adjacent muscles. The stimulation must be very violent: simple shaking or squeezing of the animal does not affect gland secretion, in general (Fig.
Instead of discouraging a predator from an attack using repellent glands, terrestrial isopods may display unpalatability from a distance in order to avoid risking damage. One way to do this is by using a warning aposematic colouration. This strategy is widely adopted by different insects, millipedes (
There are dozens of species with an ostentatious colouration (Fig.
Colourful species of terrestrial isopods: A Armadillidium werneri Strouhal, 1927 B Porcellio duboscqui Paulian de Félice, 1941 C Armadillidium gestroi Tua, 1900 D Porcellio haasi Arcangeli, 1925 E “Merulanella” sp. 1 from Thailand F “Merulanella” sp. 2 from Thailand (photographs Adrián Purkart).
Warning colouration works only against visual predators, but there could be another possible method to warn other predators: spines on the dorsal surface of terrestrial isopods. Extravagant pin-like or blade-like spinulation is typical for several species of the families Armadillidae (species of the genera Pseudolaureola, Calmanesia, Echinodillo, Tridentodillo, Globarmadillo, Polyacanthus), Eubelidae (Panningillo), and Delatorreidae (Pseudarmadillo, Acanthoniscus). All of these species are able to conglobate, and are of small size (~ 1 cm at maximum).
Long spines on terrestrial isopods can also, theoretically, be useful against predators (Fig.
The spiky yellow woodlouse Pseudolaureola atlantica (Vandel, 1977), endemic to St. Helena Island A its bright coloration and spines can serve as protection from potential predators (photograph Amy-Jayne Dutton, St Helena National Trust) B juveniles of P. atlantica are well protected as soon as they leave the marsupium, and remain close to their mother (photograph Phil Lambdon).
A threatening posture, as seen in scorpions, bird-spiders, or centipedes, is another warning signal that protects prey from predators (
We have summarised what is known about the antipredatory strategies of terrestrial isopods. Some anatomical and behavioural traits should be classified as pre-adaptations because they help to solve other challenges of woodlouse life, such as the reduction of water loss. Examples include conglobation and aggregation, as well as clinging (
This study was partly supported by an internal grant of the Faculty of Science of Palacký University Olomouc (IGA_PrF_2021_014). Gert Arijs kindly translated an older French description for us. Moreover, we are grateful to Adrián Purkart, a famous animal breeder, for his illustrations and to Amy Dutton and Phil Lambdon for their photographs of unbelievable and super-rare yellow spike woodlice. We highly value the comments and suggestions of all reviewers (Pallieter De Smedt, Pierre Broly, and Giuseppe Montesanto).