External marking of terrestrial isopods (Isopoda, Oniscidea): efficiency of materials and influence on feeding behavior

Abstract

Many monitoring studies use marking techniques to obtain dispersal data on individuals. Marking procedures may influence the vital activities of the terrestrial isopods, such as feeding behavior. The objective of this study was to identify the efficiency of different materials for external marking of woodlice and the influence on their feeding performance. Cyanoacrylate glue + glitter and nail polish were used as separate marking materials on three species: Balloniscus glaber, Benthana picta and Armadillidium vulgare. The material efficiency was compared using Kaplan-Meier curves and Log-Rank analysis. Individuals were fed with leaf discs of Machaerium stipitatum for feeding performance trials, and consumption rates were compared using ANOVA (α<0.05). There was no difference in durability between the materials used for external markings, except between marked and unmarked Benthana specimens when the observation period exceeded 15 days (Log-Rank=8.446, p=0.015). Nail polish was considered more suitable for feeding experiments. Statistical differences in consumption rates were observed only between the marked individual treatments of Benthana (ANOVA, F=7.5440, p=0.0002). These results indicate that external marking does not affect the feeding habits of the animals and suggest that this technique can be used to monitor dispersal of terrestrial isopods in field conditions for approximately 15 days.

Keywords:
Woodlice; consumption rates; material efficiency; Kaplan-Meier curve; nail polish

INTRODUCTION

Animal marking techniques are widely used in monitoring research, such as in density and population size studies, through the recognition of marked individuals in recapture events (Suzuki et al., 2010; Drag et al., 2011). This method is also used in animal dispersal observations, via periodic inspections of hotspots or by active searching for marked individuals in natural environments (Nazni et al., 2005; Hamer et al., 2014). Researchers can also employ marking technique for the evaluation of survivorship aspects and growth rate studies following the behavior of a specific animal by regular observations of this same specimen exposed to different conditions (Muir and Kay, 1998; Rose et al., 2018). In biological control, species conservation and animal physiology experiments, this technique is also useful for differentiating individuals that have undergone an a prior process of distinct treatment (i.e., exposure to volatiles or drugs) and then they go through the observation process all together in the same area (i.e., arenas or chambers) (Baguette et al., 2000; Horton et al., 2009; Groner et al., 2018).

There are a considerable number of marking and recapture techniques for invertebrates and vertebrates, such as internal and external dyes, mutilation and amputation, radio-telemetry, fluorescent powder, water-based and oil-based paints and labels (Hagler and Jackson, 2001). According to Hagler and Jackson (2001) the durability of the mark is considered the main aspect of a technique for the material to be considered “efficient”. Failure to attach the material to the cuticle surface of some arthropods may compromise long-term studies (i.e., more than one intermoult period for crustaceans) (Walker and Wineriter, 1981; Frisch and Hobbs, 2006; Hagler and Jackson, 2001). In addition, the mark can also be removed by the animal itself, due to chemical constituents of the cuticle (Lok et al., 1975), abrasion with elements present in the environment (Tuf et al., 2013), grooming behavior (Wojcik et al., 2000), or even by simple loss through the molting process (Willows, 1987).

Depending on the goal to be achieved, these methods can show both positive and negative points. Sometimes though the researchers fail to describe or analyze the influence of marking techniques on animal behavior (Hagler and Jackson, 2001; De Souza et al., 2012; Drahokoupilová and Tuf, 2012). For vertebrates, for example, toe clipping may compromise the animal’s locomotor ability, as well as their foraging behavior (Schmidt and Schwarzkopf, 2010; Petit et al., 2012). The use of colored materials in invertebrates can increase their visibility to predators and, consequently, their survivorship rate after the marking procedure (Janks and Barker, 2013). In addition, excessive marking can alter the individuals’ vital activities and it can imply misrepresentation of the data and distort the analyses (Pardo et al., 1996; Döge et al., 2009; Lucía et al., 2018). However, in consonance with Southwood and Henderson (2000), the animals’ survivorship and behavior should not be affected by the marking process for the technique to be considered plausible and reliable.

Most animal tracking studies aim at home range mapping and to infer migration routes of vertebrates (Luschi, 2013; Gnanadesikan et al., 2017; Child et al., 2019). They usually discuss patterns of locomotion of predators and other organisms at the top of the food web (Phillips et al., 2004; Morgan et al., 2009; Pérez et al., 2018). Generally, this information is linked with dispersion data about their prey, since these prey animals (smaller vertebrates and invertebrates) act as movement motivators of predators (Austin et al., 2004; Block et al., 2011; Gnanadesikan et al., 2017). Some of these preys participate in the first trophic levels of many food chains, serving as a link between producer organisms and primary consumers (Bridgeland et al., 2010; Wu et al., 2014), like woodlice.

Woodlice are among the terrestrial arthropods with special notoriety, due to their mechanical fragmentation activity in the leaf litter and soil organic matter (Zimmer, 2006; Frouz et al., 2008; Wood et al., 2012).. They therefore play an important role, with other detritivores, since they work together in soil nutrient cycles (Caseiro et al., 2000; Quadros and Araujo, 2008). Observing terrestrial isopod movement in natural environments is a difficult process because of their small body size and how quickly some species shelter in refuges with difficult access (Paoletti and Hassall, 1999; Hassall and Tuck, 2007). Oniscidean isopod species are classified into ecomorphological types according to their anti-predatory strategies, which reflect their morphology (i.e., cuticle thickness, antennae and leg length), behavior and habitat use (Schmalfuss, 1984; Csonka et al., 2013). The three most common surface-active ecomorphological groups are: (1) runners, which have long legs and antennae and move quickly; (2) rollers, which have the thickest cuticle and are able to roll up into a ball to protect their ventral parts, and (3) clingers, which have short and strong legs and they can press down firmly to the substratum (Schmalfuss, 1984, Hornung, 2011; Csonka et al., 2013).

Although isopods are considered to have low dispersive capacity (Lemos de Castro, 1971), some authors understand that woodlice food selection is driven by direct locomotion to a food source (Zidar et al., 2002; Gerlach et al., 2014). Monitoring isopod dispersal on a local scale is of paramount importance for the understanding of the relationships between the detritivores and the fauna and/or flora (food source) associated with the colonization process and the edaphic community establishment (Purger et al., 2007; Quadros, 2010).

Although some studies do not recommend the use of external marking on woodlice (Drahokoupilová and Tuf, 2012; Tuf et al., 2013), there are still many questions regarding intra-moult period observations, mortality rates, behavioral differences between ecomorphological groups and durability of the marks in terrestrial isopods. Thus, there were two objectives of this present study utilizing a runner, a roller and a clinger isopod species: 1) to test materials for external marking; and 2) to observe possible influences of this process on the feeding performance of woodlice, since this is an essential behavior in an animal’s life. We hypothesized that the most efficient material will be the one with the highest frequency of weekly-marked animals remaining at the end of the 28 day experiment. We expected distinct responses from each different ecomorphological group of isopods based on the thickness of their cuticles in the material efficiency tests. For example, rollers should be more resistant to both materials tested, runners should be negatively affected by them and clingers should show intermediate sensitivity. Additionally, we hypothesize that the best material will not interfere in the ability of the isopod to ingest food and consumptions rates will be similar for the three tested ecomorphological groups, as well as between the treatments (number of marks on each animal).

MATERIAL AND METHODS

Woodlice species

Three terrestrial isopods species from three distinct ecomorphological groups (sensuSchmalfuss, 1984) were used for both experiments: Balloniscus glaber Araujo and Zardo, 1995 (Balloniscidae), an endemic clinger species from the state of Rio Grande do Sul and Santa Catarina, Brazil, associated with Atlantic Forest fragments (Quadros et al., 2009; Kenne and Araujo, 2015; Wood et al., 2017; Campos-Filho et al., 2018); Benthana picta (Brandt, 1833) (Philosciidae), a runner species from the state of Espírito Santo to Rio Grande do Sul in Brazil and also recorded in Paraguay (Campos-Filho et al., 2015); and Armadillidium vulgare (Latreille, 1804) (Armadillidiidae), our roller model, a Mediterranean species with a global distribution and commonly associated with anthropogenic areas (Paoletti and Hassal, 1999). To avoid ambiguity regarding species names they will be referred to by their genus denomination.

The Balloniscus and Armadillidium specimens were collected from a secondary forest in Porto Alegre city, state of Rio Grande do Sul (RS), Brazil (30°12’30”S, 51°10’12”W); and the Benthana specimens were collected at the Henrique Luiz Roesler Park in the municipality of Novo Hamburgo, RS, Brazil (29°41’15”S, 51°06’35”W). Additional specimens of Armadillidium were collected at ‘Campus do Vale’ at Universidade Federal do Rio Grande do Sul (UFRGS) (30°04’07”S, 51°07’10”W). The animals were taken to the ‘Laboratório de Carcinologia’ (UFRGS) and kept in a controlled temperature and photoperiod room (18 ± 1°C and 12:12 hr, respectively). The collection of the animals occurred several times, in order to supply enough specimens for the experiments. The largest body size woodlice were selected for both tests. After experiments, all specimens were returned do their original natural areas.

External marking materials

Two types of materials were used for the efficiency (durability) evaluation: cyanoacrylate glue (LOCTITE^TM Super Bonder Power Flex Gel Control) mixed with silver glitter, and nail polish (Risqué^TM). These two materials were easy to handle and were chosen due to their superior adhesion to the animals’ cuticle, as observed in previous pilot experiments.

Experiment 1: Material efficiency

For each isopod species we used five (Armadillidium, N = 150) or three (Balloniscus, N = 45; Benthana, N = 69) individuals per experimental unit (EU) (a circular plastic container, 8 cm in diameter and 4.5 cm in height) in order to maintain the minimum aggregation required for animal stability (Broly et al., 2012). Each EU contained a shelter (a piece of 1 ( 2 cm folded polypropylene paper), a moist cotton ball for internal moisture maintenance and leaf discs (1 cm in diameter) of Machaerium stipitatum (DC) Vogel (Fabaceae). This plant species is considered a good food source to feed to isopods (Quadros et al., 2014).

All terrestrial isopods in two-thirds of the total number of EU’s of each species were marked every seven days, one-third with nail polish and one-third with glue + glitter. The external marking procedure consisted of the application of a small drop of the material with a very small pointed brush, initially on the cephalothorax and later on the subsequent pereonites (Fig. 1). The remaining one third were considered the control treatment and the isopods were only handled and underwent the same marking process, but with distilled water. Before the animals were returned to the EU’s after this step, they were left in a Petri dish (13cm in diameter) for approximately 5 minutes to dry the marking material on their cuticle. The observation period lasted 28 days.

Figure 1
Woodlice (Armadillidium vulgare) external marking process during the 28 days of experiment.

Animals that showed any incidence of marking material inefficiency (i.e., death or a non-durable marking event) were removed from the EU’s. In these cases, the circumstance of death and the number of days the individuals had survived in the experiment were registered. The material durability was demonstrated through Kaplan-Meier curves and Log-Rank (Mantel-Cox) analysis (α<0.05). The mortality rates were calculated weekly, observing the remaining number of animals in each event of marking.

Experiment 2: Influence on feeding performance

For the feeding activity test we selected the material which we observed the lowest mortality during the efficiency trials. New individuals of each species, who did not participate in Experiment 1, were fed with carrots in order to empty their digestive tract of any previous food source (Wood et al., 2012). This is observed through the presence of orange fecal pellets in the EU. Intermoult animals of both sexes were used in the experiment, except for ovigerous females (Wood et al., 2012). After this, each animal received either one, two, three, four or no (unmarked = control treatment) external marks and was placed individually in EU’s (5 cm in diameter and 2.5 cm in height). Each EU contained three M. stipitatum leaf discs (1 cm in diameter) and a wet cotton ball. All leaf discs were previously dried for 48 hours at 60°C, weighed (mg) and then re-hydrated before being offered to the animals (Boelter et al., 2009).

The oniscidean isopods were weighed at the beginning, at every one or two day interval, and at the end of the experiment. For Armadillidium (50 individuals) and Benthana (47 individuals) the experiment lasted 10 days. For Balloniscus (32 individuals) it lasted seven days. The remaining plant material was dried and weighed at the end of the experiment. In order to obtain the autogenic mass loss percentage of the leaves, leaf disks were weighed from EU’s without woodlice (Wood et al., 2012). The relative consumption was calculated according to the adapted formula from Waldbauer (1968):

EQUAÇÃO 01

where (RC) is the Relative Consumption, (M_if ) the initial food (three leaf discs) mass (mg), (M_af ) the food autogenic mass loss (mg), (M_ff ) the final food mass (mg) and (M_isop ) the mean isopod mass (mg). Relative consumption was compared between treatments using ANOVA, and post-hoc Tukey test (α<0.05).

RESULTS

Experiment 1

The durability of the marks for the two materials used on the three oniscidean species showed no statistical difference, except for the occurrence of a significant higher frequency of remaining animals in the Benthana control group (Log-Rank: Armadillidium = 4.830, p = 0.089; Balloniscus = 3.706, p = 0.157; Benthana = 8.446, p = 0.015). At least until the 15^th day of observation all species showed more than 50% survival of total individuals with the marks, and this fact indicates that the animals can tolerate three external marking events on a weekly frequency (Figs. 2-4). Armadillidium showed the highest proportion of live animals bearing all marks reaching the 28^th day, following by Balloniscus and then Benthana (Table 1).

Figure 2
Kaplan-Meier curves for the external marking efficiency (durability) of the two materials tested on Armadillidium vulgare for 28 days of observation. Vertical dotted lines indicate the second, third and the forth event of external marking (8^th, 15^th and 22^th days, respectively). Horizontal dotted line delimits the 50% of remaining marked individuals.

Figure 3
Kaplan-Meier curves for the external marking efficiency (durability) of the two materials tested on Balloniscus glaber for 28 days of observation. Vertical dotted lines indicate the second, third and the forth event of external marking (8^th, 15^th and 22^th days, respectively). Horizontal dotted line delimits the 50% of remaining marked individuals.

Figure 4
Kaplan-Meier curves for the external marking efficiency (durability) of the two materials tested on Benthana picta for 28 days of observation. Vertical dotted lines indicate the second, third and the forth event of external marking (8^th, 15^th and 22^th days, respectively). Horizontal dotted line delimits the 50% of remaining marked individuals. * indicates statistical significance.

Table 1
Percentage of the remaining animal bearing all four marks in the end of 28 days of experiments.

Material	Armadillidium	Balloniscus	Benthana
Nail polish	92.0%	35.7%	15.0%
Glue + glitter	89.8%	46.7%	29.2%
Unmarked	100%	64.3%	61.1%
Total	93.9%	48.8%	33.9%

The following events were observed during the experiment: lost mark (nail polish or glue+glitter drops in the EU), lost mark on exuvia (marks intact on old exoskeleton), natural death, death during ecdysis (dead woodlice partially attached to the old exoskeleton), cannibalism (dead individuals with no cephalothorax and/or pleon, probably consumed by the other animals in the same EU) and presumed drowning (dead animals trapped in the cotton ball). The drowning and cannibalism occurrences were not considered for efficiency comparison between materials. They most likely had no direct relation to the external marking process or with the material composition used in this process.

Armadillidium showed the lowest mortality rates in all treatments, regardless of the events of marking. Unexpectedly, unmarked Balloniscus exhibited a crescent mortality rate during the experiment, while the nail polish treatment fell to 0% mortality after the third event. The highest mortality rate was observed in Benthana for the last week of experiment (33.3%, nail polish treatment) (Fig. 5).

Figure 5
Mortality rates for the three woodlice species, unmarked and marked with nail polish and glue + glitter. The events of marking corresponding to the 1^st, 8^th, 15^th, 22^th and 28^th day, respectively.

Although glue+glitter exhibited a higher durability but not significant for Balloniscus and indicated statistically different for Benthana, this material combination was the only one where we observed death incidents during the ecdysis process (Fig. 6). Thus, nail polish was elected for the ecdysis process behavior experiments. Animal death during feeding (a crucial arthropod event) indicates a greater risk for oniscidean survivorship and for the efficient use of these materials in field studies.

Figure 6
Number of inefficiency events during the 28 days experimental observation on three terrestrial isopods marked with glue + glitter, nail polish and the unmarked treatment. * indicates death event during ecdysis.

Experiment 2

The highest consumption of M. stipitatum leaves was observed in Armadillidium and Balloniscus control treatments (0.518 mg/mg*day and 0.816 mg/mg*day, respectively), and in the four-mark treatment for Benthana (1.015 mg/mg*day). There was no difference in the mean relative consumption of M. stipitatum leaf discs between treatments with marked and unmarked animals in the Armadillidium and Balloniscus experiments (ANOVA, F_{Armadillidium} = 1.8496, p = 0.1351; F_Balloniscus = 0.8160, p = 0.5279) (Figs. 7, 8). Benthana, on the other hand, showed a distinction in the mean relative consumption of the leaf discs, only in the four-marks treatment when compared between marked animal treatments. (ANOVA, F_Benthana = 7.5440, p = 0.0002) (Figure 9).

Figure 7
Mean relative consumption of Armadillidium vulgare fed with three leaf disks of M. stipitatum during 10 days of experiment. Each treatment corresponding to the number of nail polish external marks on animals' cuticle (zero - unmarked, one, two, three and four). Vertical bars indicate standard error.

Figure 8
Mean relative consumption of Balloniscus glaber fed with three leaf disks of M. stipitatum during seven days of experiment. Each treatment corresponding to the number of nail polish external marks on animals’ cuticle (zero - unmarked, one, two, three and four). Vertical bars indicate standard error.

Figure 9
Mean relative consumption of Benthana picta fed with three leaf disks of M. stipitatum during 10 days of experiment. Each treatment corresponding to the number of nail polish external marks on animals’ cuticle (zero - unmarked, one, two, three and four). Vertical bars indicate standard error. Different letters above the bars show statistical difference through analysis of variance (ANOVA) and post-hoc Tukey’s test (α<0.05).

DISCUSSION

Both materials used herein followed most basics premises of viable techniques for marking and recapture studies (Southwood and Henderson, 2000; Wang et al., 2010). They are easy to apply and the materials have low cost. Even though glue+glitter has made the ecdysis difficult, it showed no significant influence on the mortality rates for almost all isopods species tested in this work. Studies with aeglid crabs, beetles, stinky bugs, limulus and scorpions report the use of cyanoacrylate glue, and none of them have mentioned any effect on mortality rates (Bueno et al., 2007; Backlund et al., 2008; Lee et al., 2013; Bibbs et al., 2014).

Regarding the nail polish, it did not negatively interfere in the animals feeding activity. Its efficiency, durability and ease of application are also commented with freshwater crustaceans, spiders, beetles and stinky bugs (Parmenter et al., 1989; Dreyer and Baumgartner, 1997; Zambonato et al., 2010; Ramalho et al., 2010). Castillo and Kight (2005) used nail polish in prey-predation behavioral experiments with two terrestrial isopods species, and they do not report any external marking influence in relation to the parameters analyzed. Recently, Leclercq-Dransart et al. (2019) performed the same technique in physiology experiments with four woodlice species. They also did not describe any negative aspects about nail polish’s external marks. However, Drahokoupilová and Tuf (2012) and Tuf et al. (2013) do not recommend nail polish for external marks on woodlice because their results indicated high mortality rates through the marking process. In addition, the authors also observed low nail polish durability. Our results showed there is little relation of death and the external marking procedure, since dead animals also were observed in the unmarked treatments. Besides, we emphasized that nail polish did not affect ecdysis success and the woodlice survivorship during this process. Nail polish’s durability observed in the present study was longer than cited by Drahokoupilová and Tuf (2012) (9 days) and some individuals reached 28 days with the external mark, as observed by Tuf et al. (2013).

According to our observations, direct marking on the woodlice cuticle may have influenced the woodlice survivorship and the mark’s adhesion due to particular characteristics of each oniscidean ecomorphological group, regardless the material used. Unlike what is described for other terrestrial arthropods (Roer et al., 2015), the woodlice cuticle thickness varies among different groups, and this characteristic provides to rollers, runners and clingers’ species distinct permeability degrees (Greenaway and Warburg, 1998; Csonka et al., 2013; Broly et al., 2015; Wood et al., 2017; Khemaissia et al., 2018). Armadillidium showed low sensitivity to external marking and higher frequency of marked individuals until the end of the 28 days experiment. This can be explained as a result of their cuticle characteristics: thickness, low permeability and low water loss (Broly et al., 2015; Nako et al., 2018; Csonka et al., 2018). Armadillidium can increase its resistance to desiccation in dry microhabitats or when exposed to high temperatures (Csonka et al., 2018) and additionally, as we observed, to the possible nail polish toxicity.

The Benthana species has a delicate, lighter and flexible cuticle, which can be highly affected by fluctuation in temperature and humidity and less tolerance to environmental changes, as described for another runner species, Atlantoscia floridana (Van Name, 1940) (Araujo and Bond-Buckup, 2005; Sokolowicz and Araujo, 2013; Wood et al., 2017, Csonka et al., 2018). The high permeability and thinnest cuticle compared to the species we tested in the present study may explain the higher number of death events and higher frequency in cases of mark loss. Even though we observed individuals trapped in the old exoskeleton only when they were marked with glue+glitter, Benthana was the most fragile to both external marking materials.

As described by Wood et al. (2017), the Balloniscus’ cuticle has lighter thickness in comparison to the Armadillidium one and it has many curved scales. In relation to runner species, clingers demand a tougher cuticle because the individuals need to adhere to the substrate to protect their soft parts from predators (Wood et al., 2017). In the present study, material’s external marking efficiency on Balloniscus’ cuticle was intermediate when compared with the other two species. This result is supported by the clinger's intermediary cuticle attributes between rollers and runners discussed above.

Taking into consideration that the bigger the woodlouse the longer the intermoult interval (Lawlor, 1976), we selected the largest animals for both tests. This strategy was adopted to avoid the chances of the loss of the mark after ecdysis (Frisch and Hobbs, 2006; Bueno et al., 2007; Zambonato et al., 2010; Tuf et al., 2013). Even attempting to minimize the effect in case of ecdysis, the information about the animal location, for example, may be not totally lost. The exuvia still maintains the last marking data, as we observed, and it can be found in the field if the animal monitoring studies use periodic trap observations. However, this will be that individual’s last dispersion record. Thus we recommend the use of nail polish only on the biggest adult animals and implement the marking as soon as possible after the ecdysis. Intermoult period has a crucial role in this process.

There is little quantitative information about marking techniques' effects on feeding activity of invertebrates. In general, the studies discuss some qualitative data along with other behavioral approaches (Kobelt et al., 2009; Drahokoupilová and Tuf, 2011, 2012; De Souza et al., 2012; Wells and Sebens, 2017). A great number of studies that use marking techniques only report their main application for distinct treatments identification in experiments (Rieske and Raffa, 1990; Loreto et al., 2009; Perry et al., 2017; Leclercq-Dransart et al., 2019). Bueno et al. (2007) observed marked and unmarked aeglid crabs in baited traps, which means the animals were attracted to food in spite of the external marking process. In a study with another detritivore, the millipede Glomeris tetrasticha Brandt, 1833, the authors observed unmarked animals feeding more often than the marked individuals (Drahokoupilová and Tuf, 2011). They also compared other behavioral parameters, and it was suggested this marking technique could provide biased or false results (Drahokoupilová and Tuf, 2011). Drahokoupilová and Tuf (2012) recorded a decrease in the feeding activity of marked terrestrial isopods compared to unmarked animals. Our data showed the marked and unmarked woodlice feeding similarly, quantitatively. Only four-marked Benthana exhibited higher mean relative consumption of M. stipitatum leaf discs than the other marked animal treatments. This probably indicates the three oniscidean species are not deprived of the ability to feed, since none of them showed significant statistical difference in comparison to control treatments (unmarked woodlice).

Considering our results, the external marking did not show negative influence on feeding activity of the terrestrial isopods and this method using nail polish can be effective for mark-recapture and monitoring studies in the field, taking into account the whole species intermoult period and other behavioral aspects. More studies about these topics are being conducted to enhance these techniques.

ACKNOWLEDGEMENTS

The authors thak Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting scholarship to DCK, fellowship to PBA and GLGS, Instituto de Biociências of UFRGS for the assistance, colleagues from Laboratório de Carcinologia and Laboratório de Ecologia Química e Quimiotaxonomia (Leqtax) for the help on perform the experiments and Augusto F. Huber for editing the image of marked animals.

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• Zoobank:

  http://zoobank.org/urn:lsid:zoobank.org:pub:CAA6F33A-8124-46DA-A401-B6BD1E9D838A

Publication Dates

• Publication in this collection
  02 Dec 2019
• Date of issue
  2019

History

• Received
  27 June 2019
• Accepted
  30 Sept 2019