DOES THE REDUCTION OF LOCOMOTOR ACTIVITY SERVE AS AN AGGRESSION AVOIDANCE MECHANISM IN SHREWS (SORICIDAE)?

Rafał Zwolak, Leszek Rychlik

ABSTRACT

The hypothesis, that shrews avoid intra- and interspecific aggression through a reduction of their loco-motor activity, was tested. In 55 neutral arena tests (each of 30-min-duration), 10 subadult individuals of Sorex minutus, 14 of S. araneus, 9 (including 1 adult male) of Neomys anomalus, and 13 of N. fodiens were used. Loco-motor activity and sum of conflicts (attacks, chases, escapes and threats) in 1st-5th minutes of interactions (phase I) and 10th-15th minutes (phase II) were compared. In all the species, both in intra- and interspecific interactions, a reduction of mobility between phases I and II was observed (in 6 out of 16 comparisons the difference was statistically significant, and in the 7th comparison it was fairly significant). The highest reduction of activity was observed in the smallest S. minutus, and the lowest reduction (no difference was significant) in the largest, dominating N. fodiens. In all the species, and in all combinat

Key words: shrews, Neomys, Sorex, behaviour, loco-motor activity, aggression avoidance.

INTRODUCTION

The method of dyadic encounters in neutral arena was used relatively often to study agonistic behaviour in shrews [e.g. 2,7,12,30]. Usually, intraspecific conflicts were the subject of these experiments. The researchers studied prevalently domination and factors influencing it, such as sex and age of animals [19], or place of interaction and territory ownership (residents versus intruders - [23]). The analyses of interspecific interactions in the neutral field remain rare [e.g. 14].

Nevertheless, using other enclosure and laboratory methods, the mechanisms of aggression avoidance in the interactions of shrews have been already studied. [20,21] suggest that acoustic communication serves as such a mechanism. According to [11,28] and others, olfactory communication plays a role. Mechanisms found in N. anomalus were (1) learning the presence of aggressive N. fodiens in the vicinity and (2) group occupation of shelters [15,16]. S. minutus avoided aggression of S. araneus by maintaining distance [5,6]. Another possible - and still not investigated mechanism in shrews – could be the asynchronous activity and the reduction of loco-motor activity.

In this study we analysed the changes of loco-motor activity (mobility) in four species of shrews coexisting in Białowieża Forest (pygmy shrew Sores minutus, common shrew S. araneus, Mediterranean water shrew Neomys anomalus, and Eurasian water shrew N. fodiens) during intra- and interspecific interactions. Our goal was to test the hypothesis stating that shrews avoid conflicts by reducing mobility. We predicted that, with the passage of time, individuals (or species) exposed to the aggression of other shrews will significantly reduce their activity, while the dominating shrews will not. Using the method of dyadic encounters in the neutral arena, we simulated interactions and conflicts that probably take place in the wild among individuals from the mentioned species.

METHODS AND MATERIALS

Animals were caught in the wet habitats of Białowieża Forest in July and September 2000, and in October 2001. After transportation to the laboratory, they were placed in individual cages (30 × 40 × 15 cm) and acclimatised to the captive conditions over at least 5 days. Every cage was equipped with a shelter: a handful of moss in the case of pygmy shrews, and a reversed pot filled with moss for all other species. Litter consisted of a mixture of sand, sawdust, peat, and moss. Food (minced meat, fly and mealworm larvae, and dried crustaceans Gammarus sp.) and water were provided ad lib. In the laboratory, a natural cycle of light and darkness was maintained, temperatures oscillated between 16° and 20°C, and air humidity equalled about 80%.

Only subadult shrews were tested: 10 individuals of S. minutus, 14 of S. araneus, 9 of N. anomalus, and 13 of N. fodiens. An exception was made for N. anomalus because of the difficulties in catching these rare animals: among nine individuals tested, one adult male was used.

Dyadic encounters were conducted under the same temperature and humidity conditions as was maintained in the room with individual animals’ cages. The animals were tested during daytime, usually between 9:00 and 16:00 hr; that is during the period of shrews’ reduced activity [3,27]. In each test, an intra- or interspecific pair of animals was placed in the glass terrarium (measuring 70 × 30 × 40 cm) and their behaviour was video-recorded. To ensure an adequate quality of the record, the terrarium was illuminated with a 60-W lamp hanging about 1.5 m above.

Each test lasted 30 minutes and consisted of four consecutive parts. In the first one (“separated”, duration 5 minutes), the animals stayed on the halves of the terrarium, separated by the Plexiglas partition. During this stage, shrews could settle in after removal from individual cages and explore the new surroundings, as well as display the basic level of the loco-motor activity (i.e. without physical contact with the second individual). In the second part (“together”, duration 5 minutes), the partition was removed and the animals could begin interactions in the so-called “neutral open arena”. In the third part (“food”, duration 10 minutes), a bowl with minced meat was placed in the middle of terrarium’s floor, in order to stimulate animals to compete for food. In the fourth stage (“shelter”, duration 10 minutes), the object of the possible competition was changed: namely, the bowl was replaced with a reversed pot, which served as a shelter.

In order to study the relationship between loco-motor activity and conflicts, the behaviour of shrews in two phases of the test was compared. Phase I consisted of 5 minutes of the part “together” (i.e. from 1st to 5th minute of the interaction), while phase II was composed of the last 5 minutes of the part “food” (that is from 10th to 15th minute of the interaction).

The lines that were drawn on the bottom of the terrarium divided it into 8 equal rectangles. The number of lines crossed by an animal (i.e. the number of moves from one rectangle to another) during 5 minutes served as a measure of the loco-motor activity (mobility index). Conflicts included offensive behaviours (attacks, combats, chases), defensive behaviours (retreating, jumping away, running away and escaping), and threatening postures (stance, tripedal, sideways, back and upright; detailed descriptions of these behaviours and postures are in [17,22,31].

In total, we analysed the shrews’ behaviour in 55 tests. The number of trials per each pair of species is presented in Table 1. Each individual took part in 1-4 trials (mean 2.8 trials per individual), but each time with a different species. The only exception was made by the participation of one of the Mediterranean water shrews in two tests with pygmy shrews, caused by already mentioned difficulties with catching the sufficient number of animals. In order to calculate the results for N. anomalus, we took into account only the first from these two trials (see Table 1). Consecutive tests of the same individual were separated by at least a 3-day interval.

In statistical analysis, differences within species-combinations (paired values) were compared using the Wilcoxon test, and differences between species-combinations (unpaired values) with the use of U Mann-Whitney test. Regression analysis was also conducted [9,29].

RESULTS

Intraspecific interactions

All studied species reduced their mobility in the second phase of the experiment (Fig. 1). The decrease was statistically significant in S. minutus (Wilcoxon test: Z = -2.201, p = 0.028) and in S. araneus (Z = -2.521, p = 0.012). Arranging the species from the most to the least active, in both phases the following order arose: N. anomalus > S. minutus > S. araneus > N. fodiens. During phase I, the activity of N. fodiens was significantly lower than the activity of N. anomalus (U Manna-Whitney test: U = 3.0, p = 0.01), and of S. minutus (U = 6.0, p = 0.02). During phase II N. anomalus was significantly more mobile than the three other species: N. fodiens (U = 3.5, p = 0.02), S. araneus (U = 6.0, p = 0.05), and S. minutus (U = 6.0, p = 0.02).

In every species, the number of conflicts was lower during phase II than during phase I (Fig. 2.). This reduction was statistically significant in N. fodiens (Z = -2.171, p = 0.030), and in S. araneus and N. anomalus was marginally significant (Z = -1.993, p = 0.064 in S. araneus and Z = -1.859, p = 0.063 in N. anomalus). Considering the number of intraspecific conflicts, in both phases of the test the order was as follows: N. anomalus > N. fodiens > S. minutus > S. araneus. With the exception of the differences between S. araneus and S. minutus in both phases and between N. fodiens and S. minutus in phase II, all remaining interspecies differences in the number of conflicts were statistically significant (U = 0.0 to 12.5, p = 0.001 to 0.038).

Interspecific interactions

A decrease of the shrews’ mobility between phases I and II was observed in every combination of species (Fig. 1). Statistically significant differences were found in the following interactions: (1) common shrews versus pygmy shrews (Z = -2.336, p = 0.018 in S. araneus and Z = -2.197, p = 0.028 in S. minutus), (2) common shrews versus Mediterranean water shrews (reduction significant only in S. araneus: Z = -2.100, p = 0.036), and (3) Mediterranean water shrews versus Eurasian water shrews (reduction significant only in N. anomalus: Z = -2.103, p = 0.035). In interactions between S. minutus and N. anomalus, the decrease of Mediterranean water shrew’s mobility reached the margin of significance (Z = 1.826, p = 0.068).

The number of conflicts dropped between the phases I and II in every tested pair of species (Fig. 2). Nevertheless, only two significant decreases were found: (1) in S. minutus interacting with S. araneus (Z = -2.366, p = 0.018) and (2) in N. fodiens interacting with N. anomalus (Z = -2.380, p = 0.017).

Reduction of loco-motor activity versus reduction of aggression

In general, the largest decrease of mobility was observed in the smallest S. minutus (on average by 38.0 index points), and the smallest decrease in the biggest, dominating N. fodiens (on average by 22.8 points and all the differences were insignificant). In contrast, the most pronounced reduction in the number of conflicts was recorded in N. fodiens (on average by 7.7), and the least in S. minutus (by 3.3) and S. araneus (by 3.4). The regression analysis showed the negative (reversed) relationship between the decrease of mobility and the reduction of the number of conflicts: the bigger the decrease in mobility, the smaller the drop in the number of conflicts (Fig. 3). This relationship was marginally significant (p = 0.051).

DISCUSSION

Because the studied species are syntopic [e.g. 26], and their temporal niche markedly overlap (from 74 to 93%; [27]), frequent direct contacts seem to be inevitable. Then, the interactions following are usually agonistic [4,5,14]. In this situation, the existence of efficient mechanisms of aggression avoidance or reduction is of great importance for coexisting species. Some of these behavioural mechanisms have been already described (see ‘Introduction’). But so far it has not been investigated whether the reduction of loco-motor activity serves as a behavioural expedient reducing the number of conflicts in Soricidae.

A decrease in the shrews’ mobility between phases I and II of the test was found in all studied species (but the smallest reduction took place in the biggest, dominating N. fodiens). As a consequence, the number of conflicts also dropped in every combination of species. Although not all differences were statistically significant, the tendency is clear. Thus, this result complies with the hypothesis that a reduction in mobility acts as a mechanism for aggression avoidance.

However, we presumed that the greatest reduction would be seen in the mobility, then a larger drop in the number of conflicts will follow. The observed reverse relationship between reduction in mobility and reduction in the number of conflicts contradicts our prediction. In spite of relatively the biggest decrease in the mobility of S. minutes, the reduction in the number of conflicts was the least marked in this species. In N. fodiens the opposite was true, whereas we expected that Eurasian water shrews, as dominants, do not have to use this mechanism of aggression avoidance (i.e. that both their mobility and number of conflicts will drop only slightly or not at all).

Considering the above result, we cannot rule out the possibility that the reduction in animals’ mobility during the trials had different reasons than the avoidance of aggression. First, this decrease could be caused by a diminishing motivation to escape and/or explore the terrarium, coupled with the habituation to stressful experimental conditions. The factors that could elicit stress in animals tested in the neutral field are: capture and removal from their cages, placement in the unfamiliar surroundings, bright light, and open space [8]. In fact, some aspects of shrews’ behaviour could indicate stress, e.g. freeze, moving mainly along the sides of the terrarium, or frequent defecation. Nevertheless, these factors strongly influence the activity of solitary animals in the neutral field [8,24], whereas in our experimental treatment a significant part of the activity was certainly induced by interactions with another animal. In addition, the influence of listed factors was largely eli minated in the first stage of the experiment (part “separated” that was not used to calculate the results) when the animals could habituate, explore their new surroundings, and lessen their motivation to escape. As a result, they reduced their activity before the analysed part of the trial.

Secondly, lower mobility during the second phase could be related to the presence of food. However, shrews were rarely stopped by food: the animals ate a little or nothing and spent a relatively small amount of time by the bowl (on average 72.1 s per 10 min; range 19.7-133.0 s). On the other hand, we cannot preclude the possibility that the presence of food stimulated shrews to increase their activity and induced additional conflicts.

The larger the studied shrew species, the lower its loco-motor activity during the tests. N. anomalus, which yields only to N. fodiens in body size, which was also the most active species, posed an exception to this rule. [14] compared the behaviour of these two species in the open field and also found a much higher mobility in N. anomalus than N. fodiens. This phenomenon is attributed to the greater susceptibility of N. anomalus to stress in the open field and/or unfamiliar surroundings [14,15,18]. This susceptibility can also explain the preferences of N. anomalus for habitat with dense plant cover [1,26], decreased foraging efficiency in absence of cover [25], and – what is the most important in the context of this study – increase in the number of conflicts [15]. Thus, the highest mobility and the most numerous conflicts observed in this study in N. anomalus were probably caused by a low resistance to the experimental conditions, rather t han by aggressiveness or assuming a dominating position in the community of species studied.

N. fodiens and S. araneus react to experimental conditions by immobility (freeze behaviour) rather than by increased activity. At this time, the animals sat in the corner of terrarium, restricting their activity to sniffing. [14] observed a similar reaction in N. fodiens. Adaptive significance of this behaviour probably relates to the animal finding itself in an open space, protecting itself from being detected by predators [8].

In S. minutus such immobility was rare. Due to their small size, these animals are hard to perceive even when they move and it is easier for them to hide in crevices that are inaccessible for the larger species. Furthermore, predators prefer larger species of shrews as prey [13], which also reduces the threat to S. minutus. On the other hand, considering the unusually small body reserves of pygmy shrews [10], they cannot stop foraging for a longer period. Presumably in this case the risk of starvation exceeds the danger of being hunted by predators or attacked by another shrew. Fortunately, despite high mobility, the number of conflicts involving the participation of pygmy shrews was the lowest among the studied species. It proves that these animals were very effective in aggression avoidance and suggests that they can achieve this through actively maintaining distance.

Numerous conflicts between N. anomalus and S. araneus can be explained by the relatively high mobility of these species, which causes them to frequently run into each other. Nevertheless, another reason could be that these animals have a comparable size, strength, and – as a consequence – intermediate ranks in the interspecific domination hierarchy.

CONCLUSIONS

1. With passage of time, a reduction in both shrews’ mobility and the number of conflicts was observed in all kinds of interactions.

2. However, an inverse relationship between reduction in activity and reduction in the number of conflicts appeared.

3. Thus, further investigations are needed to determine if the reduction of loco-motor activity serves as an aggression avoidance mechanism in shrews.

ACKNOWLEDGEMENTS

We are very grateful to A. Arasim, M. Babski, K. Bochowicz, I. Smerczyński and E. Sorato for their field and technician assistance. S. Prior kindly improved our English. This study was supported by funds of the Mammal Research Institute PAS and by grant no. 6 P04F 036 21 from the Committee for Scientific Research.

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Leszek Rychlik
Mammal Research Institute
Polish Academy of Sciences, Bialowieza
ul. Waszkiewicza 1, 17-230 Białowieża, Poland
tel./fax: (085) 6812289
e-mail: lrychlik@bison.zbs.bialowieza.pl

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