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Foraging behaviour as a mechanism for trophic niche separation in a millipede community of southern Vietnam
European Journal of Soil Biology 90 (2019) 36–43
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European Journal of Soil Biology journal homepage: www.elsevier.com/locate/ejsobi
Foraging behaviour as a mechanism for trophic niche separation in a millipede community of southern Vietnam
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Irina I. Semenyuka,b,∗, Alexei V. Tiunova a b
A.N. Severtsov Institute of Ecology and Evolution, Leninsky prospekt 33, Moscow, 119071, Russia Joint Russian-Vietnamese Tropical Center, Street 3 Thang 2, Q10, Ho Chi Minh City, Vietnam
A R T I C LE I N FO
A B S T R A C T
Handling editor: Prof. C.C. Tebbe
Trophic differentiation is one of the mechanisms for species coexisting in the communities of soil arthropods. Even in saprophagous animals having a generalized diet, separation of the trophic niches can be achieved by using different behavioural foraging strategies. We examined the foraging behaviour and time budget use in two millipede species, Thyropygus carli and Orthomorpha sp., which share the same habitat and have similar diet, in a lowland monsoon forest in southern Vietnam. We performed field observations of the millipedes’ behaviour with 1 min resolution time. For both species, observations covered full day and night with ten replications (240 h for each species). Species differed in their time budget use. T. carli spent most time in searching for food and much less time feeding and resting. Orthomorpha sp. usually spent the middle of the day resting and night time eating. The midday rest and relatively short periods of searching in Orthomorpha sp. are most likely caused by avoiding heat and dryness, whereas T. carli has no circadian rhythm, which is facilitated by a large body size, high mobility and a relative independence of abiotic conditions. We conclude that T. carli behaviour is related to an energy maximising foraging strategy, whereas Orthomorpha sp. realises time minimising strategy. Thus, behavioural differentiations and different use of time budget contribute to the trophic niche separation among coexisting millipede species.
Keywords: Diplopoda Foraging strategy Tropical forest Trophic behaviour Circadian rhythm Time budget
1. Introduction Diplopoda are primary decomposers feeding mainly on dead plant material like leaf litter, decaying wood or fallen fruits on the forest floor [1]. Like many other soil saprotrophic animals, millipedes tend to form species-rich communities, especially diverse in tropical forests [2,3]. Although the species coexistence in communities may be achieved by neutral mechanisms [4,5], most studies indicated a presence of differentiation of ecological niches among coexisting species of saprophagous soil animals, such as millipedes. The niche differentiation can be realised by several mechanisms including segregation in space or in time, as well as by using different food sources [6–8]. Although experimental works on food preferences, and studies of the community trophic structure using stable isotope analysis showed pronounced trophic differentiation in the species-rich millipede communities [9], mechanisms leading to the separation of trophic niches in millipedes remain poorly known. In many animal communities trophic differentiation of species is associated with using different foraging strategies [10–12]. The foraging strategy theory supposes animals tend to use a specific ‘optimal
∗
foraging strategy’ for balancing foraging costs and benefits in order to achieve maximum fitness from foraging [13]. According to this theory there are two main strategies of manipulating the balance between foraging cost and benefit, i.e. ‘time minimising’ and ‘energy maximising’ strategies [13,14]. Energy maximising animals are focused on getting the highest energy input while foraging. It can be reflected in behaviour such as spending a lot of effort searching for food with the highest benefit rate. Time minimising animals tend to reduce the foraging time, namely the searching time or feeding time or both, for the sake of saving time for other activities. Schoener [14] supposed time minimisers need some fixed amount of energy input; they try to get it during minimum time neglecting potentially available extra energy sources [15]. Time minimising strategy can be reflected in such behaviour as a drastic reduction of searching time, which means a decrease in the ability to find high-quality food. Consequently, the amount of consumed food should be increased. Closely related to this strategy is the phenomenon called ‘compensatory feeding’, when feeding animals prefer quantity to quality and consume a large amount of nutritionally poor food [16,17]. The decrease in foraging time for the sake of decreasing the risk of a predator's attacks during searching
Corresponding author. A.N. Severtsov institute of Ecology and Evolution, Leninsky prospekt 33, Moscow, 119071, Russia. E-mail address: [email protected] (I.I. Semenyuk).
https://doi.org/10.1016/j.ejsobi.2018.12.001 Received 5 December 2017; Received in revised form 16 May 2018; Accepted 2 December 2018 1164-5563/ © 2018 Elsevier Masson SAS. All rights reserved.
European Journal of Soil Biology 90 (2019) 36–43
I.I. Semenyuk, A.V. Tiunov
night humidity changes only slightly but after sunrise it decreases quickly, the driest time being the middle of day (Nam Cat Tien biometeorological station, http://asiaflux.net/index.php?page_id=86 [34]).
might be one of the reasons for compensatory feeding [18]. Animals that use time minimising or energy maximising foraging strategies both get enough energy for performing their life cycles, but they often differ in their diet. Features of foraging strategies in different species can be expressed in trophic behaviour such as a different distribution of time between searching and feeding activities [19]. In soil saprotrophic communities, behavioural aspects of foraging are poorly studied with the possible exception of earthworms and termites [20,21]. Millipedes forage mostly in the dark or at twilight [22–25]. Even cave millipede species living in permanent darkness retain a certain circadian rhythm [26,27]. Recent experiments and observations confirm predominately nocturnal activity of millipedes in general, but also revealed species with a weakly pronounced circadian rhythm [28–30]. It indicates that the mechanisms that regulate millipedes’ circadian rhythms are more complicated than it was assumed before, but they are still unclear. In particular, a few works showed that taxonomically closely related species from the same community can differ in the daily time budget use (dividing time between feeding, resting and searching). It can be viewed as differences in feeding tactics leading to trophic differentiation [7,31]. We therefore supposed that behavioural differences contribute into the trophic niche differentiation in millipede communities. In this work we aimed to quantify behavioural differences, especially differences in use of the time budget, among coexisting millipede species. To this end two millipede species were selected from a species-rich tropical millipede community and their diurnal activity was analysed by direct round-the-clock observations.
2.2. Model species The millipede community in Cat Tien National Park includes at least 40 species and most of them share habitats with each other ([35], I. Semenyuk, unpublished observations). The community is quite diverse in trophic habits; stable isotope analysis showed some trophic differentiation even among generalist feeders [9]. Species also differ in their reaction to seasonal changes in moisture and temperature and have a peak of abundance in different seasons. Two millipede species, Thyropygus carli Attems, 1938 (Spirostreptida) and Orthomorpha sp. (Polydesmida; the species is in the process of taxonomic description), were chosen as a model in this study. Both species are generalist feeders as was confirmed by a wide range of consumed materials found in their faeces. These mainly include debris of leaves, dead wood, fungal mycelium and sporocarps, soil, and fragments of arthropods (data not shown). Two model species have mandibles of similar morphological structure [9]. Nevertheless, the stable isotope analysis detected differences in the species trophic niches. T. carli has higher δ15N values and thus appears to be more ‘carnivorous’ and presumably consumes a more protein-rich diet compared to Orthomorpha sp. [9]. (Orthomorpha sp. in this study corresponds to Orthomorpha sp. 1 in Ref. [9]). Both species are quite abundant and conspicuous, though T. carli is considerably larger than Orthomorpha sp. (Table 1). The abundance of both species slightly decreases in the dry season and increases in the rainy season (unpublished observations). Both species prefer similar microhabitats: forest floor, branches of bushes, surface of tree trunks and logs. Unlike most other species, T. carli and Orthomorpha sp. spend most of their time in open habitats and do not hide under bark or in the leaf litter. These features allow observation of the two species under field conditions.
2. Material and methods 2.1. Study site Material was collected in November–December 2014 and May–August 2015 in the Cat Tien National Park (11º25’ N, 107º25’ E, about 120 m a.s.l.). The territory is covered by monsoon lowland forest with Lagerstroemia calyculata, Tetrameles nudiflora, Afzelia xylocarpa, and Dipterocarpaceae species being dominant in the upper canopy [32]. The forest is rich in epiphytes, lianas, and suspended soils, and forms several canopy layers. Leaf litter on the soil surface is present seasonally for about half of the year. The litter layer is quite diverse and consists of leaves of different species, branches and twigs, bark fragments, and also numerous logs of different size and stages of decay. Fruits and seeds are very abundant seasonally and form heaps of decaying organic matter under particular trees. Fungal sporocarps are abundant seasonally on woody debris and on soil. Tree trunks are typically covered by crustose lichens or algae film, and occasionally by moss. Soil in sampling areas is classified as thin clayey brown tropical soil, or Dystric Skeletic Rhodic Cambisol (Clayic) according to the WRB system [33]. There is a monsoon climate in Cat Tien National Park with strongly marked dry and rainy seasons, a mean annual air temperature of 26 °C, an annual rainfall of 2470 mm. Rain mostly occurs in May-September [34]. In the second part of the rainy season large areas in the forest are flooded for a period of up to several months. Abiotic conditions during the dry season are not suitable for most millipede species; from January to April they have a relatively low abundance. Abundance of millipedes also declines in the second part of the rainy season while the forest is partly flooded. Our observations were performed in the beginning of the rainy season (late spring and summer) and in the beginning of the dry season (autumn), when millipedes are most abundant. In non-raining days of these time periods, a typical air temperature under the canopy varies from about 24 to about 30 °C; soil temperature at the depth of 5 cm varies much less, within 25–27 °C (Fig. 1). The coldest time is just before dawn, around 5 a.m., then after sunrise air temperature increases until the middle of day. Relative humidity varies during the day from 90% to 100%. During the
2.3. Data collecting Individuals of the two species were observed in forest habitats at least 200 m away from forest huts, roads, and other human-derived objects. Millipedes were observed on the soil and leaf litter surface, on logs, tree trunks and bushes up to 2 m in height. For finding specimens, neither digging into leaf litter nor shaking bushes were used. Only adult specimens without any visible damage were selected for observation. Observation started 15 min after finding a specimen to eliminate the possible aberration in its behaviour caused by disturbance during searching. Observation of each specimen lasted as long as possible and ceased either when animal went into a hidden or unapproachable place for more than 5 min or when the rain started. Rain strongly affects millipede behaviour; they start moving chaotically and try to hide from raindrops under leaf litter. During the dark period (typically from 6 p.m. till 5:30 a.m.) a head torch was used. As found in preliminary experiments, individuals of the model millipede species do not react to the artificial light, while some other species immediately stop feeding, turn away and hide. During the observation, neither mosquitoes repellent nor sun protection were used, because in preliminary studies some millipedes demonstrated avoiding behaviour when exposed to the smell of chemicals. During the observation any contact with animals (such as touching or breathing at them) was strongly avoided, observer staying minimum at a half meter distance from the millipede. Diplopoda do not have particularly good vision (if any), so no hiding was needed. Following millipedes during their movements was performed very carefully, avoiding potential vibrations or shaking leaf litter or twigs. We separated four main types of millipede activity, including Searching, Feeding, Resting and Grooming (Table 2). We also observed 37
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Fig. 1. Diurnal rhythms of air temperature under canopy, soil temperature, and air humidity in July 2015. Mean values are given with 1 standard deviation as whiskers, n = 15 (days with rain are excluded). Grey areas mark the dark period of the day. Data from http://asiaflux.net/index.php?page_id=86.
2.4. Data analysis
communicating activity, while millipedes interacted with specimens of the same or another species. This activity includes touching each other by antennae during occasional meetings or prolonged interactions like copulating. Communicating activity happened sporadically and in both species took less than 2% of the time budget. Searching for mate that includes specific behavioural patterns happened very rarely during our observations. These types of activity were not included in further analyses. During field observations the type of activity was recorded every minute. In addition, the total distance passed by a specimen per half an hour was recorded, as a measure of species mobility. Searching for specimens and subsequent observations were performed at different times of day uniformly covering light and dark periods. Thus, for both species, observations covered full day and night with ten replications (240 h for each species).
The 24 h of day were broken into 30 min intervals from 0:00–0:30 to 23:30–0:00. The distribution of time among four main types of activity (in %) was calculated for each 30 min interval and averaged across all replications of the same time interval (n = 10 for each species). The duration of single acts of feeding and searching were calculated as the average duration of unbroken acts started at each hour across all 10 replications. The duration of continuous observation differs among specimens, but most observations lasted for less than 2 h (69% of all observations). We therefore considered all half-hour intervals as independent replications. The mobility of millipede species was estimated in mean body lengths (110 mm and 38.2 mm for T. carli and Orthomorpha sp., respectively) passed per 30 min. Values in the text are given as means ± 1 SD. Mann-Whitney U test was used for comparing means. Millipedes can change diurnal activity with season [7], but we did
Table 1 The main characteristics of the two model species of millipedes. For numeric parameters the mean values are given with ± 1 SD. Mann-Whitney U test was used for comparing means. Thyropygus carli
Eyes (ocelli) presence yes Adult body size (mm) 110.0 ± 7.1 (n = 38) δ15N values, ‰ [9] 4.8 ± 1.9 (n = 10) Time used for different activities, per day (%), n = 10 Searching 46.1 ± 5.2 Feeding 21.6 ± 2.5 Resting 16.7 ± 5.5 Grooming 5.8 ± 4.4 Communicating 0.1 ± 0.1 Unknown (could not be observed) 9.7 ± 5.7 Distance passed per day, cm 12298 ± 1731 Distance passed per day, body lengths 1118 ± 157
38
Orthomorpha sp.
U test, p - values
no 38.2 ± 3.8 (n = 44) 1.5 ± 1.0 (n = 5)
not applicable 0.000 0.002
10.4 ± 3.0 38.5 ± 8.3 38.1 ± 12.7 3.7 ± 3.2 1.7 ± 1.7 7.5 ± 12.8 1888 ± 717 497 ± 189
0.000 0.000 0.001 0.199 0.028 not applicable 0.000 0.000
European Journal of Soil Biology 90 (2019) 36–43
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Table 2 Description of the four main types of millipedes’ activities. Main type of activity
Activities observed in the field
Description of activity
Searching
Searching
Millipedes walk slowly and examine the surface by antennae, with lateral moving of the head also being typical. Sometimes millipedes make short stops for a closer examination of certain objects.
Feeding
Eating Grazing Drinking
Millipedes stay and eat Millipedes slowly walk while scraping food from the surface (usually tree trunks) Millipedes make stops for drinking drops of water
Resting
Resting Sleeping
Millipedes make stops for several minutes, antennae can be collapsed to the head or not, the reaction to disturbing stimuli is maintained Millipedes make stops for a prolonged time and do not react to stimuli like wind, antennae are collapsed to the head
Grooming
Millipedes stay and clean themselves
Grooming
not find substantial differences in the behaviour of the model species in different seasons. In T. carli the average duration of resting was significantly longer in dry than in the wet season (22.9 and 13.9% of the whole time budget, respectively), while in Orthomorpha sp. searching in the dry season was longer than in the wet season (21.8 and 9.6%, respectively). Other types of activity were not affected. Data collected in different months were therefore bulked in this study. Males usually spend more time in searching for mates, while females spend more time in feeding [30,36]. Sexing animals during observations without disturbing them was not always possible. To account for the possible sex-related difference in the behaviour we therefore analysed a subset of observations that included sexed animals only. The analysis suggested that the behaviour of males and females (observed within the same time periods) was similar, although both in T. carli and Orthomorpha sp. males were on average more mobile, passing ca. 95% and 55% longer distances, respectively, than females of the same species. Sex-related differences in the behaviour were not likely to affect our main results, as the proportion of males and females in the subset of sexed animals was nearly equal: 56.8 and 43.2% observations, respectively, were made on males and on females in Thyropygus and 53.0 and 47.0% in Orthomorpha.
3.2. Mobility T. carli passed on average 25 ± 9 body lengths per half-hour and ca. 1120 body lengths (123 m) per day (Fig. 4). Orthomorpha sp. passed on average 13 ± 11 body lengths per half-hour and ca. 500 body lengths (19 m) per day. In both cases the difference between species was significant (p < 0.001). The mobility of T. carli peaked in the middle of day (more than 50 body lengths per half-hour) but was never less than nine body lengths per half-hour. Orthomorpha sp. was mostly immobile in the afternoon and started moving after sunset. Its mobility peaked around 9 p.m. (up to 39 body lengths per half-hour). 4. Discussion 4.1. Circadian rhythm Most millipede species have a pronounced circadian rhythm and are active mainly at dusk or night [22]. Orthomorpha sp. behaviour was quite typical, i.e. millipedes were more active during the dark period (Fig. 2). Changes in the activity patterns seemingly correlated with abiotic conditions; searching and feeding became much less frequent and mobility decreased with increasing temperature and dryness in the afternoon (Fig. 1). Millipedes loose much more water with increasing temperature [1,36], which can explain the reduction in activity during the hottest part of the day. Orthomorpha sp. has very thin integuments in comparison with many other millipede species in the studied community (I. Semenyuk, unpublished results). Resting in the hottest part of the day in Orthomorpha sp. can be induced by physiological intolerance to dry and hot conditions, but can also appear as the way to save energy when the cost for maintenance of activity is too high because of a high rate of water loss [37]. Such strategy is widespread among desert animals [38]. Many insects use daily torpor for saving energy, especially in non-suitable weather conditions [39]. The role of abiotic conditions in regulating Orthomorpha sp. behaviour is still unclear. Orthomorpha sp. are blind and often choose for the rest open sites such as bushes, leaves, or tree trunk surfaces, rather than soil or other sheltered microsites. Millipedes change resting place if direct sunlight comes (the midday increase in the mobility is likely related to this behaviour; Fig. 4), but usually remain in the open sites where temperature increases significantly during the day. The daily activity patterns of T. carli differed strongly from those of Orthomorpha sp. Proportions of activities in time budget did not correlate with time of the day (Fig. 2). Moreover, the mobility peaked in the middle of the day, which is the hottest and driest time (Fig. 4). This phenomenon is probably related to morphological traits of T. carli that increase its resistance to abiotic conditions. These millipedes have very thick and well calcinated integuments, and are much bigger than Orthomorpha sp. which gives them a more favourable surface-to-volume ratio. In addition T. carli is rufous colour and has a glossy body surface,
3. Results 3.1. Time budget T. carli used 46 ± 5% of the time for searching, 22 ± 3% for feeding, and 17 ± 6% for resting (Table 1, Fig. 2). Proportions of main activities did not change during the day. Orthomorpha sp. spent 10 ± 3% of the time searching, 39 ± 8% feeding, and 38 ± 13% resting. Feeding took maximum time in the dark period (up to 81% at 4:00–4:30 a.m.) and decreased in the light period to only about 5% from 2 p.m. to 4 p.m. Resting took minimum time in the dark period (around 5% from midnight till 5 a.m.) and maximum time in the light period (up to 93% at 3:30–4:00 p.m.). Grooming did not take more than 20.6% of the T. carli time budget, it was more frequent before dawn and before midday. Orthomorpha sp. spent a maximum 17.2% of time grooming; this activity was more frequent at night while no grooming was observed during the midday resting period. The duration of single feeding and searching acts did not change across the day in T. carli (13.9 ± 5.2 min and 16.1 ± 3.7 min, respectively, Fig. 3). In Orthomorpha sp. searching acts were shorter (9.6 ± 4.5 min) and feeding acts much longer (32.4 ± 18.8 min) than in T. carli (p < 0.001 in both cases). The duration of feeding acts in Orthomorpha sp. did not differ between light and dark periods. As a rule, feeding acts were longer during the first half of the day than in the afternoon (Fig. 3). 39
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Fig. 2. The distribution of main types of activity in daily time budget of T. carli (upper panel) and Orthomorpha sp. (lower panel). Standard errors (n = 10) are shown for the proportion of searching to illustrate the degree of variability. Grey areas mark dark period of the day.
properties [44,45]. The major part of the knowledge on the food choice of millipedes is based on laboratory experiments that used a restricted set of leaf litter from different species or of a different quality, while in the field millipedes use a wider range of food items [46,47]. Differentiation in the diet among millipede species can possibly be related to different energetic strategies. This assumption is indirectly supported by the stable isotope analyses which indicated that T. carli has higher trophic level than most other species in the community including Orthomorpha sp. [9]. High δ15N values of T. carli tissues can indicate feeding on a more protein-rich diet [48,49]. According to our observations, Orthomorpha sp. in most cases fed on algae and lichen films on tree trunks or on the soil surface and only rarely on fungal fruit
whereas Orthomorha sp. is black and ridged. Likely, a large light-reflecting and well-protected body is more resistant to overheating and water loss and allows T. carli to maintain activity even at the hottest time of the day. 4.2. Food selection and daily time budget Large saprotrophic invertebrates including millipedes are food-selective. Their food selection is based on physical and chemical properties of food material, such as physical softness and wetness of litter [40], stage of decomposition [41,42], abundance and palatability of microflora [43], presence of secondary compounds or other chemical
Fig. 3. The duration of single feeding and searching acts during the day in two millipede species. Mean values for each hour are shown with 1 SE, n = 10. 40
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Fig. 4. The distance passed by two millipede species per half-hour intervals during the day. Mean values are shown with 1 SE, n = 10.
The amount of energy spending for foraging (mainly for searching food) differs widely among animals. In some cases it is so low that it can be not taken into account (e.g. walking in ants [56]) or appears as the main limiting factor for foraging (e.g. flying in humming birds and in other birds [57,58]). Consumption of low nutritional food makes foraging cost more significant as a limiting factor because it restricts the energy intake that needs to cover foraging efforts and other activities. As Orthomorpha sp. consumes less nutritional food than T. carli, minimising searching time is a possible way to minimise foraging cost.
bodies even if they were abundant. On the contrary, T. carli was often observed eating fungal fruit bodies, tree seeds and fruits; these food items are more N-rich and nutritional than algae and lichens [50,51]. Furthermore, Orthomorpha sp. mostly ignored dead insects or other protein-rich materials, while T. carli usually ate them. Such differences in food preferences of examined millipede species suggest differences in their energy balance and in the choice of optimal foraging strategies. Peculiarities of the food selection by two species might be related to morphological traits of mouthparts and particularly to the difference in the mandible structure. T. carli has more robust teeth and chewing parts of mandibles while Orthomorpha sp. has more dense teeth on pectinate lamellae [9], which can be used for scratching of thin organic films from hard surface as it was shown in cave millipedes [52]. Wolf et al. [53] singled out three main and mutually dependent components influencing animal's trophic behaviour: foraging time, foraging efficiency, and non-foraging energetic. Assuming that an organism requires a fixed amount of energy input, changes in one component should lead to changes in others. Our data suggest that Orthomorpha sp. is limited in the foraging duration by abiotic conditions. On the other hand, this species consumes relatively abundant but nutritionally poor food. This should lead to minimising the searching time and maximising the feeding time in order to obtain the required amount of energy. Indeed, compared to T. carli, Orthomorpha sp. uses much less time for searching than for other activities. Orthomorpha sp. spends most of its active period (night and first half of day) feeding. T. carli spends more time searching and does not have long rests (minimal time compared to other activity types, Fig. 2), thus for obtaining a required amount of energy T. carli can increase its foraging efficiency by consuming high nutritional food as it was indeed observed. Millipedes likely do not have receptors for effectively detecting food items from a distance. Seemingly, they can estimate the palatability of food at a short distance only, when it can be touched by antennae [1,54]. Therefore searching for particular items must take a prolonged time. In the case of Orthomorpha sp., limited foraging time and relatively small body size decrease the possibility of finding specific food items, therefore the risk of shortage of food intake increases because high-nutrition food items could be not found during limited foraging time. In summary, Orthomorpha sp. feeding behaviour can be classified as a time minimising strategy [13,14]. T. carli is more resistant to abiotic conditions, which allows using more time for searching palatable food items without critical risk of shortage of energy input. Therefore, T. carli foraging strategy can be classified as energy maximising. Regarding use of daily time budget and food quality, Orthomorphas' foraging strategy has features of the ‘compensatory feeding’ phenomenon [16,17]. In some cases the compensatory mechanisms lead to the separation of trophic niches [55]. For example, in marine amphipod community there is trophic differentiation based on nutritional quality of food, some species are adopted to high-quality food while others consume low-nutritional food in large amount [18]. One more factor for Orthomorphas' minimisation of searching time may be the foraging cost.
4.3. Single feeding and searching acts duration The mechanisms that regulate switching between searching and feeding activity in millipedes are poorly known. In experimental conditions millipedes usually spent less time searching and more time feeding continuously if they were fed on preferable food items [59]. Nevertheless, animals often started a new search before reaching satiety even if fed on palatable food [60]. Animals coming close to satiety become more selective than hungry ones because most of the required energy has already been received and there is a chance to find preferable food without the risk of a massive energy shortage [59]. This might be a mechanism inducing millipedes to stop feeding and to start searching before reaching satiety. The average time of a single (continuous) feeding act of T. carli was ca. two times shorter than in Orthomorpha sp. (Fig. 3). High-quality food items such as fungal fruit bodies, dead insects, or plant seeds are usually quite small and discretely located in the forest. As a selective eater, T. carli spends relatively little time eating each food unit. In most cases we observed T. carli stopped feeding without any visible external disturbance. Only in a few cases fallen leaves, rain, or other animals lead to breaking of the millipedes’ feeding process. In contrast, litter and algae films on tree trunks seem to be an unlimited food source for millipedes. Orthomorpha sp. can feed for a long time without decreasing the amount of available food. Indeed, Orthomorpha sp. stopped feeding mainly due to various external reasons. In particular, inter-specimen interaction often affected Orthomorpha sp. behaviour because this species tends to form groups of several individuals in a restricted area whereas T. carli meet each other very rarely. Detritivores, and particularly millipedes, with greater body mass often move faster than smaller ones [61]. In absolute values, T. carli was much more mobile than smaller Orthomorpha sp., but if the passed distance is normalized to mean body length of each species, their mobility is comparable (Fig. 4, Table 1). In the dark period when they are most active, Orthomorpha sp. spent little time searching, only ∼20%, compared with ∼47% in T. carli at the same time (Fig. 2). Nevertheless, Orthomorpha sp. passed about the same distance as T. carli, if measured in body lengths (Fig. 4), indicating that their movement was relatively much faster. It reflects a different way of scanning substrate by the two millipede species, which supports trophic differentiation. T. carli examines substrate slowly and carefully, with lots of lateral head movement. Orthomorpha sp. examinations are much faster and rectilinear, 41
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likely in order to find only large aggregations of food, while T. carli looks for discrete small-sized food items. Differentiation in resolution and speed of substrate examination during foraging were assumed as one of the mechanisms for trophic separation among species which forage in the same place, as it has been shown in mixed bird flocks [62,63]. To conclude, we found a strong difference in the use of time budget and trophic behaviour among two coexisting millipede species. Orthomorpha sp. spends the hottest and driest time of the day inactive and feeds in the dark period. This species uses relatively little time for searching food and consumes typically nutritionally poor substrates. The behaviour of Orthomorpha sp. includes traits related to the time minimising strategy, in particular a strongly reduced searching time. This can be related to a smaller body size and a less effective resistance to desiccation. In contrast, the activity of T. carli does not differ in the light and dark periods. This species spends most of the time moving, presumably searching for the palatable food items. These data suggest that T. carli uses an energy maximising strategy, which is facilitated by a large body size, high mobility and a relative independence of abiotic conditions. Thereby, coexisting millipede species from the same trophic guild differ in their foraging strategies, and behavioural differentiation contributes into the trophic niche separation among species in millipede communities.
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Acknowledgements This study was supported by the Presidium of the Russian academy of sciences, Program # 41 “Biodiversity of natural systems”. We are grateful to the administration of Cat Tien National Park for giving the opportunity to collect material, field work was conducted in accordance with Agreement No. 37/HD for the scientific cooperation between the Cat Tien National Park and the Joint Russian-Vietnamese Tropical Center. We thank J. Holden (Harper Adams University, Newport, UK) for improving English of the manuscript. References [1] S.P. Hopkin, H.J. Read, The Biology of Millipedes, Oxford University Press, Oxford, 1992. [2] J.M. Anderson, The enigma of soil animal species diversity, in: J. Vanek (Ed.), Progress in Soil Zoology, Academia, Prague, 1975, pp. 51–58. [3] S.I. Golovatch, R.D. Kime, Millipede (Diplopoda) distributions: a review, Soil Organisms 81 (3) (2009) 565–597. [4] T. Caruso, M. Taormina, M. Migliorini, Relative role of deterministic and stochastic determinants of soil animal community: a spatially explicit analysis of oribatid mites, J. Anim. Ecol. 81 (2012) 214–221. [5] T. Wronski, K. Gilbert, E. Long, B. Micha, R. Quinn, B. Hausdorf, Species richness and meta-community structure of land snails along an altitudinal gradient on Bioko Island, Equatorial Guinea, J. Molluscan Stud. 80 (2014) 161–168. [6] H. Enghoff, Macaronesian millipedes (Diplopoda) with emphasis on endemic species swarms on Madeira and the Canary Islands, Biol. J. Linn. Soc. 46 (1992) 153–161. [7] J.M. Dangerfield, A.E. Milner, R. Matthews, Seasonal activity patterns and behaviour of juliform millipedes in south- eastern Botswana, J. Trop. Ecol. 8 (4) (1992) 451–464. [8] M.D. Greyling, R.J. Van Aarde, S.M. Ferreira, Seasonal changes in habitat preferences of two closely related millipede species, Afr. J. Ecol. 39 (2001) 51–58. [9] I.I. Semenyuk, A.V. Tiunov, S.I. Golovatch, Structure of mandibles in relation to trophic niche differentiation in a tropical millipede community, Int. J. Myriapodol. 6 (2011) 37–49. [10] S.R. Sabo, Niche and habitat relations in subalpine bird communities of the White Mountains of New Hampshire, Ecol. Monogr. 50 (2) (1980) 241–259. [11] Y. Ziv, J.A. Smallwood, Gerbils and heteromyids – interspecific competition and the spatio-temporal niche/activity patterns in small mammals, Ecol. Stud. 141 (2000) 159–176. [12] T.E. Leeuwen, J.S. Rosenfeld, J.G. Richards, Adaptive trade-offs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams, J. Anim. Ecol. 80 (2011) 1012–1023. [13] G.H. Pyke, H.R. Pulliam, E.L. Charnov, Optimal foraging: a selective review of theory and tests, Q. Rev. Biol. 52 (2) (1977) 137–154. [14] T.W. Schoener, Theory of feeding strategies, Annu. Rev. Ecol. Systemat. 2 (1971) 369–404. [15] M.A. Hixon, Energy maximizers and time minimizers: theory and reality, Am. Nat. 119 (4) (1982) 596–599.
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Contents lists available at ScienceDirect
European Journal of Soil Biology journal homepage: www.elsevier.com/locate/ejsobi
Foraging behaviour as a mechanism for trophic niche separation in a millipede community of southern Vietnam
T
Irina I. Semenyuka,b,∗, Alexei V. Tiunova a b
A.N. Severtsov Institute of Ecology and Evolution, Leninsky prospekt 33, Moscow, 119071, Russia Joint Russian-Vietnamese Tropical Center, Street 3 Thang 2, Q10, Ho Chi Minh City, Vietnam
A R T I C LE I N FO
A B S T R A C T
Handling editor: Prof. C.C. Tebbe
Trophic differentiation is one of the mechanisms for species coexisting in the communities of soil arthropods. Even in saprophagous animals having a generalized diet, separation of the trophic niches can be achieved by using different behavioural foraging strategies. We examined the foraging behaviour and time budget use in two millipede species, Thyropygus carli and Orthomorpha sp., which share the same habitat and have similar diet, in a lowland monsoon forest in southern Vietnam. We performed field observations of the millipedes’ behaviour with 1 min resolution time. For both species, observations covered full day and night with ten replications (240 h for each species). Species differed in their time budget use. T. carli spent most time in searching for food and much less time feeding and resting. Orthomorpha sp. usually spent the middle of the day resting and night time eating. The midday rest and relatively short periods of searching in Orthomorpha sp. are most likely caused by avoiding heat and dryness, whereas T. carli has no circadian rhythm, which is facilitated by a large body size, high mobility and a relative independence of abiotic conditions. We conclude that T. carli behaviour is related to an energy maximising foraging strategy, whereas Orthomorpha sp. realises time minimising strategy. Thus, behavioural differentiations and different use of time budget contribute to the trophic niche separation among coexisting millipede species.
Keywords: Diplopoda Foraging strategy Tropical forest Trophic behaviour Circadian rhythm Time budget
1. Introduction Diplopoda are primary decomposers feeding mainly on dead plant material like leaf litter, decaying wood or fallen fruits on the forest floor [1]. Like many other soil saprotrophic animals, millipedes tend to form species-rich communities, especially diverse in tropical forests [2,3]. Although the species coexistence in communities may be achieved by neutral mechanisms [4,5], most studies indicated a presence of differentiation of ecological niches among coexisting species of saprophagous soil animals, such as millipedes. The niche differentiation can be realised by several mechanisms including segregation in space or in time, as well as by using different food sources [6–8]. Although experimental works on food preferences, and studies of the community trophic structure using stable isotope analysis showed pronounced trophic differentiation in the species-rich millipede communities [9], mechanisms leading to the separation of trophic niches in millipedes remain poorly known. In many animal communities trophic differentiation of species is associated with using different foraging strategies [10–12]. The foraging strategy theory supposes animals tend to use a specific ‘optimal
∗
foraging strategy’ for balancing foraging costs and benefits in order to achieve maximum fitness from foraging [13]. According to this theory there are two main strategies of manipulating the balance between foraging cost and benefit, i.e. ‘time minimising’ and ‘energy maximising’ strategies [13,14]. Energy maximising animals are focused on getting the highest energy input while foraging. It can be reflected in behaviour such as spending a lot of effort searching for food with the highest benefit rate. Time minimising animals tend to reduce the foraging time, namely the searching time or feeding time or both, for the sake of saving time for other activities. Schoener [14] supposed time minimisers need some fixed amount of energy input; they try to get it during minimum time neglecting potentially available extra energy sources [15]. Time minimising strategy can be reflected in such behaviour as a drastic reduction of searching time, which means a decrease in the ability to find high-quality food. Consequently, the amount of consumed food should be increased. Closely related to this strategy is the phenomenon called ‘compensatory feeding’, when feeding animals prefer quantity to quality and consume a large amount of nutritionally poor food [16,17]. The decrease in foraging time for the sake of decreasing the risk of a predator's attacks during searching
Corresponding author. A.N. Severtsov institute of Ecology and Evolution, Leninsky prospekt 33, Moscow, 119071, Russia. E-mail address: [email protected] (I.I. Semenyuk).
https://doi.org/10.1016/j.ejsobi.2018.12.001 Received 5 December 2017; Received in revised form 16 May 2018; Accepted 2 December 2018 1164-5563/ © 2018 Elsevier Masson SAS. All rights reserved.
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night humidity changes only slightly but after sunrise it decreases quickly, the driest time being the middle of day (Nam Cat Tien biometeorological station, http://asiaflux.net/index.php?page_id=86 [34]).
might be one of the reasons for compensatory feeding [18]. Animals that use time minimising or energy maximising foraging strategies both get enough energy for performing their life cycles, but they often differ in their diet. Features of foraging strategies in different species can be expressed in trophic behaviour such as a different distribution of time between searching and feeding activities [19]. In soil saprotrophic communities, behavioural aspects of foraging are poorly studied with the possible exception of earthworms and termites [20,21]. Millipedes forage mostly in the dark or at twilight [22–25]. Even cave millipede species living in permanent darkness retain a certain circadian rhythm [26,27]. Recent experiments and observations confirm predominately nocturnal activity of millipedes in general, but also revealed species with a weakly pronounced circadian rhythm [28–30]. It indicates that the mechanisms that regulate millipedes’ circadian rhythms are more complicated than it was assumed before, but they are still unclear. In particular, a few works showed that taxonomically closely related species from the same community can differ in the daily time budget use (dividing time between feeding, resting and searching). It can be viewed as differences in feeding tactics leading to trophic differentiation [7,31]. We therefore supposed that behavioural differences contribute into the trophic niche differentiation in millipede communities. In this work we aimed to quantify behavioural differences, especially differences in use of the time budget, among coexisting millipede species. To this end two millipede species were selected from a species-rich tropical millipede community and their diurnal activity was analysed by direct round-the-clock observations.
2.2. Model species The millipede community in Cat Tien National Park includes at least 40 species and most of them share habitats with each other ([35], I. Semenyuk, unpublished observations). The community is quite diverse in trophic habits; stable isotope analysis showed some trophic differentiation even among generalist feeders [9]. Species also differ in their reaction to seasonal changes in moisture and temperature and have a peak of abundance in different seasons. Two millipede species, Thyropygus carli Attems, 1938 (Spirostreptida) and Orthomorpha sp. (Polydesmida; the species is in the process of taxonomic description), were chosen as a model in this study. Both species are generalist feeders as was confirmed by a wide range of consumed materials found in their faeces. These mainly include debris of leaves, dead wood, fungal mycelium and sporocarps, soil, and fragments of arthropods (data not shown). Two model species have mandibles of similar morphological structure [9]. Nevertheless, the stable isotope analysis detected differences in the species trophic niches. T. carli has higher δ15N values and thus appears to be more ‘carnivorous’ and presumably consumes a more protein-rich diet compared to Orthomorpha sp. [9]. (Orthomorpha sp. in this study corresponds to Orthomorpha sp. 1 in Ref. [9]). Both species are quite abundant and conspicuous, though T. carli is considerably larger than Orthomorpha sp. (Table 1). The abundance of both species slightly decreases in the dry season and increases in the rainy season (unpublished observations). Both species prefer similar microhabitats: forest floor, branches of bushes, surface of tree trunks and logs. Unlike most other species, T. carli and Orthomorpha sp. spend most of their time in open habitats and do not hide under bark or in the leaf litter. These features allow observation of the two species under field conditions.
2. Material and methods 2.1. Study site Material was collected in November–December 2014 and May–August 2015 in the Cat Tien National Park (11º25’ N, 107º25’ E, about 120 m a.s.l.). The territory is covered by monsoon lowland forest with Lagerstroemia calyculata, Tetrameles nudiflora, Afzelia xylocarpa, and Dipterocarpaceae species being dominant in the upper canopy [32]. The forest is rich in epiphytes, lianas, and suspended soils, and forms several canopy layers. Leaf litter on the soil surface is present seasonally for about half of the year. The litter layer is quite diverse and consists of leaves of different species, branches and twigs, bark fragments, and also numerous logs of different size and stages of decay. Fruits and seeds are very abundant seasonally and form heaps of decaying organic matter under particular trees. Fungal sporocarps are abundant seasonally on woody debris and on soil. Tree trunks are typically covered by crustose lichens or algae film, and occasionally by moss. Soil in sampling areas is classified as thin clayey brown tropical soil, or Dystric Skeletic Rhodic Cambisol (Clayic) according to the WRB system [33]. There is a monsoon climate in Cat Tien National Park with strongly marked dry and rainy seasons, a mean annual air temperature of 26 °C, an annual rainfall of 2470 mm. Rain mostly occurs in May-September [34]. In the second part of the rainy season large areas in the forest are flooded for a period of up to several months. Abiotic conditions during the dry season are not suitable for most millipede species; from January to April they have a relatively low abundance. Abundance of millipedes also declines in the second part of the rainy season while the forest is partly flooded. Our observations were performed in the beginning of the rainy season (late spring and summer) and in the beginning of the dry season (autumn), when millipedes are most abundant. In non-raining days of these time periods, a typical air temperature under the canopy varies from about 24 to about 30 °C; soil temperature at the depth of 5 cm varies much less, within 25–27 °C (Fig. 1). The coldest time is just before dawn, around 5 a.m., then after sunrise air temperature increases until the middle of day. Relative humidity varies during the day from 90% to 100%. During the
2.3. Data collecting Individuals of the two species were observed in forest habitats at least 200 m away from forest huts, roads, and other human-derived objects. Millipedes were observed on the soil and leaf litter surface, on logs, tree trunks and bushes up to 2 m in height. For finding specimens, neither digging into leaf litter nor shaking bushes were used. Only adult specimens without any visible damage were selected for observation. Observation started 15 min after finding a specimen to eliminate the possible aberration in its behaviour caused by disturbance during searching. Observation of each specimen lasted as long as possible and ceased either when animal went into a hidden or unapproachable place for more than 5 min or when the rain started. Rain strongly affects millipede behaviour; they start moving chaotically and try to hide from raindrops under leaf litter. During the dark period (typically from 6 p.m. till 5:30 a.m.) a head torch was used. As found in preliminary experiments, individuals of the model millipede species do not react to the artificial light, while some other species immediately stop feeding, turn away and hide. During the observation, neither mosquitoes repellent nor sun protection were used, because in preliminary studies some millipedes demonstrated avoiding behaviour when exposed to the smell of chemicals. During the observation any contact with animals (such as touching or breathing at them) was strongly avoided, observer staying minimum at a half meter distance from the millipede. Diplopoda do not have particularly good vision (if any), so no hiding was needed. Following millipedes during their movements was performed very carefully, avoiding potential vibrations or shaking leaf litter or twigs. We separated four main types of millipede activity, including Searching, Feeding, Resting and Grooming (Table 2). We also observed 37
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Fig. 1. Diurnal rhythms of air temperature under canopy, soil temperature, and air humidity in July 2015. Mean values are given with 1 standard deviation as whiskers, n = 15 (days with rain are excluded). Grey areas mark the dark period of the day. Data from http://asiaflux.net/index.php?page_id=86.
2.4. Data analysis
communicating activity, while millipedes interacted with specimens of the same or another species. This activity includes touching each other by antennae during occasional meetings or prolonged interactions like copulating. Communicating activity happened sporadically and in both species took less than 2% of the time budget. Searching for mate that includes specific behavioural patterns happened very rarely during our observations. These types of activity were not included in further analyses. During field observations the type of activity was recorded every minute. In addition, the total distance passed by a specimen per half an hour was recorded, as a measure of species mobility. Searching for specimens and subsequent observations were performed at different times of day uniformly covering light and dark periods. Thus, for both species, observations covered full day and night with ten replications (240 h for each species).
The 24 h of day were broken into 30 min intervals from 0:00–0:30 to 23:30–0:00. The distribution of time among four main types of activity (in %) was calculated for each 30 min interval and averaged across all replications of the same time interval (n = 10 for each species). The duration of single acts of feeding and searching were calculated as the average duration of unbroken acts started at each hour across all 10 replications. The duration of continuous observation differs among specimens, but most observations lasted for less than 2 h (69% of all observations). We therefore considered all half-hour intervals as independent replications. The mobility of millipede species was estimated in mean body lengths (110 mm and 38.2 mm for T. carli and Orthomorpha sp., respectively) passed per 30 min. Values in the text are given as means ± 1 SD. Mann-Whitney U test was used for comparing means. Millipedes can change diurnal activity with season [7], but we did
Table 1 The main characteristics of the two model species of millipedes. For numeric parameters the mean values are given with ± 1 SD. Mann-Whitney U test was used for comparing means. Thyropygus carli
Eyes (ocelli) presence yes Adult body size (mm) 110.0 ± 7.1 (n = 38) δ15N values, ‰ [9] 4.8 ± 1.9 (n = 10) Time used for different activities, per day (%), n = 10 Searching 46.1 ± 5.2 Feeding 21.6 ± 2.5 Resting 16.7 ± 5.5 Grooming 5.8 ± 4.4 Communicating 0.1 ± 0.1 Unknown (could not be observed) 9.7 ± 5.7 Distance passed per day, cm 12298 ± 1731 Distance passed per day, body lengths 1118 ± 157
38
Orthomorpha sp.
U test, p - values
no 38.2 ± 3.8 (n = 44) 1.5 ± 1.0 (n = 5)
not applicable 0.000 0.002
10.4 ± 3.0 38.5 ± 8.3 38.1 ± 12.7 3.7 ± 3.2 1.7 ± 1.7 7.5 ± 12.8 1888 ± 717 497 ± 189
0.000 0.000 0.001 0.199 0.028 not applicable 0.000 0.000
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Table 2 Description of the four main types of millipedes’ activities. Main type of activity
Activities observed in the field
Description of activity
Searching
Searching
Millipedes walk slowly and examine the surface by antennae, with lateral moving of the head also being typical. Sometimes millipedes make short stops for a closer examination of certain objects.
Feeding
Eating Grazing Drinking
Millipedes stay and eat Millipedes slowly walk while scraping food from the surface (usually tree trunks) Millipedes make stops for drinking drops of water
Resting
Resting Sleeping
Millipedes make stops for several minutes, antennae can be collapsed to the head or not, the reaction to disturbing stimuli is maintained Millipedes make stops for a prolonged time and do not react to stimuli like wind, antennae are collapsed to the head
Grooming
Millipedes stay and clean themselves
Grooming
not find substantial differences in the behaviour of the model species in different seasons. In T. carli the average duration of resting was significantly longer in dry than in the wet season (22.9 and 13.9% of the whole time budget, respectively), while in Orthomorpha sp. searching in the dry season was longer than in the wet season (21.8 and 9.6%, respectively). Other types of activity were not affected. Data collected in different months were therefore bulked in this study. Males usually spend more time in searching for mates, while females spend more time in feeding [30,36]. Sexing animals during observations without disturbing them was not always possible. To account for the possible sex-related difference in the behaviour we therefore analysed a subset of observations that included sexed animals only. The analysis suggested that the behaviour of males and females (observed within the same time periods) was similar, although both in T. carli and Orthomorpha sp. males were on average more mobile, passing ca. 95% and 55% longer distances, respectively, than females of the same species. Sex-related differences in the behaviour were not likely to affect our main results, as the proportion of males and females in the subset of sexed animals was nearly equal: 56.8 and 43.2% observations, respectively, were made on males and on females in Thyropygus and 53.0 and 47.0% in Orthomorpha.
3.2. Mobility T. carli passed on average 25 ± 9 body lengths per half-hour and ca. 1120 body lengths (123 m) per day (Fig. 4). Orthomorpha sp. passed on average 13 ± 11 body lengths per half-hour and ca. 500 body lengths (19 m) per day. In both cases the difference between species was significant (p < 0.001). The mobility of T. carli peaked in the middle of day (more than 50 body lengths per half-hour) but was never less than nine body lengths per half-hour. Orthomorpha sp. was mostly immobile in the afternoon and started moving after sunset. Its mobility peaked around 9 p.m. (up to 39 body lengths per half-hour). 4. Discussion 4.1. Circadian rhythm Most millipede species have a pronounced circadian rhythm and are active mainly at dusk or night [22]. Orthomorpha sp. behaviour was quite typical, i.e. millipedes were more active during the dark period (Fig. 2). Changes in the activity patterns seemingly correlated with abiotic conditions; searching and feeding became much less frequent and mobility decreased with increasing temperature and dryness in the afternoon (Fig. 1). Millipedes loose much more water with increasing temperature [1,36], which can explain the reduction in activity during the hottest part of the day. Orthomorpha sp. has very thin integuments in comparison with many other millipede species in the studied community (I. Semenyuk, unpublished results). Resting in the hottest part of the day in Orthomorpha sp. can be induced by physiological intolerance to dry and hot conditions, but can also appear as the way to save energy when the cost for maintenance of activity is too high because of a high rate of water loss [37]. Such strategy is widespread among desert animals [38]. Many insects use daily torpor for saving energy, especially in non-suitable weather conditions [39]. The role of abiotic conditions in regulating Orthomorpha sp. behaviour is still unclear. Orthomorpha sp. are blind and often choose for the rest open sites such as bushes, leaves, or tree trunk surfaces, rather than soil or other sheltered microsites. Millipedes change resting place if direct sunlight comes (the midday increase in the mobility is likely related to this behaviour; Fig. 4), but usually remain in the open sites where temperature increases significantly during the day. The daily activity patterns of T. carli differed strongly from those of Orthomorpha sp. Proportions of activities in time budget did not correlate with time of the day (Fig. 2). Moreover, the mobility peaked in the middle of the day, which is the hottest and driest time (Fig. 4). This phenomenon is probably related to morphological traits of T. carli that increase its resistance to abiotic conditions. These millipedes have very thick and well calcinated integuments, and are much bigger than Orthomorpha sp. which gives them a more favourable surface-to-volume ratio. In addition T. carli is rufous colour and has a glossy body surface,
3. Results 3.1. Time budget T. carli used 46 ± 5% of the time for searching, 22 ± 3% for feeding, and 17 ± 6% for resting (Table 1, Fig. 2). Proportions of main activities did not change during the day. Orthomorpha sp. spent 10 ± 3% of the time searching, 39 ± 8% feeding, and 38 ± 13% resting. Feeding took maximum time in the dark period (up to 81% at 4:00–4:30 a.m.) and decreased in the light period to only about 5% from 2 p.m. to 4 p.m. Resting took minimum time in the dark period (around 5% from midnight till 5 a.m.) and maximum time in the light period (up to 93% at 3:30–4:00 p.m.). Grooming did not take more than 20.6% of the T. carli time budget, it was more frequent before dawn and before midday. Orthomorpha sp. spent a maximum 17.2% of time grooming; this activity was more frequent at night while no grooming was observed during the midday resting period. The duration of single feeding and searching acts did not change across the day in T. carli (13.9 ± 5.2 min and 16.1 ± 3.7 min, respectively, Fig. 3). In Orthomorpha sp. searching acts were shorter (9.6 ± 4.5 min) and feeding acts much longer (32.4 ± 18.8 min) than in T. carli (p < 0.001 in both cases). The duration of feeding acts in Orthomorpha sp. did not differ between light and dark periods. As a rule, feeding acts were longer during the first half of the day than in the afternoon (Fig. 3). 39
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Fig. 2. The distribution of main types of activity in daily time budget of T. carli (upper panel) and Orthomorpha sp. (lower panel). Standard errors (n = 10) are shown for the proportion of searching to illustrate the degree of variability. Grey areas mark dark period of the day.
properties [44,45]. The major part of the knowledge on the food choice of millipedes is based on laboratory experiments that used a restricted set of leaf litter from different species or of a different quality, while in the field millipedes use a wider range of food items [46,47]. Differentiation in the diet among millipede species can possibly be related to different energetic strategies. This assumption is indirectly supported by the stable isotope analyses which indicated that T. carli has higher trophic level than most other species in the community including Orthomorpha sp. [9]. High δ15N values of T. carli tissues can indicate feeding on a more protein-rich diet [48,49]. According to our observations, Orthomorpha sp. in most cases fed on algae and lichen films on tree trunks or on the soil surface and only rarely on fungal fruit
whereas Orthomorha sp. is black and ridged. Likely, a large light-reflecting and well-protected body is more resistant to overheating and water loss and allows T. carli to maintain activity even at the hottest time of the day. 4.2. Food selection and daily time budget Large saprotrophic invertebrates including millipedes are food-selective. Their food selection is based on physical and chemical properties of food material, such as physical softness and wetness of litter [40], stage of decomposition [41,42], abundance and palatability of microflora [43], presence of secondary compounds or other chemical
Fig. 3. The duration of single feeding and searching acts during the day in two millipede species. Mean values for each hour are shown with 1 SE, n = 10. 40
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Fig. 4. The distance passed by two millipede species per half-hour intervals during the day. Mean values are shown with 1 SE, n = 10.
The amount of energy spending for foraging (mainly for searching food) differs widely among animals. In some cases it is so low that it can be not taken into account (e.g. walking in ants [56]) or appears as the main limiting factor for foraging (e.g. flying in humming birds and in other birds [57,58]). Consumption of low nutritional food makes foraging cost more significant as a limiting factor because it restricts the energy intake that needs to cover foraging efforts and other activities. As Orthomorpha sp. consumes less nutritional food than T. carli, minimising searching time is a possible way to minimise foraging cost.
bodies even if they were abundant. On the contrary, T. carli was often observed eating fungal fruit bodies, tree seeds and fruits; these food items are more N-rich and nutritional than algae and lichens [50,51]. Furthermore, Orthomorpha sp. mostly ignored dead insects or other protein-rich materials, while T. carli usually ate them. Such differences in food preferences of examined millipede species suggest differences in their energy balance and in the choice of optimal foraging strategies. Peculiarities of the food selection by two species might be related to morphological traits of mouthparts and particularly to the difference in the mandible structure. T. carli has more robust teeth and chewing parts of mandibles while Orthomorpha sp. has more dense teeth on pectinate lamellae [9], which can be used for scratching of thin organic films from hard surface as it was shown in cave millipedes [52]. Wolf et al. [53] singled out three main and mutually dependent components influencing animal's trophic behaviour: foraging time, foraging efficiency, and non-foraging energetic. Assuming that an organism requires a fixed amount of energy input, changes in one component should lead to changes in others. Our data suggest that Orthomorpha sp. is limited in the foraging duration by abiotic conditions. On the other hand, this species consumes relatively abundant but nutritionally poor food. This should lead to minimising the searching time and maximising the feeding time in order to obtain the required amount of energy. Indeed, compared to T. carli, Orthomorpha sp. uses much less time for searching than for other activities. Orthomorpha sp. spends most of its active period (night and first half of day) feeding. T. carli spends more time searching and does not have long rests (minimal time compared to other activity types, Fig. 2), thus for obtaining a required amount of energy T. carli can increase its foraging efficiency by consuming high nutritional food as it was indeed observed. Millipedes likely do not have receptors for effectively detecting food items from a distance. Seemingly, they can estimate the palatability of food at a short distance only, when it can be touched by antennae [1,54]. Therefore searching for particular items must take a prolonged time. In the case of Orthomorpha sp., limited foraging time and relatively small body size decrease the possibility of finding specific food items, therefore the risk of shortage of food intake increases because high-nutrition food items could be not found during limited foraging time. In summary, Orthomorpha sp. feeding behaviour can be classified as a time minimising strategy [13,14]. T. carli is more resistant to abiotic conditions, which allows using more time for searching palatable food items without critical risk of shortage of energy input. Therefore, T. carli foraging strategy can be classified as energy maximising. Regarding use of daily time budget and food quality, Orthomorphas' foraging strategy has features of the ‘compensatory feeding’ phenomenon [16,17]. In some cases the compensatory mechanisms lead to the separation of trophic niches [55]. For example, in marine amphipod community there is trophic differentiation based on nutritional quality of food, some species are adopted to high-quality food while others consume low-nutritional food in large amount [18]. One more factor for Orthomorphas' minimisation of searching time may be the foraging cost.
4.3. Single feeding and searching acts duration The mechanisms that regulate switching between searching and feeding activity in millipedes are poorly known. In experimental conditions millipedes usually spent less time searching and more time feeding continuously if they were fed on preferable food items [59]. Nevertheless, animals often started a new search before reaching satiety even if fed on palatable food [60]. Animals coming close to satiety become more selective than hungry ones because most of the required energy has already been received and there is a chance to find preferable food without the risk of a massive energy shortage [59]. This might be a mechanism inducing millipedes to stop feeding and to start searching before reaching satiety. The average time of a single (continuous) feeding act of T. carli was ca. two times shorter than in Orthomorpha sp. (Fig. 3). High-quality food items such as fungal fruit bodies, dead insects, or plant seeds are usually quite small and discretely located in the forest. As a selective eater, T. carli spends relatively little time eating each food unit. In most cases we observed T. carli stopped feeding without any visible external disturbance. Only in a few cases fallen leaves, rain, or other animals lead to breaking of the millipedes’ feeding process. In contrast, litter and algae films on tree trunks seem to be an unlimited food source for millipedes. Orthomorpha sp. can feed for a long time without decreasing the amount of available food. Indeed, Orthomorpha sp. stopped feeding mainly due to various external reasons. In particular, inter-specimen interaction often affected Orthomorpha sp. behaviour because this species tends to form groups of several individuals in a restricted area whereas T. carli meet each other very rarely. Detritivores, and particularly millipedes, with greater body mass often move faster than smaller ones [61]. In absolute values, T. carli was much more mobile than smaller Orthomorpha sp., but if the passed distance is normalized to mean body length of each species, their mobility is comparable (Fig. 4, Table 1). In the dark period when they are most active, Orthomorpha sp. spent little time searching, only ∼20%, compared with ∼47% in T. carli at the same time (Fig. 2). Nevertheless, Orthomorpha sp. passed about the same distance as T. carli, if measured in body lengths (Fig. 4), indicating that their movement was relatively much faster. It reflects a different way of scanning substrate by the two millipede species, which supports trophic differentiation. T. carli examines substrate slowly and carefully, with lots of lateral head movement. Orthomorpha sp. examinations are much faster and rectilinear, 41
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likely in order to find only large aggregations of food, while T. carli looks for discrete small-sized food items. Differentiation in resolution and speed of substrate examination during foraging were assumed as one of the mechanisms for trophic separation among species which forage in the same place, as it has been shown in mixed bird flocks [62,63]. To conclude, we found a strong difference in the use of time budget and trophic behaviour among two coexisting millipede species. Orthomorpha sp. spends the hottest and driest time of the day inactive and feeds in the dark period. This species uses relatively little time for searching food and consumes typically nutritionally poor substrates. The behaviour of Orthomorpha sp. includes traits related to the time minimising strategy, in particular a strongly reduced searching time. This can be related to a smaller body size and a less effective resistance to desiccation. In contrast, the activity of T. carli does not differ in the light and dark periods. This species spends most of the time moving, presumably searching for the palatable food items. These data suggest that T. carli uses an energy maximising strategy, which is facilitated by a large body size, high mobility and a relative independence of abiotic conditions. Thereby, coexisting millipede species from the same trophic guild differ in their foraging strategies, and behavioural differentiation contributes into the trophic niche separation among species in millipede communities.
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