Lepcey  

Entomology Journal  of  Tropical  Asian  

Lepcey  

Diurnal  periodicity  of  three  giant  pill-­‐millipedes  (Sphaerotheriida:  Arthrosphaera)  of  the  Western  Ghats:  an  ex  situ  study  

Cheviri N. Ambarish and Kandikere R. Sridhar*

Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore 574 199, Karnataka, India

*Correspondence:kandikere@gmail.com

Received: 20 October 2014 Accepted: 4 November 2015

Geotags: Western Ghats

[Adyanadka,12°41'N, 75°6'E|

Karike,12°45¢N, 75°38¢E|

Shimoga: 13°35'N, 75°48'E]

Abstract  Diurnal periodicity of three giant pill-‐millipedes

(Arthrosphaera spp.) was carried out in laboratory mesocosms during their active period in monsoon season. Feeding, crawling, guarding, mating, resting and burrowing activities of millipedes (3 adult males and 3 females per mesocosm) were studied up to 24 hours at every three-‐hour interval. The majority of millipedes were feeding throughout the day and crawling was significantly higher in males compared to females (p<0.01). Feeding behaviour was prominent during the day time and most of the females were resting for long duration especially during the night. The average crawling behaviour was significantly higher in males than in females. Guarding was initiated by stridulation which was often seen in A. magna than in A. disticta and A. fumosa, while mating was up to 3% in A. fumosa and A. magna. It is predicted that the females accumulate more energy throughout the day for breeding, while males spend substantial time crawling for the purpose of foraging as well as attracting females for mating. High feeding (43-50%) and crawling (22-31%) activity of pill-‐millipedes in mesocosms facilitates production of organic manure ex situ.

Keywords: Arthrosphaera, behaviour, diurnal periodicity, giant pill-‐millipedes, mesocosm, Sphaerotheriid

ISSN 2012 – 8746 | 04 (1): 1–10 | Published 30 December 2015    OPEN  RESEARCH  ARTICLE  

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Introduction   Arthropod fauna constitute an important biotic component of soil ecosystems and involve in many ecological services especially plant detritus decomposition and humus formation (Plowman, 1990; Stork, 1993; Giller, 1996). Diversity and abundance of soil fauna is very high in the Oriental Zoogeographic regions and their circadian rhythms assume importance in understanding their basic behaviour (Tuf et al., 2006). Assessment of circadian and diurnal activities is one of the essential tasks needed to follow the lifestyles of soil invertebrates like vagility, food selection, capacity of food ingestion and mating phenomenon to enforce restoration and conservation strategies for habitat management. The epigeal activities of most of the myriapod communities vary from day to night and also during twilight conditions (Bano and Krishnamoorthy, 1979; Hopkin and Read, 1992).

Distribution of giant pill-millipedes belonging to the order Sphaerotheriida is restricted to paleotropic (Ethiopian, Oriental and Australian) zoogeographic regions of the southern hemisphere (Wesener et al., 2010). Many genera of pill-millipedes showed microendemism probably due to requirement of precise environmental and soil edaphic conditions. Studies on the behavioural aspects of pill-millipedes are scanty and needs further insights as they are sensitive to narrow changes in edaphic conditions, restricted distribution and highly affected due to human interference. The daily activities of one of the pill-millipedes (Zephronia cf. viridescens) inhabiting deciduous forests of Northern Thailand were recently reported (Wongthamwanich et al., 2012). So far, a few studies are available on the seasonal periodicity on the genus Arthrosphaera of the Indian Subcontinent (Ashwini and Sridhar 2006; Kadamannaya et al., 2009). Recently, Kadamannaya and Sridhar (2009a) studied the in situ diurnal periodicities in three Arthrosphaera spp. during southwest monsoon season in the Western Ghats of India. Many Arthrosphaera spp. inhabiting the Western Ghats were maintained in the laboratory mesocosms for several months to years for experimental purposes especially to assess leaf litter feeding, production of faecal pellets and to follow mating strategies. To compliment the in situ diurnal study (Kadamannaya and Sridhar, 2009a), the present study followed ex situ diurnal activities of three species of Arthrosphaera in laboratory mesocosms.

Methods    Pill-millipedes: Adult pill-millipedes were sampled from the Western Ghat forests during July through August 2012: Arthrosphaera disticta (Shimoga: 13°35'N, 75°48'E), Arthrosphaera fumosa (Karike: 12°45'N, 75°38'E) and Arthrosphaera magna (Adyanadka: 12°41'N, 75°6'E). They were identified based on morphological descriptions using taxonomic keys (Pocock, 1899; Attems, 1936; Kadamannaya and Sridhar, 2009b). They were acclimatized to the mesocosms for about two weeks. Weight, dimensions and speed of locomotion of each acclimatized species in mesocosms were documented. Mesocosm setup: Glass tanks (60×30×30 cm) were used as laboratory mesocosm for assessment of diel activity. Initially, a bed of partially wet soil was prepared followed by spreading wet leaf litter (2-3 cm) and provision was made to drain the excess water to avoid

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water logging. Fallen, dried and partially decomposed leaf litter of Cocos nucifera, Lagerstroemia microcarpa and Terminalia paniculata (250 g each) were mixed (1:1:1) and transferred to each tank. The tops of the tanks were covered with wire mesh and a wet cloth was spread to maintain the humidity in the chamber. To each tank, six pill-millipedes (3 males and 3 females) of A. disticta, A. fumosa and A. magna were released separately. Three replicate mesocosms were maintained for evaluating the diurnal (day), nocturnal (night) and crepuscular (twilight) activities. Observations: Weight and dimensions of pill-millipedes used for the study were recorded. The speed of crawling of each millipede was measured in the mesocosm for 30 min without any external disturbance. Diurnal activities of millipedes were monitored during September 4th-16th, 2012. Activities of millipedes were observed for a 24 hr duration at 3hr intervals. Crawling, feeding, resting, burrowing, guarding and mating behaviours of millipedes were recorded in each mesocosm. During night hours, a compact fluorescent lamp was covered with green plastic sheet to avoid disturbance. Temperature and humidity were recorded at every 3 hr interval. Differences between male and female locomotion were compared by t-test (SigmaPlot, Systat Inc., USA).

Results  

Weight, dimensions and average distance traveling capacity of each species of millipede are given in Table 1. The females showed higher weight as well as dimension compared to males. In mesocosms, movement of millipedes will be restricted in a specific area compared to natural habitats. Males travelled more distance compared to females, distance travelled by A. magna was the longest and was shortest in A. disticta. Some of the major activities of millipedes in 24 hr duration were recorded in mesocosms (Figure 2). They spent most time feeding (~43-50%) and the time spent guarding (2-4%), mating (~3%) and burrowing (~2%) was relatively less. The resting and crawling behaviours were up to ~22-31% and 14-27% of duration, respectively. Significantly higher feeding rate was observed in A. disticta (p<0.001) than A. fumosa and A. magna.

Crawling: The overall crawling behaviour was more or less similar in the three millipede species studied (Figure 1a; Figure 3). There was a peak between 9 pm and 12 am and decreased thereafter (3 am), crawling further increased between 6 am to 9 am but only in A. disticta and A. fumosa. Crawling was independent of day or night conditions. During crawling, they were more attracted to light than dark, they actively moved their antennae, while some individuals were trying to climb the glass surface. Feeding: The overall pattern of feeding behaviour was similar in the three millipede species studied (Figure 1b; Figure 3). The maximum number of individuals was shown feeding between 12 pm and 6 pm followed by another less pronounced peak between 3 am and 6 am. The feeding activity was consistent in A. disticta and A. magna. Most of the millipedes feed on moist litter

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over partially dried litter on the edges of the mesocosm and some were feeding on moist soil particles below the litter strata.

Figure 1. a. Arthrosphaera fumosa (crawling and feeding); b. A. magna (crawling and feeding); c. Guarding in A. magna (arrow); d. Mating in A. fumosa (arrow).

Resting: The overall resting behaviour is consistent in the three millipede species studied (Figure 3). During resting, they were usually partially or fully conglobated. A large number of individuals exhibited resting phase between 12 am and 3 am, which was higher in A. disticta compared to A. fumosa and A. magna. The resting duration required for females was higher compared to males and males spent more time crawling and feeding. Burrowing: Burrowing behaviour was rare but did occur; only males were involved in burrowing (Figure 2). Males of A. fumosa and A. magna showed constant tilling of soil particles and sometimes rest in partially constructed burrow. Guarding and mating: Guarding nature in pill-millipedes is a symptom of pre-mating behaviour for partner selection, which was seen in all millipede species studied (Figure 1c). Guarding behaviour was more often noticed in A. magna compared to A. disticta and A. fumosa. Mating is initiated by guarding behaviour of males whichattracts females. Guarding will not always end up in mating but a few guarding males will be successful. (Figure 1d). Guarding is initiated with stridulation, which leads to selection of suitable female and results in

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probable copulation. Up to 3% mating was seen in A. fumosa and A. magna in mesocosms. However, none of the A. disticta mated in mesocosms although they showed guarding behaviour. Edaphic features: Temperature during the study period in mesocosms ranged from 27.5 to 29.5°C, while the relative humidity was 70 to 85%. During night hours, relatively low temperature and elevated humidity were recorded. Discussion  

Diurnal activity of animals is normally associated with accumulation of energy through feeding for reproduction. The epigeal activities like feeding, crawling, resting, burrowing, guarding and mating are the major diurnal rhythms found in pill-millipedes (Kadamannaya and Sridhar, 2009a; Wongthamwanich et al., 2012). In the current study, feeding, resting and crawling are the most frequent diel activities observed in mesocosms in three Arthrosphaera species. Females consume more during day time compared to males and it was opposite in the night time. Earlier ex situ studies on Arthrosphaera revealed feeding rate was almost constant during 24 hr of duration (Kadamannaya and Sridhar, 2009a). Recent studies on Zephronia cf. viridescens showed high consumption rates in males especially during morning hours and also during dusk (Wongthamwanich et al., 2012). Important factors that affect the food ingestion by millipedes include nitrogen content, phenolics, sugar content and moisture level of leaf litter (Mahsberg, 1997; Ashwini and Sridhar, 2005).

Earlier studies on tropical millipedes revealed maximum activity during night or dusk (Tuf et al., 2006; Kadamannaya and Sridhar, 2009a). In a recent study on Zephronia cf. viridescens, ocelli could detect light and hides underneath the litter during day to avoid the impact of light in the forests of Thailand (Wongthamwanich et al., 2012). The distance migrated per day by Zephronia cf. viridescens in forests ranged from 0.2-3.7 m in males and 0.02-1.12 m in females. Resting during the day may be helpful so animals can decrease their metabolic rate, consumption of oxygen and transpiration rate. In the present study, transpiration rates are expected to be low unlike in forests or plantations. The transpiration rate may not have a strong impact on day activities of Arthrosphaera in mesocosms. Naturally, they have adopted to reduce the risk of transpiration by migrating from sun exposed area to canopy covered litter rich regions (Tuf et al., 2006).

Resting of males and females in mesocosms was almost comparable with activity of A. dalyi and A. fumosa in plantations of the Western Ghats (Kadamannaya and Sridhar, 2009a). Some of the males were involved in burrowing and rested in the burrow itself. This may be one of the protection strategies against predation adopted in field conditions. Burrowing activity of A. fumosa was prominent in in situ (Kadamannaya and Sridhar, 2009a), but it was less in ex situ possibly due to lack of predation risk. Resting in females during monsoon period may be for accumulation of more energy for egg maturation (Wongthamwanich et al., 2012). Males of Arthrosphaera spp. showed high crawling activity compared to females, which is comparable with earlier reports on Zephronia cf. viridescens (Wongthamwanich et al., 2012).

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Figure 2. Diurnal changes in behaviours of Arthrosphaera disticta, A. fumosa and A. magna.

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Figure 3. Diurnal changes in Arthrosphaera disticta, A. fumosa and A. magna: crawling, feeding and resting activities.

Crawling in males may be necessary to attract appropriate females for mating because

females rest more during night compared to day. Crawling behavior is also one of the essential foraging strategies in millipedes to locate high quality litter sources and also for finding a mating partner (Dangerfield et al., 1992). However, such drastic crawling may not be required in

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mesocosms as food is available in their vicinity, as is a female partner. The mean distance travelled by males was high compared to females in Arthrosphaera in mesocosms. Higher mobility rate in males may be due to their smaller size and also to attract a female partner. Movement of Arthrosphaera spp. in mesocosms corroborates with earlier studies on Julus scandinavius (Julidae) (Kheirallah, 1979) and Alloporus uncinatus (Spirostreptidae) (Dangerfield and Telford, 1993). In mesocosms, males encounter females more frequently than in natural habitats, but the percentage of mating is surprisingly low. However, Kadamannaya and Sridhar (2009a) did not see mating behaviour during 24 hr duration in three species of Arthrosphaera in forest locations.

Table 1. Weight, dimensions and distance travelled by pill-millipedes (n=10±SD, range in parenthesis).

Mean distance moved followed by asterisk between males and females are significantly different (P<0.05; t-test).

The current revealed that mating in Arthrosphaera spp. is not dependent on day or

night. Guarding as pre-mating behaviour was seen in the current study and such behaviour was also reported in Zephronia cf. viridescens in Northern Thailand (Wongthamwanich et al., 2012). Guarding can increase the chances of mating by increasing the fitness in males (Parker, 1974). Rather than encountering partners, fitness andinterest of partner is more important in potential mating strategies in pill-millipedes and such observation was supported by copulation behaviour studies in pill-millipedes of the genus Sphaerotherium (Sphaerotheriidae) in Madagascar (Wesener et al., 2011). The valentine alerts of male in Arthrosphaera are communicated to its potential partner through stridulation. The females select the males by uncoiling based on the specificity of signals and its interest in male.

Most of the activities of soil fauna are directly influenced by edaphic factors such as changes in temperature, rainfall, photoperiod and availability of food sources (Koilraj et al., 2000). Activities of pill-millipedes mainly depend upon transpiration rate, temperature and humidity (Tuf et al., 2006). Diurnal activities of millipedes of super order Juliformia in Zimbabwe were found to be high during initial stages of rain and later rapidly diminished during the onset of rain (Dangerfield and Telford, 1991). The current observations were supported by a previous report that found the activities of millipedes is closely correlated to

A. disticta A. fumosa A. magna

male female male female male female

Weight (g) 1.35±0.05 1.62±0.03 17.05±0.12 17.65±0.12 13.69±0.09 14.14±0.19

Length (mm) 25±2 27±1 56±1 57±1 54±1 56±1

Conglobated diameter (mm)

11±1 14±1 34±3 35±3 33±2 34±2

Mean distance moved in 24 hr (m)

1.82±0.14b*

(0.95-1.23)

0.96±0.10a

(0.89-1.09)

2.09±0.43a

(1.60-2.36)

1.99±0.05a

(1.94-2.04)

2.16±0.25b*

(1.80-2.63)

1.32±0.21a

(1.51-2.02)

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their rate of transpiration (Haacker, 1968), while the night time activities of tropical arthropods are highly related to their high transpiration rates in the daytime, which in turn depends on the moisture content of the atmosphere (Cloudsley-Thompson, 1959). Doratogonus bilobatus (Spirostreptidae) showed positive correlation with rate of transpiration and consumption levels of oxygen (Webb and Telford, 1995). In Syngalobolus sp., the activities are shorter during 24 hr of darkness compared 12:12 dark and light period (Koilraj et al., 1999). The effect of temperature is less in mesocosm because such changes were very narrow.

In conclusion, diurnal activities of Arthrosphaera in ex situ was investigated for the first time. The feeding activities were highest in all three species, while crawling behaviour was highest in males compared to females. Males were resting less compared to females during day as well as night, while a few males were resting during dusk. Males spend their time foraging and finding a partner for mating, while females were feeding more possibly to accumulate energy for reproduction. Guarding behaviour was associated with stridulation, it was frequent in A. magna and up to 3% mating was seen in A. fumosa and A. magna. The high amount of of feeding and crawling activity are positive signs of organic matter utilization in mesocosms likely facilitate domestication for large production of organic manure ex situ.  Acknowledgements The authors are grateful to Mangalore University for permission to carryout studies on pill-millipedes in the Department of Biosciences. CNA acknowledges the award of INSPIRE Fellowship, Department of Science and Technology, New Delhi (DST/INSPIRE Fellowship/2011/294: Award # IF110540). KRS acknowledges the award UGC-BSR Faculty Fellowship by the University Grants Commission, New Delhi.

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Ambarish C.N. and Sridhar K.R. (2015) Diurnal periodicity of three giant pill-millipedes (Sphaerotheriida: Arthrosphaera) of the Western Ghats: an ex situ study. Journal of Tropical Asian Entomology 04 (1): 1 – 10