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Effect of starvation on phototaxis and geotaxis of collembolans
European Journal of Soil Biology 39 (2003) 9–12 www.elsevier.com/locate/ejsobi
Effect of starvation on phototaxis and geotaxis of collembolans Karsten M. Dromph 1 Department of Ecology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark Received 5 July 2002; accepted 10 September 2002
Abstract The effect of starvation on the behavioural response of three common hemiedaphic collembolan species Hypogastrura assimilis (H. assimilis), Isotoma notabilis (I. notabilis) and Proisotoma minuta (P. minuta) to light was examined. Adults of all the three species were shown to respond negatively to light, as approximately 40% of the H. assimilis, 20% of the P. minuta and 30% of the I. notabilis were recorded in the light area of the arena. However, when adults of H. assimilis were starved, they became increasingly attracted to light with increasing length of the starvation period and after 5 d of starvation, 83% were recorded in the light area. Starvation was not observed to change the behaviour of the other two species. Following these experiments, the effect of starvation on the response to gravity was tested for H. assimilis by placing individuals on a 15° slope. At day 0 of the starvation period, half of the specimens were recorded to move down the slope whilst the other half remained in the middle compartment; none were observed to move upwards. After 1 d of starvation, the proportion of collembolans moving downwards had reduced to 17% and remained low for the following 4 d of starvation. The proportion of collembolans that moved upwards increased significantly during the starvation period from 0% on day 0 to 28% on day 5 of the starvation period. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Collembola; Starvation; Behaviour; Light; Gravity
1. Introduction Epedaphic and hemiedaphic collembolans often have well developed eyes [5,15]. Despite this, hemiedaphic species are generally considered to respond negatively to light, although this response has only been tested for very few species [19,22]. In contrast, migrating Hypogastrura socialis (H. socialis) (Uzel) appears to move in the direction of the sun [13], and preliminary laboratory tests conducted by Lyford [17] on migrating individuals of H. nivicola Fitch indicated that during migration, the collembolans were attracted to a light source. Likewise, Zettel et al. [23] found that Ceratophysella sigillata (Uzel) orientated in relation to a light source, but not necessarily towards it, while they
1 Present address: Department of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK. E-mail address: [email protected] (K.M. Dromph)
showed non-directional movements under diffuse light conditions. Field surveys of the diurnal activity pattern of collembolans have shown that the highest surface activity of collembolans is during the day especially in the afternoon [4,8]. Further several species mainly of the family Hypogastruridae, and also occasionally from Isotomidae, have been observed to perform directional mass migrations on the soil or snow surface. These migrations usually take place during the day orientated after the sun, while the colonies disappear into the soil during the night [12,17]. The inconsistency in the observed behavioural response to light of collembolans is likely caused by environmental factors. Abiotic factors, especially humidity, are known to affect both horizontal and vertical movements of collembolans [1,14,22], while biotic factors such as food supply have been demonstrated to affect their dispersal rate [2,14]. Further, starvation has been shown to have a marked effect on the behaviour of the spider mite Tetranychus urticae Koch, as starved individuals become attracted to light and move to the
© 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 0 0 0 3 - 1
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K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
uppermost parts of the plant as an initial step towards long distance dispersal [16]. The objective of the present study was therefore to test the effect of starvation on the behavioural response of three collembolan species representing two families, Hypogastruridae: H. assimilis (Krausbauer) and Isotomidae: Isotoma notabilis (Schäffer) (I. notabilis) and Proisotoma minuta (P. minuta) (Tullberg) to light and gravity.
2. Materials and methods 2.1. Collembolans The collembolans used in the experiments originated from laboratory stock cultures derived from specimens collected in a clover-grass ley at an experimental farm situated 20 km west of Copenhagen, Denmark. The cultures were maintained at 20 °C in a mix of sphagnum and finely chopped barley straw (v:v 4:1) with the addition of baker’s yeast as a food source. Samples were taken from the cultures at several times and identified under a light microscope according to Gisin [11] and Fjellberg [6,7] in order to confirm the purity of the cultures. For the present experiments, reproductive adults were selected based on size. On day 0 of the experiment, adult collembolans were transferred to 30 ml plastic vials with 5 ml of moist Plaster of Paris with activated charcoal (v:v 5:1), and either supplied with granules of dried baker’s yeast as a food source or starved. 2.2. Response to light In order to test the effect of starvation on the response to light of the three collembolan species, 10 collembolans that had been starved for 0, 1, 2, 3, 4 or 5 d were placed in the middle of a 9 cm Petri-dish lined with moist filter paper and with one half of the lid painted black. The dish was placed inside a 15 cm high black plastic pipe to exclude light from the sides and a light tube from a Volpi Intralux® 5000-1 cold light lamp was placed 15 cm above the dish. After 1 h at 20 °C, the distribution of the collembolans between the dark and lit areas of the dish was recorded. The experiment was repeated 10 times for each starvation time; collembolans kept under similar conditions but fed baker’s yeast were used as a control. Between trials, the dish was cleaned several times with deionised water and ethanol; individual collembolans were only tested once. The data were logit transformed and analysed by fitting generalised linear regression models as defined by Nelder and Wedderburn [18] using the GENMOD procedure in SAS 6.12 [20]. The number of starved and fed collembolans recorded in the light area was compared for each starvation time using a two-tailed t-test for comparing samples with unequal variance [20].
2.3. Response to gravity The effect of starvation on the response to gravity was then tested for H. assimilis starved for 0, 1, 2, 3, 4 or 5 d by using a device consisting of three chambers, each 3 cm in diameter and lined with moist filter paper, connected with 5 cm long plastic tubes (15 mm in diameter) forming a latitude gradient of 15°. Ten collembolans were placed in the middle chamber and after incubation for 1 h in darkness at 20 °C and their distribution was recorded. Any movement of more than 2.5 cm into either of the tubes was considered a directional choice. The experiment was repeated 10 times for each starvation time. Collembolans kept under similar conditions but fed baker’s yeast were used as a control. The device was cleaned in deionised water and ethanol between each trial and individual collembolans were only tested once. The data were logit transformed and analysed by fitting generalised linear regression models using the GENMOD procedure in SAS 6.12 [20]. The mean treatment differences were subsequently compared using the CONTRAST procedure for pair-wise comparison, computing likelihood ratio tests (P < 0.05) [20].
3. Results 3.1. Response to light The effect of the length of starvation period on the response of the three collembolan species to light is shown in Fig. 1. Fed adults of all three tested species showed a significant negative response to light (P < 0.001), as approximately 40% of the fed H. assimilis, 20% of the fed P. minuta and 30% of the fed I. notabilis were recorded in the light area of the arena. For H. assimilis, the length of the starvation period was further found to significantly influence the proportion recorded in the light area (P < 0.001). Starved specimens of this species showed an increasingly positive response to light with increasing starvation period, reaching a maximum of 92% of the individuals in the light area when tested after 3 d of starvation, Fig. 1a. Starvation was, however, not observed to change the behaviour of neither I. notabilis (P = 0.2583) nor P. minuta (P = 0.9291), Fig. 1b,c. A similar constant response to light was shown during the experimental period by individuals kept under similar conditions but fed baker’s yeast (H. assimilis: P = 0.8244, I. notabilis: P = 0.7352, and P. minuta: P = 0.9698). This shows that the change in the behaviour of starved H. assimilis was not caused by factors other than the deprivation of food. 3.2. Response to gravity The distribution of H. assimilis on the latitude gradient as a function of the length of the starvation period is shown in Fig. 2. At the start of the period, half of the collembolans
K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
11
remained low, varying between 7% and 31%, for the following 4 d of starvation. The proportion recorded in the central compartment after 1 h increased to 76% after 1 d of starvation and was reduced again during the following days to 61% after 5 d of starvation. However, differences between days were not significantly different. The proportion of collembolans that moved upwards increased significantly during the starvation period from 0% on day 0 to 28% on day 5 of the starvation period.
4. Discussion
Fig. 1. Effect of starvation on the response of collembolans to light, shown as means of 10 replicates, error bars indicate ± S.E. (a) H. assimilis; (b) I. notabilis; (c) P. minuta. The results of the twotailed t-test for comparing samples with unequal variance are given as: NS P > 0.05; * P < 0.05; ** P < 0.01; *** P < 0.001.
were recorded to have moved downwards while the other half remained in the middle compartment; none were observed to have moved upwards. After 1 d of starvation, the proportion of collembolans moving down had reduced to 17% and
Fig. 2. Effect of starvation on the direction of movement in response to gravity of H. assimilis, shown as means of 10 replicates, error bars indicate ± S.E. Columns headed by different letters are significantly different (P < 0.05) in pair-wise comparison.
Fed specimens of the three hemiedaphic collembolan species tested in the present study responded negatively to light, in agreement with the response shown by Heteromurus nitidus (Templeton) and Pseudosinella dobarti (Gisin) in the only other experimental studies of the response of hemiedaphic collembolans to light [19,22]. When starved specimens of H. assimilis were tested, they showed, however, an increased positive response to light, Fig. 1a, while neither I. notabilis nor P. minuta changed their behaviour as a result of starvation, Fig. 1b,c. The difference in the effect of starvation on the behaviour of the tested species is likely to be an effect of the different microhabitats occupied by the species. Hypogastrura spp. are often found to be associated with decaying organic matter like dung pads, where they are the dominating collembolan species during the initial steps of decomposition [3,21]. The search for non-colonised dung pads is likely to involve long distance movements and therefore may be far more efficient if the collembolans move on the soil surface rather than below it. The starvation induced changes in the behaviour of H. assimilis observed in the present study are likely therefore to be an adaptation to the patchy distribution of their microhabitat. Live collembolans have been caught in the air plankton, indicating that wind dispersal may play an important role in their long distance dispersal [9,10]. The possibility of wind dispersal would be enhanced if dispersing individuals moved upward to exposed points and, during migrations, collembolans have been observed to climb up tree trunks in high numbers [5,12]. The upward movements showed by starved H. assimilis in the present study, Fig. 2, may therefore also be seen as a behavioural response to increase the possibility of long distance wind dispersal. This hypothesis is supported by a similar starvation induced change in the behavioural response to light and gravity observed in the spider mite Tetranychus urticae. The mites respond to a poor host quality or unfavourable abiotic factors by both increased activity levels and positive light response, that has been shown to increase their search efficiency for a new host [14]. The starvation induced changes in the behaviour of H. assimilis are most likely linked to the dispersal behaviour of this species. It is, however, unlikely that this behavioural response is related to the mass migrations observed for Hy-
12
K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
pogastrura spp. Field observations of migrating H. socialis (Uzel), have shown that the migration coincides with a mass release of Picea pollen on which the migrating collembolans were feeding [24]. It is therefore unlikely that the migrations are initiated by a shortage of food, despite migrating individuals of H. nivicola appearing to show the same response to light as starved H. assimilis in the present study [17].
References [1]
T. Bauer, Die Feuchtigkeit als steuernder Faktor für das Kletterverhalten von Collembolen, Pedobiologia 19 (1979) 165–175. [2] G. Bengtsson, K. Hedlund, S. Rundgren, Food- and densitydependant dispersal: evidence from a soil collembolan, Journal of Animal Ecology 63 (1994) 513–520. [3] A.J. Davidson, Mesofaunal responses to cattle dung with particular reference to Collembola, Pedobiologia 19 (1979) 402–407. [4] K. Desender, J. Mertens, M. D’Huster, P. Berbiers, Diel activity patterns of Carabidae (Coleoptera), Staphylinidae (Coleoptera) and Collembola in a heavily grazed pasture, Revue d’écologie et de Biologie du Sol 21 (1984) 347–361. [5] R.A. Farrow, P. Greenslade, A vertical migration of Collembola, The Entomologist 111 (1992) 38–45. [6] A. Fjellberg, Identification keys to Norwegian Collembola, Norsk entomologisk forening, Ås-NLH, 1980. [7] A. Fjellberg, The Collembola of Fennoscandia and Denmark, Part 1: Poduromorpha, Brill, Leiden, 1998. [8] G.K. Frampton, P.J. Van den Brink, S.D. Wratten, Diel activity patterns in an arable collembolan community, Applied Soil Ecology 17 (2001) 63–80. [9] J.A. Freeman, Studies in the distribution of insects by aerial currents. The insect population of the air from ground level to 300 feet, Journal of Animal Ecology 14 (1945) 128–154. [10] J.A. Freeman, Occurrence of Collembola in the air, Proceedings of the Royal Entomological Society of London 27A (1952) 28. [11] H. Gisin, Collembolen Fauna Europas, Museum d’Histoire Naturelle, Genève, 1960.
[12] A. Grinbergs, On mass occurrence and migration of Collembola, with contribution to the ecology of Anurophorus laricis Nic, Opuscula Entomologica 25 (1960) 52–58. [13] S. Hågvar, Long distance, directional migration on snow in a forest collembolan, Hypogastrura socialis (Uzel), Acta Zoologica Fennica 196 (1995) 200–205. [14] M. Hassall, S. Visser, D. Parkinson, Vertical migration of Onychiurus subtenuis (Collembola) in relation to rainfall and microbial activity, Pedobiologia 29 (1986) 175–182. [15] S.P. Hopkin, Biology of the springtails (Insecta: Collembola), Oxford University Press, Oxford, 1997. [16] C.B. Huffaker, M. Van de Vier, J.A. McMurtry, The ecology of tetranychid mites and their natural control, Annual Review of Entomology 14 (1969) 125–174. [17] W.H. Lyford, Overland migration of Collembola (Hypogastrura nivicola Fitch) colonies, American Midland Naturalist 94 (1975) 205–209. [18] J.A. Nelder, R.W.M. Wedderburn, Generalized linear models, Journal of Royal Statistical Society A 135 (1972) 370–384. [19] S. Salmon, J.F. Ponge, Responses to light in a soil-dwelling springtail, European Journal of Soil Biology 34 (1998) 199–201. [20] SAS Institute, SAS/STAT(R) User’s guide, version 6, 4th edition, vols. 1-2, Cary, North Carolina, 1990. [21] J.P. Thome, M. Desière, Évolution de la densité numérique des populations de Collemboles dans les excréments de Bovidés et d’équidés, Revue d’écologie et de Biologie du Sol 12 (1975) 627–641. [22] J. Wilson, The effect of low humidity on the distribution of Heteromurus nitidus (Collembola) in Radford Cave, Devon, Transactions British Cave Research Association 2 (1975) 123–126. [23] J. Zettel, U. Zettel, B. Egger, Jumping technique and climbing behaviour of the collembolan Ceratophysella sigillata (Collembola: Hypogastruridae), European Journal of Entomology 97 (2000) 41–45. [24] R. Zernecke, Streifenförmige Wanderzüge von Hypogastrura socialis (Uzel) (Collembola, Hypogastruidae), Mitteilungen der Münchener Entomologischen Gesellschaft 89 (1999) 95–117.
Effect of starvation on phototaxis and geotaxis of collembolans Karsten M. Dromph 1 Department of Ecology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark Received 5 July 2002; accepted 10 September 2002
Abstract The effect of starvation on the behavioural response of three common hemiedaphic collembolan species Hypogastrura assimilis (H. assimilis), Isotoma notabilis (I. notabilis) and Proisotoma minuta (P. minuta) to light was examined. Adults of all the three species were shown to respond negatively to light, as approximately 40% of the H. assimilis, 20% of the P. minuta and 30% of the I. notabilis were recorded in the light area of the arena. However, when adults of H. assimilis were starved, they became increasingly attracted to light with increasing length of the starvation period and after 5 d of starvation, 83% were recorded in the light area. Starvation was not observed to change the behaviour of the other two species. Following these experiments, the effect of starvation on the response to gravity was tested for H. assimilis by placing individuals on a 15° slope. At day 0 of the starvation period, half of the specimens were recorded to move down the slope whilst the other half remained in the middle compartment; none were observed to move upwards. After 1 d of starvation, the proportion of collembolans moving downwards had reduced to 17% and remained low for the following 4 d of starvation. The proportion of collembolans that moved upwards increased significantly during the starvation period from 0% on day 0 to 28% on day 5 of the starvation period. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Collembola; Starvation; Behaviour; Light; Gravity
1. Introduction Epedaphic and hemiedaphic collembolans often have well developed eyes [5,15]. Despite this, hemiedaphic species are generally considered to respond negatively to light, although this response has only been tested for very few species [19,22]. In contrast, migrating Hypogastrura socialis (H. socialis) (Uzel) appears to move in the direction of the sun [13], and preliminary laboratory tests conducted by Lyford [17] on migrating individuals of H. nivicola Fitch indicated that during migration, the collembolans were attracted to a light source. Likewise, Zettel et al. [23] found that Ceratophysella sigillata (Uzel) orientated in relation to a light source, but not necessarily towards it, while they
1 Present address: Department of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK. E-mail address: [email protected] (K.M. Dromph)
showed non-directional movements under diffuse light conditions. Field surveys of the diurnal activity pattern of collembolans have shown that the highest surface activity of collembolans is during the day especially in the afternoon [4,8]. Further several species mainly of the family Hypogastruridae, and also occasionally from Isotomidae, have been observed to perform directional mass migrations on the soil or snow surface. These migrations usually take place during the day orientated after the sun, while the colonies disappear into the soil during the night [12,17]. The inconsistency in the observed behavioural response to light of collembolans is likely caused by environmental factors. Abiotic factors, especially humidity, are known to affect both horizontal and vertical movements of collembolans [1,14,22], while biotic factors such as food supply have been demonstrated to affect their dispersal rate [2,14]. Further, starvation has been shown to have a marked effect on the behaviour of the spider mite Tetranychus urticae Koch, as starved individuals become attracted to light and move to the
© 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 0 0 0 3 - 1
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K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
uppermost parts of the plant as an initial step towards long distance dispersal [16]. The objective of the present study was therefore to test the effect of starvation on the behavioural response of three collembolan species representing two families, Hypogastruridae: H. assimilis (Krausbauer) and Isotomidae: Isotoma notabilis (Schäffer) (I. notabilis) and Proisotoma minuta (P. minuta) (Tullberg) to light and gravity.
2. Materials and methods 2.1. Collembolans The collembolans used in the experiments originated from laboratory stock cultures derived from specimens collected in a clover-grass ley at an experimental farm situated 20 km west of Copenhagen, Denmark. The cultures were maintained at 20 °C in a mix of sphagnum and finely chopped barley straw (v:v 4:1) with the addition of baker’s yeast as a food source. Samples were taken from the cultures at several times and identified under a light microscope according to Gisin [11] and Fjellberg [6,7] in order to confirm the purity of the cultures. For the present experiments, reproductive adults were selected based on size. On day 0 of the experiment, adult collembolans were transferred to 30 ml plastic vials with 5 ml of moist Plaster of Paris with activated charcoal (v:v 5:1), and either supplied with granules of dried baker’s yeast as a food source or starved. 2.2. Response to light In order to test the effect of starvation on the response to light of the three collembolan species, 10 collembolans that had been starved for 0, 1, 2, 3, 4 or 5 d were placed in the middle of a 9 cm Petri-dish lined with moist filter paper and with one half of the lid painted black. The dish was placed inside a 15 cm high black plastic pipe to exclude light from the sides and a light tube from a Volpi Intralux® 5000-1 cold light lamp was placed 15 cm above the dish. After 1 h at 20 °C, the distribution of the collembolans between the dark and lit areas of the dish was recorded. The experiment was repeated 10 times for each starvation time; collembolans kept under similar conditions but fed baker’s yeast were used as a control. Between trials, the dish was cleaned several times with deionised water and ethanol; individual collembolans were only tested once. The data were logit transformed and analysed by fitting generalised linear regression models as defined by Nelder and Wedderburn [18] using the GENMOD procedure in SAS 6.12 [20]. The number of starved and fed collembolans recorded in the light area was compared for each starvation time using a two-tailed t-test for comparing samples with unequal variance [20].
2.3. Response to gravity The effect of starvation on the response to gravity was then tested for H. assimilis starved for 0, 1, 2, 3, 4 or 5 d by using a device consisting of three chambers, each 3 cm in diameter and lined with moist filter paper, connected with 5 cm long plastic tubes (15 mm in diameter) forming a latitude gradient of 15°. Ten collembolans were placed in the middle chamber and after incubation for 1 h in darkness at 20 °C and their distribution was recorded. Any movement of more than 2.5 cm into either of the tubes was considered a directional choice. The experiment was repeated 10 times for each starvation time. Collembolans kept under similar conditions but fed baker’s yeast were used as a control. The device was cleaned in deionised water and ethanol between each trial and individual collembolans were only tested once. The data were logit transformed and analysed by fitting generalised linear regression models using the GENMOD procedure in SAS 6.12 [20]. The mean treatment differences were subsequently compared using the CONTRAST procedure for pair-wise comparison, computing likelihood ratio tests (P < 0.05) [20].
3. Results 3.1. Response to light The effect of the length of starvation period on the response of the three collembolan species to light is shown in Fig. 1. Fed adults of all three tested species showed a significant negative response to light (P < 0.001), as approximately 40% of the fed H. assimilis, 20% of the fed P. minuta and 30% of the fed I. notabilis were recorded in the light area of the arena. For H. assimilis, the length of the starvation period was further found to significantly influence the proportion recorded in the light area (P < 0.001). Starved specimens of this species showed an increasingly positive response to light with increasing starvation period, reaching a maximum of 92% of the individuals in the light area when tested after 3 d of starvation, Fig. 1a. Starvation was, however, not observed to change the behaviour of neither I. notabilis (P = 0.2583) nor P. minuta (P = 0.9291), Fig. 1b,c. A similar constant response to light was shown during the experimental period by individuals kept under similar conditions but fed baker’s yeast (H. assimilis: P = 0.8244, I. notabilis: P = 0.7352, and P. minuta: P = 0.9698). This shows that the change in the behaviour of starved H. assimilis was not caused by factors other than the deprivation of food. 3.2. Response to gravity The distribution of H. assimilis on the latitude gradient as a function of the length of the starvation period is shown in Fig. 2. At the start of the period, half of the collembolans
K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
11
remained low, varying between 7% and 31%, for the following 4 d of starvation. The proportion recorded in the central compartment after 1 h increased to 76% after 1 d of starvation and was reduced again during the following days to 61% after 5 d of starvation. However, differences between days were not significantly different. The proportion of collembolans that moved upwards increased significantly during the starvation period from 0% on day 0 to 28% on day 5 of the starvation period.
4. Discussion
Fig. 1. Effect of starvation on the response of collembolans to light, shown as means of 10 replicates, error bars indicate ± S.E. (a) H. assimilis; (b) I. notabilis; (c) P. minuta. The results of the twotailed t-test for comparing samples with unequal variance are given as: NS P > 0.05; * P < 0.05; ** P < 0.01; *** P < 0.001.
were recorded to have moved downwards while the other half remained in the middle compartment; none were observed to have moved upwards. After 1 d of starvation, the proportion of collembolans moving down had reduced to 17% and
Fig. 2. Effect of starvation on the direction of movement in response to gravity of H. assimilis, shown as means of 10 replicates, error bars indicate ± S.E. Columns headed by different letters are significantly different (P < 0.05) in pair-wise comparison.
Fed specimens of the three hemiedaphic collembolan species tested in the present study responded negatively to light, in agreement with the response shown by Heteromurus nitidus (Templeton) and Pseudosinella dobarti (Gisin) in the only other experimental studies of the response of hemiedaphic collembolans to light [19,22]. When starved specimens of H. assimilis were tested, they showed, however, an increased positive response to light, Fig. 1a, while neither I. notabilis nor P. minuta changed their behaviour as a result of starvation, Fig. 1b,c. The difference in the effect of starvation on the behaviour of the tested species is likely to be an effect of the different microhabitats occupied by the species. Hypogastrura spp. are often found to be associated with decaying organic matter like dung pads, where they are the dominating collembolan species during the initial steps of decomposition [3,21]. The search for non-colonised dung pads is likely to involve long distance movements and therefore may be far more efficient if the collembolans move on the soil surface rather than below it. The starvation induced changes in the behaviour of H. assimilis observed in the present study are likely therefore to be an adaptation to the patchy distribution of their microhabitat. Live collembolans have been caught in the air plankton, indicating that wind dispersal may play an important role in their long distance dispersal [9,10]. The possibility of wind dispersal would be enhanced if dispersing individuals moved upward to exposed points and, during migrations, collembolans have been observed to climb up tree trunks in high numbers [5,12]. The upward movements showed by starved H. assimilis in the present study, Fig. 2, may therefore also be seen as a behavioural response to increase the possibility of long distance wind dispersal. This hypothesis is supported by a similar starvation induced change in the behavioural response to light and gravity observed in the spider mite Tetranychus urticae. The mites respond to a poor host quality or unfavourable abiotic factors by both increased activity levels and positive light response, that has been shown to increase their search efficiency for a new host [14]. The starvation induced changes in the behaviour of H. assimilis are most likely linked to the dispersal behaviour of this species. It is, however, unlikely that this behavioural response is related to the mass migrations observed for Hy-
12
K.M. Dromph / European Journal of Soil Biology 39 (2003) 9–12
pogastrura spp. Field observations of migrating H. socialis (Uzel), have shown that the migration coincides with a mass release of Picea pollen on which the migrating collembolans were feeding [24]. It is therefore unlikely that the migrations are initiated by a shortage of food, despite migrating individuals of H. nivicola appearing to show the same response to light as starved H. assimilis in the present study [17].
References [1]
T. Bauer, Die Feuchtigkeit als steuernder Faktor für das Kletterverhalten von Collembolen, Pedobiologia 19 (1979) 165–175. [2] G. Bengtsson, K. Hedlund, S. Rundgren, Food- and densitydependant dispersal: evidence from a soil collembolan, Journal of Animal Ecology 63 (1994) 513–520. [3] A.J. Davidson, Mesofaunal responses to cattle dung with particular reference to Collembola, Pedobiologia 19 (1979) 402–407. [4] K. Desender, J. Mertens, M. D’Huster, P. Berbiers, Diel activity patterns of Carabidae (Coleoptera), Staphylinidae (Coleoptera) and Collembola in a heavily grazed pasture, Revue d’écologie et de Biologie du Sol 21 (1984) 347–361. [5] R.A. Farrow, P. Greenslade, A vertical migration of Collembola, The Entomologist 111 (1992) 38–45. [6] A. Fjellberg, Identification keys to Norwegian Collembola, Norsk entomologisk forening, Ås-NLH, 1980. [7] A. Fjellberg, The Collembola of Fennoscandia and Denmark, Part 1: Poduromorpha, Brill, Leiden, 1998. [8] G.K. Frampton, P.J. Van den Brink, S.D. Wratten, Diel activity patterns in an arable collembolan community, Applied Soil Ecology 17 (2001) 63–80. [9] J.A. Freeman, Studies in the distribution of insects by aerial currents. The insect population of the air from ground level to 300 feet, Journal of Animal Ecology 14 (1945) 128–154. [10] J.A. Freeman, Occurrence of Collembola in the air, Proceedings of the Royal Entomological Society of London 27A (1952) 28. [11] H. Gisin, Collembolen Fauna Europas, Museum d’Histoire Naturelle, Genève, 1960.
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