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Effects of spatial heterogeneity on feeding behaviour of Porcellio scaber (Isopoda: Oniscidea)
European Journal of Soil Biology 38 (2002) 53−57 www.elsevier.com/locate/ejsobi
Effects of spatial heterogeneity on feeding behaviour of Porcellio scaber (Isopoda: Oniscidea) Mark Hassall a,*, Joanne M. Tuck a, David W. Smith b, James J. Gilroy b, Richard K. Addison b a
School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK b School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK Received 14 August 2000; accepted 2 May 2001
Abstract Foraging behaviour of Porcellio scaber was observed in laboratory arenas in which the spatial distribution of patches of high quality food (powdered dicotyledonous leaf litter) was varied within a matrix of lower quality food (powdered grass leaf litter). The hypotheses that feeding behaviour of isopods would vary with the degree of clumping of high quality food patches and with the density of conspecifics, were tested. In more clumped treatments, animals spend less time on high quality food and more on a low quality one. At higher densities more time was spent searching. This effect was more pronounced in clumped treatments, but negligible in homogeneous ones. The effects of variation in the spatial heterogeneity of high quality foods on the trade-off between searching costs and intake-rate benefits for saprophages are discussed in the context of predictions from optimal foraging theory for scenarios in which intake-rate maximisation is constrained by nutrient limitation. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Competition; Food quality; Optimal foraging; Porcellio scaber; Resource patchiness; Woodlice
1. Introduction Optimal foraging theory predicts that individuals will evolve foraging strategies that maximise net energy gain, through trade-offs between searching costs and resourceintake benefits. Although questioned [16,17], since MacArthur and Pianka [15] and Emlen [7] first proposed the core of optimality theory, both theoretical and empirical studies have shown that many predators and herbivores behave in accordance with its predictions [8,22,25]. The trade-off between searching costs and intake gains is influenced by numerous variables but prominent amongst them are the spatial distribution of food resources [17,19,24] and
* Corresponding author. Fax: +44-1603-507719. E-mail address: [email protected] (M. Hassall).
intra-specific competition [9]. In addition, for phytophages, the quality of food resource has an important influence on foraging decisions [5]. Grazing ungulates are known to feed selectively when confronted with a patchy forage distribution, tending to select those swards containing higher concentrations of nutrients [24]. Resource quality is now widely recognised as being important for decomposers [4] but relatively little is known about the effects of patchiness in resource quality on saprophages. For the terrestrial isopod Armadillidium vulgare (Latrielle, 1804) in a heterogeneous grassland, a behavioural trade-off between foraging and sheltering results in a demographic trade-off between growth and survivorship rates, the balance of which is determined by the patchy distribution of dicotyledenous plant leaf litter [10]. This species also undergoes scramble competition in the field for limited high quality food resources [12,21] while its growth rates are strongly influenced by interference competition [6].
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 1 ) 0 1 1 2 4 - 4
54
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57 Table 1 Nitrogen and carbon contents of high and low quality foods
Porcellio scaber (Latrielle, 1804) occcurs on many of the same grassland sites as A. vulgare in England [11] where its abundance is also influenced by the distribution of dicotyledonous plant leaf litter [10]. In this paper we test the hypotheses that the foraging behaviour of P. scaber will be influenced by the patchiness of high quality food resources and changes in the density of conspecifics.
Nutrient
% Nitrogen
% Carbon
S. olusatrum leaf litter F. ovina leaf litter t P
2.46 ± 0.06 2.03 ± 0.07 4.89 0.0006
38.98 ± 0.18 42.79 ± 0.52 6.93 < 0.0001
2. Methods
2.3. Effects of density
2.1. Design of the experimental arenas
In the low density treatment 20 individually marked woodlice, of varying size, were placed in each arena (i.e. at a density of 56 m–2). Each arena contained an excess of dicotyledonous plant material in order to reduce exploitation competition for the high quality food resource. In the high density treatment 100 woodlice were placed in each arena (i.e. at a density of 278 m–2), of which 20 were individually marked. Each arena was observed for 30 replicate periods.
High quality food consisted of naturally senesced leaves from the umbellifer Smyrnium olusatrum L. and low quality food of dead Festuca ovina L. agg leaves. Both the foods were dried, powdered with a pestle and mortice and sieved so that all offered fragments were a similar size and all woody tissue was removed from the umbellifer litter. Foods were placed on the bases of feeding arenas consisting of 60 cm × 60 cm × 7 cm high gravel trays lined with 2 cm of plaster of Paris. On each base a 10 × 10 grid of 5.5 cm × 5.5 cm squares was marked out. Foam rubber draft excluder was placed along the top of the rims of the arenas to ensure that the clear perspex lids fitted closely. Carbon and nitrogen content of experimental foods was determined using a CHNO-S Carbo Erba EA 1108 elemental analyser calibrated with acetanalide. Foods were placed directly on the plaster of Paris in three separate spatial arrangements: homogeneous, 50 squares covered with high quality food patches interspersed with 50 squares covered with low quality food in a chequer board pattern; clumped, nine single squares covered with high quality food, eight of them in a square pattern 11 cm from the edge of the arena and 8 cm apart with the ninth square in the centre; and very clumped, a single 11 cm × 11 cm patch covering the four squares in the centre of the arena. Foods were laid out at a constant depth of approximately 1 mm, which was sufficiently shallow to prevent the woodlice from burying themselves in the food. The bases of arenas were saturated with 300 ml of water before the start of each experiment to maintain a constant high relative humidity throughout the experiments. Woodlice were left for 24 h to acclimatise to each arena and observations completed during the following 48 h. All observations were made at approximately 21 ºC in a dark room illuminated with a red light.
2.4. Statistical analyses Data were not normally distributed (Kolmogorov–Smirnov test) so Kruskal–Wallis analyses were used to ascertain the significance of differences between treatments and a series of Mann–Whitney analyses used to test for significant differences between each pair of spatial treatments. Mann–Whitney analyses were also used to test differences between high and low density scenarios.
3. Results 3.1. Nutrient content of foods The nitrogen content of the ground umbellifer leaf litter was significantly higher than that of the powdered grass leaf litter but the grass litter contained significantly more carbon than the dicotyledonous plant litter (Table 1). Results for the homogeneous treatment in which equal quantities of high and low quality food were distributed over equal areas show that the high quality food was very strongly preferred as of the total time spent feeding in this treatment, 85.3 ± 20.6% was spent eating high quality food and 14.7 ± 5.7% eating low quality food.
2.2. Recording of foraging and searching behaviour
3.2. Effects of spatial heterogeneity on foraging behaviour
Foraging movements of the 20 individually marked woodlice were monitored for periods of 10 min. The time spent feeding, as identified by movement of the mouth parts and head, on both good and bad food resources, were recorded using a stop watch. Time spent walking at any speed or direction was recorded as searching time.
At low densities, time spent feeding on high quality food decreased significantly as the distribution of this food became more patchy (Fig. 1a), with a corresponding increase in time spent eating the low quality grass litter in the clumped and very clumped treatments, compared with the homogeneous one (Fig. 1b). Similar effects of increasing
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57
55
Fig. 1. Mean time (± 1 SE) within 10 min observation periods that Porcellio scaber spent feeding on a) high quality and b) low quality food patches differing in spatial heterogeneity of the high quality food resource.
spatial heterogeneity were observed in the high density treatments. 3.3. Effects of density of conspecifics Effects of differences in density on searching behaviour became significantly more pronounced as the degree of spatial heterogeneity increased (Fig. 2). In the homogeneous treatment there was no difference in the amount of time spent searching between the two densities, whereas in both the clumped and very clumped treatments focal individuals at high densities spent significantly more time searching than did those at low densities.
4. Discussion Most consumers forage in spatially complex environments with patchily distributed food resources [18]. This
heterogeneity can affect the ability of consumers to search for and detect these resources [18]. Based on the spatial distribution of resources the consumer must ‘decide’, when to forage in a resource patch, for how long to forage, and when to leave in search of a new resource patch. These decisions will depend on the precise differentials in profitability between patches, the average profitability of the environment, the rate of resource depletion in a patch and the distance between patches [1,17]. Clearly the currency in which profitability is defined will influence the outcome of these decisions. A trade-off exists between the cost of searching for a potentially more profitable food resource and the benefits of feeding in the current patch. To search, the consumer must stop feeding and expend energy in searching with the risk of creating an energy deficit. However, should the consumer find another resource patch of sufficiently high quality, these energetic costs might be outweighed by the significantly higher fitness benefits associated with that resource. For predators, foraging strat
56
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57
Fig. 2. Mean time (± 1 SE) within 10 min observation periods that Porcellio scaber spent searching at densities in arenas differing in the spatial heterogeneity of high quality food patches.
egies are often modelled in relation to optimizing energyintake rates, but for herbivores the need to maximize energetic gains from foraging is often constrained by the requirements for one or more essential nutrients [2,3,14,23], most commonly nitrogen [26]. Decomposers are similarly constrained by food quality limitations [4] which for grassland isopods are also very strongly determined by nitrogen content [13,19]. In this experiment the nitrogen content of umbellifer litter was significantly higher than that of the grass litter. This may partly explain why A. vulgare grew so much faster on S. olusatrum plant litter than on Festuca litter (Tuck, unpublished data), as was found to be the case in comparisons between Festuca and other dicotyledonous species by Rushton and Hassall [20]. These authors also showed that survivorship and reproduction were significantly lower on this grass litter than on that from dicotyledonous plants with higher nitrogen contents. Clearly serious fitness costs can be incurred by isopods as a result of feeding on grass litter alone. The present study shows that over short time intervals P. scaber risked incurring such fitness costs by feeding more on the low nitrogen content foods when the high quality food was more heterogeneously distributed. In the short term (e.g. over a few days), simply replenishing energy expended by eating grass litter with a higher carbon content, might not have any very serious deleterious effects. Over a longer time period (e.g. of weeks) the effects of nitrogen limitation could have a more serious effect on fitness [19]. Experiments are currently in progress to quantify how the above distributions of high quality food affect fitness correlates of isopods over a time scale of 4–6 weeks.
Most optimal foraging models developed for predators show that the density and proximity of conspecifics strongly influence the foraging decisions of individuals as a result of both exploitation and interference competition [23]. Isopods undergo scramble exploitation competition for high quality leaf litter [19] and are also very sensitive to interference competition [6], even when high quality food is available in excess. It might therefore be predicted that foraging behaviour would alter at different densities. The results of analysing behaviour at low and higher densities, both of which are well within the range of densities found in the field for this species [11], show that this is the case. The time individuals spent searching was significantly greater at high densities than at low densities for both of the more heterogeneous treatments but not when the high quality food was homogeneously distributed around the arenas. This might have been because encounters that disturbed the feeding animals were more frequent when they were feeding on a more aggregated high quality resource. Experiments are currently in progress to test this hypothesis. Overall the present results show that spatial heterogeneity of high quality food resources can have a strong influence on the foraging behaviour of arthropod macrodecomposers and that it can strongly affect the outcome of intra-specific interactions that underlie density-dependant regulation of their populations in the field. Furthermore this study illustrates that, when the constraints of nutrient availability are incorporated as determinants of patch profitability at different time scales, the application of optimal foraging theory to saprophages can lead to a significant increase in our understanding of their trophic interactions.
Acknowledgements We are very grateful to Mr. Gareth Lee for culturing the experimental animals, Ms. Laura Sturman for assistance with developing the arenas, Dr. Isabelle Coté for translating the title, abstract and key words into French and the Royal Society for the provision of a travel grant.
References [1] M. Begon, J.L. Harper, C.R. Townsend, Ecology, 3rd ed, Blackwell Sciences Ltd, London, 1996. [2] G.E. Belovsky, Food selection by a generalist herbivore: the moose, Ecology 62 (1988) 1020–1030. [3] K.E. Bjorndal, Flexibility of digestive responses in two generalist herbivores, the tortoises Geochebne carbonavia and Geochebne denticulata, Oecologia 78 (1989) 317–321. [4] G. Cadish, K.E. Giller, Driven by Nature: Plant Litter Quality and Decomposition, CAB International, Wallingford, 1997. [5] M.J. Crawley, Herbivory. The Dynamics of Plant–Animal Interactions, Blackwell Scientific, Oxford, 1983.
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57 [6] J.M. Dangerfield, Competition and the effects of density on terrestrial isopods, Monitore Zool. Ital. 4 (1989) 411–424. [7] J.M. Emlen, The role of time and energy in food preference, Am. Nat. 100 (1966) 611–617. [8] L.A. Goldberg, W.E. Hart, D.B. Wilson, Learning foraging thresholds for lizards: an analysis of a simple learning algorithm, J. Theor. Biol. 197 (1999) 361–369. [9] E.D. Grosholz, Interactions of intraspecific, interspecific and apparent competition with host-pathogen population dynamics, Ecology 73 (1992) 507–514. [10] M. Hassall, Spatial variation in favourability of a grass heath as a habitat for woodlice (Isopoda: Oniscidea), Pedobiologia 40 (1996) 514–528. [11] M. Hassall, J.M. Dangerfield, Interspecific competition and the relative abundance of grassland isopods, Monitore Zool. Ital. 4 (1989) 379–397. [12] M. Hassall, J.M. Dangerfield, Density-dependent processes in the population dynamics of Armadillidium vulgare (Isopoda: Oniscidae), J. Anim. Ecol. 59 (1990) 941–958. [13] M. Hassall, S.P. Rushton, Feeding behaviour of terrestrial isopods in relation to plant defences and microbial decay, in: S.L. Sutton, D. Holdich (Eds.), The Biology of Terrestrial Isopods, Proc. Zool. Soc. Lond. Symp., 53, 1984, pp. 487–505. [14] M. Hassall, R. Riddington, A. Helvin, Foraging behaviour of brent geese, Branta b. bernicla on grasslands: effects of sward length and nitrogen content, Oecologia 127 (2001) 97–104. [15] R.H. MacArthur, E.R. Pianka, On optimal use of a patchy environment, Am. Nat. 100 (1966) 603–609.
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[16] G.J. Pierce, J.G. Ollason, Eight reasons why optimal foraging theory is a complete waste of time, Oikos 49 (1987) 111–118. [17] G.H. Pyke, Optimal foraging theory: A critical review, Annu. Rev. Ecol. Syst. 15 (1984) 523–575. [18] M.E. Ritchie, Scale-dependent foraging and patch choice in fractal environments, Evol. Ecol. 12 (1998) 309–330. [19] S.P. Rushton, M. Hassall, Food and feeding rates of the terrestrial isopod Armadillidium vulgare (Latrielle), Oecologia 57 (1983a) 415–419. [20] S.P. Rushton, M. Hassall, The effects of food quality on the life history parameters of the terrestrial isopod (Armadillidium vulgare (Latreille), Oecologia 57 (1983b) 257–261. [21] S.P. Rushton, M. Hassall, Effects of food quality on isopod population dynamics, Funct. Ecol. 1 (1987) 359–367. [22] R. Seed, R.N. Hughes, Chelal characteristics and foraging behaviour of the blue crab Callinectes sapidus Rathburn, Estuarine Coastal Shelf Sci. 44 (1997) 229–331. [23] D.W. Stephens, J.R. Krebs, Foraging Theory, Princeton University Press, Princeton, 1986. [24] M.F. WallisDeVries, E.A. Laca, M.W. Demment, The importance of scale of patchiness for selectivity in grazing herbivores, Oecologia 121 (1998) 355–363. [25] J.H. Wanink, L. Zwarts, Can food specialisation by individual Oystercatchers Haematopus ostralegus be explained by differences in prey specific handling efficiencies? Ardea 84 (1996) 177–198. [26] T.C.R. White, The Inadequate Environment: Nitrogen and the Abundance of Animals, Springer-Verlag, Berlin, 1993.
Effects of spatial heterogeneity on feeding behaviour of Porcellio scaber (Isopoda: Oniscidea) Mark Hassall a,*, Joanne M. Tuck a, David W. Smith b, James J. Gilroy b, Richard K. Addison b a
School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK b School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK Received 14 August 2000; accepted 2 May 2001
Abstract Foraging behaviour of Porcellio scaber was observed in laboratory arenas in which the spatial distribution of patches of high quality food (powdered dicotyledonous leaf litter) was varied within a matrix of lower quality food (powdered grass leaf litter). The hypotheses that feeding behaviour of isopods would vary with the degree of clumping of high quality food patches and with the density of conspecifics, were tested. In more clumped treatments, animals spend less time on high quality food and more on a low quality one. At higher densities more time was spent searching. This effect was more pronounced in clumped treatments, but negligible in homogeneous ones. The effects of variation in the spatial heterogeneity of high quality foods on the trade-off between searching costs and intake-rate benefits for saprophages are discussed in the context of predictions from optimal foraging theory for scenarios in which intake-rate maximisation is constrained by nutrient limitation. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Competition; Food quality; Optimal foraging; Porcellio scaber; Resource patchiness; Woodlice
1. Introduction Optimal foraging theory predicts that individuals will evolve foraging strategies that maximise net energy gain, through trade-offs between searching costs and resourceintake benefits. Although questioned [16,17], since MacArthur and Pianka [15] and Emlen [7] first proposed the core of optimality theory, both theoretical and empirical studies have shown that many predators and herbivores behave in accordance with its predictions [8,22,25]. The trade-off between searching costs and intake gains is influenced by numerous variables but prominent amongst them are the spatial distribution of food resources [17,19,24] and
* Corresponding author. Fax: +44-1603-507719. E-mail address: [email protected] (M. Hassall).
intra-specific competition [9]. In addition, for phytophages, the quality of food resource has an important influence on foraging decisions [5]. Grazing ungulates are known to feed selectively when confronted with a patchy forage distribution, tending to select those swards containing higher concentrations of nutrients [24]. Resource quality is now widely recognised as being important for decomposers [4] but relatively little is known about the effects of patchiness in resource quality on saprophages. For the terrestrial isopod Armadillidium vulgare (Latrielle, 1804) in a heterogeneous grassland, a behavioural trade-off between foraging and sheltering results in a demographic trade-off between growth and survivorship rates, the balance of which is determined by the patchy distribution of dicotyledenous plant leaf litter [10]. This species also undergoes scramble competition in the field for limited high quality food resources [12,21] while its growth rates are strongly influenced by interference competition [6].
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 1 ) 0 1 1 2 4 - 4
54
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57 Table 1 Nitrogen and carbon contents of high and low quality foods
Porcellio scaber (Latrielle, 1804) occcurs on many of the same grassland sites as A. vulgare in England [11] where its abundance is also influenced by the distribution of dicotyledonous plant leaf litter [10]. In this paper we test the hypotheses that the foraging behaviour of P. scaber will be influenced by the patchiness of high quality food resources and changes in the density of conspecifics.
Nutrient
% Nitrogen
% Carbon
S. olusatrum leaf litter F. ovina leaf litter t P
2.46 ± 0.06 2.03 ± 0.07 4.89 0.0006
38.98 ± 0.18 42.79 ± 0.52 6.93 < 0.0001
2. Methods
2.3. Effects of density
2.1. Design of the experimental arenas
In the low density treatment 20 individually marked woodlice, of varying size, were placed in each arena (i.e. at a density of 56 m–2). Each arena contained an excess of dicotyledonous plant material in order to reduce exploitation competition for the high quality food resource. In the high density treatment 100 woodlice were placed in each arena (i.e. at a density of 278 m–2), of which 20 were individually marked. Each arena was observed for 30 replicate periods.
High quality food consisted of naturally senesced leaves from the umbellifer Smyrnium olusatrum L. and low quality food of dead Festuca ovina L. agg leaves. Both the foods were dried, powdered with a pestle and mortice and sieved so that all offered fragments were a similar size and all woody tissue was removed from the umbellifer litter. Foods were placed on the bases of feeding arenas consisting of 60 cm × 60 cm × 7 cm high gravel trays lined with 2 cm of plaster of Paris. On each base a 10 × 10 grid of 5.5 cm × 5.5 cm squares was marked out. Foam rubber draft excluder was placed along the top of the rims of the arenas to ensure that the clear perspex lids fitted closely. Carbon and nitrogen content of experimental foods was determined using a CHNO-S Carbo Erba EA 1108 elemental analyser calibrated with acetanalide. Foods were placed directly on the plaster of Paris in three separate spatial arrangements: homogeneous, 50 squares covered with high quality food patches interspersed with 50 squares covered with low quality food in a chequer board pattern; clumped, nine single squares covered with high quality food, eight of them in a square pattern 11 cm from the edge of the arena and 8 cm apart with the ninth square in the centre; and very clumped, a single 11 cm × 11 cm patch covering the four squares in the centre of the arena. Foods were laid out at a constant depth of approximately 1 mm, which was sufficiently shallow to prevent the woodlice from burying themselves in the food. The bases of arenas were saturated with 300 ml of water before the start of each experiment to maintain a constant high relative humidity throughout the experiments. Woodlice were left for 24 h to acclimatise to each arena and observations completed during the following 48 h. All observations were made at approximately 21 ºC in a dark room illuminated with a red light.
2.4. Statistical analyses Data were not normally distributed (Kolmogorov–Smirnov test) so Kruskal–Wallis analyses were used to ascertain the significance of differences between treatments and a series of Mann–Whitney analyses used to test for significant differences between each pair of spatial treatments. Mann–Whitney analyses were also used to test differences between high and low density scenarios.
3. Results 3.1. Nutrient content of foods The nitrogen content of the ground umbellifer leaf litter was significantly higher than that of the powdered grass leaf litter but the grass litter contained significantly more carbon than the dicotyledonous plant litter (Table 1). Results for the homogeneous treatment in which equal quantities of high and low quality food were distributed over equal areas show that the high quality food was very strongly preferred as of the total time spent feeding in this treatment, 85.3 ± 20.6% was spent eating high quality food and 14.7 ± 5.7% eating low quality food.
2.2. Recording of foraging and searching behaviour
3.2. Effects of spatial heterogeneity on foraging behaviour
Foraging movements of the 20 individually marked woodlice were monitored for periods of 10 min. The time spent feeding, as identified by movement of the mouth parts and head, on both good and bad food resources, were recorded using a stop watch. Time spent walking at any speed or direction was recorded as searching time.
At low densities, time spent feeding on high quality food decreased significantly as the distribution of this food became more patchy (Fig. 1a), with a corresponding increase in time spent eating the low quality grass litter in the clumped and very clumped treatments, compared with the homogeneous one (Fig. 1b). Similar effects of increasing
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57
55
Fig. 1. Mean time (± 1 SE) within 10 min observation periods that Porcellio scaber spent feeding on a) high quality and b) low quality food patches differing in spatial heterogeneity of the high quality food resource.
spatial heterogeneity were observed in the high density treatments. 3.3. Effects of density of conspecifics Effects of differences in density on searching behaviour became significantly more pronounced as the degree of spatial heterogeneity increased (Fig. 2). In the homogeneous treatment there was no difference in the amount of time spent searching between the two densities, whereas in both the clumped and very clumped treatments focal individuals at high densities spent significantly more time searching than did those at low densities.
4. Discussion Most consumers forage in spatially complex environments with patchily distributed food resources [18]. This
heterogeneity can affect the ability of consumers to search for and detect these resources [18]. Based on the spatial distribution of resources the consumer must ‘decide’, when to forage in a resource patch, for how long to forage, and when to leave in search of a new resource patch. These decisions will depend on the precise differentials in profitability between patches, the average profitability of the environment, the rate of resource depletion in a patch and the distance between patches [1,17]. Clearly the currency in which profitability is defined will influence the outcome of these decisions. A trade-off exists between the cost of searching for a potentially more profitable food resource and the benefits of feeding in the current patch. To search, the consumer must stop feeding and expend energy in searching with the risk of creating an energy deficit. However, should the consumer find another resource patch of sufficiently high quality, these energetic costs might be outweighed by the significantly higher fitness benefits associated with that resource. For predators, foraging strat
56
M. Hassall et al. / Eur. J. Soil Biol. 38 (2002) 53–57
Fig. 2. Mean time (± 1 SE) within 10 min observation periods that Porcellio scaber spent searching at densities in arenas differing in the spatial heterogeneity of high quality food patches.
egies are often modelled in relation to optimizing energyintake rates, but for herbivores the need to maximize energetic gains from foraging is often constrained by the requirements for one or more essential nutrients [2,3,14,23], most commonly nitrogen [26]. Decomposers are similarly constrained by food quality limitations [4] which for grassland isopods are also very strongly determined by nitrogen content [13,19]. In this experiment the nitrogen content of umbellifer litter was significantly higher than that of the grass litter. This may partly explain why A. vulgare grew so much faster on S. olusatrum plant litter than on Festuca litter (Tuck, unpublished data), as was found to be the case in comparisons between Festuca and other dicotyledonous species by Rushton and Hassall [20]. These authors also showed that survivorship and reproduction were significantly lower on this grass litter than on that from dicotyledonous plants with higher nitrogen contents. Clearly serious fitness costs can be incurred by isopods as a result of feeding on grass litter alone. The present study shows that over short time intervals P. scaber risked incurring such fitness costs by feeding more on the low nitrogen content foods when the high quality food was more heterogeneously distributed. In the short term (e.g. over a few days), simply replenishing energy expended by eating grass litter with a higher carbon content, might not have any very serious deleterious effects. Over a longer time period (e.g. of weeks) the effects of nitrogen limitation could have a more serious effect on fitness [19]. Experiments are currently in progress to quantify how the above distributions of high quality food affect fitness correlates of isopods over a time scale of 4–6 weeks.
Most optimal foraging models developed for predators show that the density and proximity of conspecifics strongly influence the foraging decisions of individuals as a result of both exploitation and interference competition [23]. Isopods undergo scramble exploitation competition for high quality leaf litter [19] and are also very sensitive to interference competition [6], even when high quality food is available in excess. It might therefore be predicted that foraging behaviour would alter at different densities. The results of analysing behaviour at low and higher densities, both of which are well within the range of densities found in the field for this species [11], show that this is the case. The time individuals spent searching was significantly greater at high densities than at low densities for both of the more heterogeneous treatments but not when the high quality food was homogeneously distributed around the arenas. This might have been because encounters that disturbed the feeding animals were more frequent when they were feeding on a more aggregated high quality resource. Experiments are currently in progress to test this hypothesis. Overall the present results show that spatial heterogeneity of high quality food resources can have a strong influence on the foraging behaviour of arthropod macrodecomposers and that it can strongly affect the outcome of intra-specific interactions that underlie density-dependant regulation of their populations in the field. Furthermore this study illustrates that, when the constraints of nutrient availability are incorporated as determinants of patch profitability at different time scales, the application of optimal foraging theory to saprophages can lead to a significant increase in our understanding of their trophic interactions.
Acknowledgements We are very grateful to Mr. Gareth Lee for culturing the experimental animals, Ms. Laura Sturman for assistance with developing the arenas, Dr. Isabelle Coté for translating the title, abstract and key words into French and the Royal Society for the provision of a travel grant.
References [1] M. Begon, J.L. Harper, C.R. Townsend, Ecology, 3rd ed, Blackwell Sciences Ltd, London, 1996. [2] G.E. Belovsky, Food selection by a generalist herbivore: the moose, Ecology 62 (1988) 1020–1030. [3] K.E. Bjorndal, Flexibility of digestive responses in two generalist herbivores, the tortoises Geochebne carbonavia and Geochebne denticulata, Oecologia 78 (1989) 317–321. [4] G. Cadish, K.E. Giller, Driven by Nature: Plant Litter Quality and Decomposition, CAB International, Wallingford, 1997. [5] M.J. Crawley, Herbivory. The Dynamics of Plant–Animal Interactions, Blackwell Scientific, Oxford, 1983.
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