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Arthropods as a prey resource: Patterns of diel, seasonal, and spatial availability
Journal of Arid Environments 73 (2009) 458–462
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Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Arthropods as a prey resource: Patterns of diel, seasonal, and spatial availability M. Vonshak*, T. Dayan, N. Kronfeld-Schor Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 July 2008 Received in revised form 26 November 2008 Accepted 27 November 2008 Available online 4 January 2009
We studied the distribution in time and in space of desert arthropods as a food resource in order to gain insight into the relationship between foraging activity, foraging microhabitat use, and temporal changes in these parameters, and resource availability. We focused on two primarily insectivorous congeneric species of spiny mice, the common spiny mouse (Acomys cahirinus) and the golden spiny mouse (Acomys russatus), that overlap in their ecology, but differ in their diel activity patterns. Arthropod availability was higher during the night, suggesting that in terms of resource availability, night should be the preferred activity time for spiny mice. Different taxa were active during day and night, suggesting that temporal partitioning could indeed be a mechanism of coexistence between the two species. Seasonal variation in arthropod availability is reflected in spiny mouse diets, with more arthropods taken during summer, allowing temporal partitioning to be a viable mechanism of coexistence. In winter when arthropod availability drops, the two species exhibit trade-offs in foraging microhabitat use. Seasonal and spatial variability in arthropod availability between habitats conforms to habitat choice. Thus resource availability appears to be a significant factor structuring this rocky desert rodent community. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Acomys Arthropods availability Food habits Resource base Temporal partitioning
1. Introduction Life on Earth is dependent upon energy; in fact, ecosystems are shaped by the level of energy available (Begon et al., 2006). Energy availability affects species richness and community structure and, at a finer scale, population sizes, their spatial distributions, and the behavior of individuals (e.g., Brown and Maurer, 1989; Damuth, 2007; Evans et al., 2006; Hillebrand, 2004; Steiner and Pfeiffer, 2007; Storch et al., 2005). Individuals require energy for growth, maintenance, and reproduction, so energy acquisition plays a major role in the life history strategies of species and populations. Ecological theory postulates that energy availability will affect population densities (Fretwell and Lucas, 1970; Sutherland, 1983). However, energy acquisition may entail costs that differ in time and in space. In the past two decades a large volume of research has focused on foraging trade-offs, the interplay between the need to acquire energy by foraging and the costs incurred in this life-sustaining activity (e.g., Brown, 1989; Brown and Kotler, 2004; Fedriani and Manzaneda, 2005; Watson et al., 2007). Much of this research has focused on mammals, in particular on desert rodents (e.g., Bouskila, 1995; Jacob and Brown, 2000; Jones and Dayan, 2000; Ziv et al.,1993) as a model system. A surprisingly few studies address resource distribution and its effect on community structure; those in desert
* Corresponding author. Tel.: þ972 3 6409024; fax: þ972 3 6409403. E-mail address: [email protected] (M. Vonshak). 0140-1963/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2008.11.013
settings have focused on the spatial and temporal variations in seed availability (Ben-Natan et al., 2004; Lortie et al., 2000; Mull and MacMahon, 1996; Price and Joyner, 1997; Price and Reichman, 1987). We studied the distribution of desert arthropods as a food resource in time (at the diel and seasonal scale) and in space (at the habitat scale) in order to gain insight into the relationship between foraging activity, foraging microhabitat use, and temporal changes in these parameters, and resource availability. We focused on a model desert ecosystem where the competitive relationships between two rodent species and their response to predation risk have been thoroughly studied in past years. We studied patterns of resource availability at diel, seasonal, and spatial scales in order to investigate the role of resources in shaping a rocky desert rodent community that comprises two largely insectivorous (KronfeldSchor and Dayan, 1999) temporally segregated congeners, the common spiny mouse (Acomys cahirinus) and the golden spiny mouse (Acomys russatus). The two species overlap significantly in their ecology but differ diametrically in their activity patterns: the common spiny mouse is nocturnal while the golden spiny mouse is diurnally active (Kronfeld-Schor and Dayan, 2008; Shkolnik, 1971). Upon removal of the common spiny mouse from the shared habitat, the golden spiny mouse exhibits also some nocturnal activity, suggesting that the common spiny mouse competitively displaces the golden spiny mouse into diurnal activity (Gutman and Dayan, 2005; Shkolnik, 1971). Food resources may vary at the diel and seasonal scale, and their abundance may also vary between habitats. The extreme climatic
M. Vonshak et al. / Journal of Arid Environments 73 (2009) 458–462
conditions in hot deserts require special adaptations of the inhabitants, especially from arthropods (reviewed by CloudsleyThompson, 2001). The reaction of most desert beetles is largely behavioral, avoiding the harsh conditions by hiding or borrowing during the day (Cloudsley-Thompson, 2001). Holm and Edney found that tenebrionid beetles in the Namib Desert differ in season and daily cycle activity, and in addition winter and summer population were substantially different from each other (Holm and Edney, 1973). Krasnov and Shenbrot (1997) found that most tenebrionid species studied in the Negev Desert (Israel) changed their microhabitat preferences seasonally. In the past decade we have been studying temporal activity patterns of spiny mice, as well as foraging behavior and foraging microhabitat choice at the diel, lunar, and seasonal scale, factoring in varying levels of perceived risk of predation (reviewed by Kronfeld-Schor and Dayan, 2003, 2008). We found that the two spiny mouse species overlap in food habits, with a preference for arthropods, taken in extremely high quantities by both species in summer (Kronfeld-Schor and Dayan, 1999). In winter spiny mice showed trade-offs in foraging efficiency that may enable their coexistence (Jones et al., 2001). In summer, however, a shift in habitat preferences of both species increases ecological overlap between them (Jones et al., 2001). This shift may result from predator activity (Jones et al., 2001), but may also reflect a shift in the spatial distribution of available resources. This microhabitat use overlap may be the driver for temporal partitioning (Gutman and Dayan, 2005). During summer both species turn primarily insectivorous. Because arthropod prey of A. cahirinus and A. russatus are likely to show diel patterns in availability, temporal partitioning among species of spiny mice could well promote resource partitioning and coexistence (Jones et al., 2001; Kronfeld-Schor and Dayan, 1999). Previous research has revealed diel, seasonal, and spatial shifts in foraging microhabitat use by spiny mice. These shifts have been ascribed to interspecific competition and to predation risks in different habitats (Jones et al., 2001; Mandelik et al., 2003). Temporal partitioning as a mechanism of coexistence assumes different resource availability during the day and night (KronfeldSchor and Dayan, 2003; Schoener, 1974), but this hypothesis has yet to be tested. Furthermore, spatial shifts in foraging patterns may result not only from predation and competition but also the spatial distribution of resources. Data of spiny mice prey species are scarce, since the mice probably digest insects’ cuticle, and even stomach pumping revealed only a small number of identifiable elements (KronfeldSchor and Dayan, 1999), which cannot be taken as representative. We studied the arthropod fauna at En Gedi, near the Dead Sea, in order to gain insight into the possible effects of varying resource levels in time and in space. We used pitfall traps in order to learn about the prey available for spiny mice; specifically, we asked: Are different arthropod taxa available during the day and during the night? Such differences would imply that temporal partitioning is a viable mechanism for coexistence between spiny mouse species. Do seasonal differences in spiny mouse diets reflect differences in resource availability? We found seasonal shifts in the arthropod component in spiny mouse diets (Kronfeld-Schor and Dayan, 1999) and ask whether they reflect resource availability in different seasons and during different activity times. Are there seasonal differences in arthropod availability between the different habitats? Seasonal differences in resource availability in different habitats could affect foraging habitat use of spiny mice during the day and night.
459
When resources are limiting, they can be expected to impact not only population dynamics but also animal foraging behavior and microhabitat use and thus also affect ecological overlap of competing species and their risk of predation. Consequently, resource availability can impact community level interactions both directly, by regulating population growth, and indirectly, by affecting diel and seasonal patterns of niche overlap. Our study was designed to investigate the effect of diel and seasonal resource availability on the community structure of rocky desert rodents. 2. Materials and methods 2.1. Study site The study was conducted at the En Gedi Nature Reserve, in the Judean Desert, near the Dead Sea (31280 N, 35 230 E, 300 m below sea level), between September 2002 and August 2003. Three habitats were chosen in which the foraging behavior of spiny mice was previously studied: (1) boulder habitat; (2) open habitat, where traps were set 5 m away from a rock terrace; (3) wadi bed – a nearby dry stream bed, with both open and boulder habitats. 2.2. Faunal sampling We sampled arthropods using pitfall traps. A caveat: our study focuses on active prey availability (see Hingrat et al., 2007) rather than on prey actually chosen. Pitfall traps are biased towards ground-dwelling active arthropods (Southwood, 1978), those we assume are most likely to be preyed by spiny mice. Inactive arthropods at En Gedi usually seek refuge under stones and in tight crevices, where they are sheltered from predators, so they are less likely to be preyed. Other studies have shown that active prey are usually more susceptible to predation than inactive individuals (Lima, 1998). In each habitat 35 pitfall traps were dug into the ground, at 5 m intervals. Pitfall traps consisted of plastic cups (10 cm in diameter, 10.5 cm deep), a plastic funnel, and tissue paper (in order to increase available surfaces and thus reduce the chance of predation). The traps were opened every month for three days and nights. They were checked twice a day – at first and last light. All organisms were identified to the lowest taxonomic unit possible, measured for body length, and usually released on site. Individuals which could not be identified in the field were taken to the Tel-Aviv University Zoological Museum for further identification. We used morphospecies for groups for which there are no taxonomists in Israel. We analyzed the cumulative data of number of individuals and the individuals’ length for each season (as an estimate of biomass). Because the wadi habitat was not checked during autumn and the first month of winter, we performed the analysis twice: once for the open and the boulder habitats without the wadi, for the entire year, and once for all three habitats but without autumn and the fist winter sampling. 2.3. Statistical analysis The length and number of individuals’ data were square root transformed and analyzed by three-way ANOVA (analysis of covariance), followed by Tukey multiple comparisons (using Statistica 7.1, StatSoft Inc., Oklahoma, USA), with season, habitat and time of activity as factors. Again, we performed the analysis twice: once for the open and the boulder habitats, for the whole year, and once for all the three habitats, without the autumn and the first winter sampling.
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3. Results 3.1. Taxon level analyses 1916 individual arthropods, of 5 mm and over, were sampled in the three habitats. Most taxa were nocturnal (18); only four were diurnal (Fig. 1). The number of active arthropods was greater at night. Nearly 80% of identified taxa were either diurnal or nocturnal (Fig. 1). The few taxa that did not exhibit a pattern are: a) ones that
we could not identify to a low taxonomic level (a part of the Zygenthoma, Bombicidae – larvae, and Grilopsis?). It is quite possible that at the species level these taxa do have a typical activity pattern; b) Acrididae – this is not a suitable method for catching them, and their trapping was much lower than their visual activity in the field; and c) Diplopoda, whose sample size is small. The workers of Messor ebeninus also did not have a fixed activity pattern; it is known that this species’ activity is set by surface temperature rather than daylight (Avidov, 1968).
Family Formicidae
Order Thysanura Lepismatidae - a
56
Lepismatidae - b
40
Machilidae
Cataglyphis lividus
15
6
2
6
0
43
305
Camponotus sp.
1
Others
312
Aphenogaster sp.
3
81
18
126
Messor ebeninus
169
Order Orthoptera Acrididae
11
3
Order Isopoda 23
Eremogryllodes sp.
0 20
Sowbug Grilopsis?
3
10
Others
Pillbugs
6
70
Adesmia abbreviata
Order Araneae
6
2
Lycosidae
3
20
Trachyderma philistina
0
9
2
18
53
Gnaphosidae
Salticidae
28
Others
15
0
Order Coleoptera Mesostena punctata
13
3
41
Others
8
74
Order Lepidoptera
21
Other arthropods Scutigeridae
Moth larva a
64
3
Others 0%
6
7 20%
4 40%
0
15
5 Scolopendridae
Moth larva b
0
60%
80%
21
Galeodidae
65
Scorpiones
20
Diplopoda 100%
3
0%
1 0
5 20%
3 40%
60%
80%
100%
Fig. 1. Activity patterns of the major arthropod taxa according to trapping times at En Gedi. The black and white bars represent the percentage of night and day activity, respectively, while the numbers inside the bars represent the number of individuals collected using pitfall traps. Taxa are the lowest taxonomic unit possible of the abundant species (more than 5% of the entire order/family).
Within most taxonomic groups no significant difference in diel activity pattern was found between habitats or seasons. 3.2. Patterns of arthropod availability The number of individuals and cumulative length showed similar trends, so we present results only for the former. Significant differences were found in number of individuals between seasons and time of activity, when only the boulder and open habitat were studied (three-way ANOVA, season: F ¼ 49.47, df ¼ 3, p < 0.0001; time: F ¼ 7.83, df ¼ 1, p < 0.0001). Significant differences were found between seasons, time of activity and habitat when data for three habitats were analyzed (season: F ¼ 80.05, df ¼ 2, p < 0.0001; habitat: F ¼ 10.08, df ¼ 2, p < 0.0001; time: F ¼ 23.448, df ¼ 1, p < 0.0001). There was a significant seasonal difference in number of individuals, lowest in winter (three-way ANOVA, F ¼ 49.47, df ¼ 3, p < 0.0001. Fig. 2). In spring the numbers increased and peaked in summer. Species richness was high in spring and summer and lower in autumn and winter. In winter and spring the number of individuals was lowest at the open habitat, but in summer and autumn it was greatest (Fig. 3). Significant differences were found between day and night when only the boulder and open habitats were studied (Tukey, F ¼ 1.46, df ¼ 1, p < 0.01. Fig. 3), and significant only in the wadi when the three habitats were studied (Tukey, F ¼ 1.46, df ¼ 1, p < 0.0001). 4. Discussion Patterns of resource availability contribute to our understanding of the structure of a rocky desert rodent community. More arthropods were trapped during the night, the activity time of common spiny mice, from which golden spiny mice are excluded. Activity patterns of mammals may be determined by extrinsic factors (Halle, 1995; Meyer et al., 2005), selective forces and phylogenetic constraints (Daan, 1981; Kronfeld-Schor and Dayan, 2003; Roll et al., 2006); nocturnality is probably the ancestral state in mammals and in rodents. Notwithstanding, it appears that night offers more feeding opportunities than day in this ecosystem. By shifting activity from night to day, golden spiny mice encounter a different resource spectrum and must take different arthropod prey. Thus, temporal partitioning at the diel scale is a viable mechanism of coexistence reducing overlap between these competitors.
No. of individuals 70
Species richness
900 800 50 700 600 500
30
400 300 10
Species richness
Accumulated no. of individuals
1000
200 100 0
-10 Winter
Spring
Summer
Autumn
Season Fig. 2. Distribution of number of individuals and species richness of arthropods sampled by pitfall traps in the research site at En Gedi.
Accumulated no. of individuals
M. Vonshak et al. / Journal of Arid Environments 73 (2009) 458–462
461
400 350 300 250 200 150 100 50 0
Open Bolder Wadi Open Bolder Wadi Open Bolder Wadi Open Bolder
Winter
Spring
Summer
Autumn
Fig. 3. Distribution of number of individuals of diurnal (white bars) and nocturnal (black bars) arthropods between seasons and habitats.
Seasonal variation in arthropod abundance, high in summer and low in winter, is reflected in spiny mouse diets; therefore, in winter both species overlap in a largely vegetarian diet (Kronfeld-Schor and Dayan, 1999). However, in winter the two species differ in their foraging behavior, thus reducing niche overlap between the species (Jones et al., 2001). Diel, lunar, and seasonal patterns in predation risk appear to affect foraging activity patterns and foraging microhabitat use, to minimize risk (Eilam et al., 1999; Jones et al., 2001; Mandelik et al., 2003). Here we asked how resource availability relates to these patterns. Both species prefer to forage in the boulder habitat where they are protected from avian and mammalian predators, and during the day, from the sun’s radiation (Gutman and Dayan, 2005; Jones et al., 2001; Kronfeld-Schor et al., 2001; Mandelik et al., 2003; Shargal et al., 2000). However, it appears that foraging in the boulder habitat is also advantageous in terms of resource availability: during three of four seasons, arthropods are more abundant in this habitat than in the open habitat. In summer, arthropods become more abundant in the open habitat. During summer spiny mice shift their activity to more open habitats. We previously ascribed this shift in foraging behavior to saw scaled vipers (Echis coloratus), seasonally active spiny mouse predators (Jones et al., 2001; Weissenberg et al., 1997). This shift also conforms to resource availability, which may be an additional force affecting foraging microhabitat use. Without experimentation (e.g., Price and Waser, 1985; Tilman, 1982) we are unable to prove the precise role of resource levels in producing these activity patterns, but we can certainly note the perceived relationship. The shift in summer microhabitat use increases predation risk from avian and mammalian predators (Jones et al., 2001), thus affecting also community level interspecific interactions. However, it should be noted that even with this shift in summer, spiny mice still forage significantly more in the protected boulder habitat (Jones et al., 2001). Thus it appears that predation risk by avian and mammalian predators, and thermal load from the sun during the day still exert stronger pressure than do predation risk by snakes and patterns of resource availability. Of numerous studies of interspecific interactions, few address patterns in resource availability and their possible role in affecting community structure (e.g., Kneitel and Chase, 2004; Kotler and Brown, 1990; Price and Joyner, 1997). Resource availability is a significant variable in ecological communities, both as a lead force in population dynamics and indirectly through diel, seasonal, and spatial variations in habitat use. Here we find a strong relationship between patterns of resource availability and community structure:
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preferred activity times are those at which resource availability is greatest, foraging microhabitat choice conforms to patterns of resource availability at the seasonal scale and diel patterns of prey activity can support temporal partitioning as a mechanism of coexistence. When arthropod availability declines during winter, their significance in spiny mouse diets drops and an alternative mechanism of coexistence comes into action (Jones et al., 2001). These patterns and choices impact both competitive and predatory interspecific interactions. Thus resource availability appears to be a significant factor structuring this rocky desert rodent community. Acknowledgments We sincerely thank Enav Vidan and Ariella Gotlieb for all the hard work in the field, Arieh Landsman for fighting the world’s bureaucracy, the En Gedi Field School of the Society for the Protection of Nature in Israel for the residence, and the Israel Nature and Parks Authority for their help. We thank Mary V. Price for her useful remarks to an early version of the manuscript. Vladimir Chikatunov, Vassiliy Kravchenko, Tova Feller, Amnon Freidberg, Leybele Friedman, Alex Shlagman and Dany Simon of the Tel Aviv University Zoological Museum helped with arthropod identifications and David Wool provided statistical advice. This research was supported by the Israel Science Foundation (grant No. 720/01-4). References Avidov, Z., 1968. The Harvester Ant in Israel. Sifriath Hassadeh, Tel Aviv, Israel (in Hebrew). Begon, M., Townsend, C.R., Taper, J.L., 2006. Ecology: from Individuals to Ecosystems. Blackwell Publishing, Maldan, MA. Ben-Natan, G., Abramsky, Z., Kotler, B.P., Brown, J.S., 2004. Seeds redistribution in sand dunes: a basis for coexistence of two rodent species. Oikos 105, 325–335. Bouskila, A., 1995. Interactions between predation risk and competition – a fieldstudy of kangaroo rats and snakes. Ecology 76, 165–178. Brown, J.S., Kotler, B.P., 2004. Hazardous duty pay and the foraging cost of predation. Ecology Letters 7, 999–1014. Brown, J.H., Maurer, B.A., 1989. Macroecology – the division of food and space among species on continents. Science 243, 1145–1150. Brown, J.S., 1989. Desert rodent community structure – a test of 4 mechanisms of coexistence. Ecological Monographs 59, 1–20. Cloudsley-Thompson, J.L., 2001. Thermal and water relations of desert beetles. Naturwissenschaften 88, 447–460. Daan, S., 1981. Adaptive daily strategies in behavior. In: Aschoff, J. (Ed.), Handbook of Behavioral Neurobiology. Biological Rhythms, vol. 4. Plenum, New York, pp. 275–298. Damuth, J., 2007. A macroevolutionary explanation for energy equivalence in the scaling of body size and population density. American Naturalist 169, 621–631. Eilam, D., Dayan, T., Ben-Eliyahu, S., Schulman, I., Shefer, G., Hendrie, C.A., 1999. Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Animal Behaviour 58, 1085–1093. Evans, K.L., Jackson, S.F., Greenwood, J.J.D., Gaston, K.J., 2006. Species traits and the form of individual species–energy relationships. Proceedings of the Royal Society B – Biological Sciences 273, 1779–1787. Fedriani, J.M., Manzaneda, A.J., 2005. Pre- and post-dispersal seed predation by rodents: balance of food and safety. Behavioral Ecology 16, 1018–1024. Fretwell, S.D., Lucas Jr., H.L., 1970. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheoretica XIX, 16–36. Gutman, R., Dayan, T., 2005. Temporal partitioning: an experiment with two species of spiny mice. Ecology 86, 164–173. Halle, S., 1995. Effect of extrinsic factors on activity of root voles, Microtus oeconomus. Journal of Mammalogy 76, 88–99. Hillebrand, H., 2004. On the generality of the latitudinal diversity gradient. American Naturalist 163, 192–211. Hingrat, Y., Ysnel, F., Saint Jalme, M., Le Cuziat, J., Be´ranger, P.M., Lacroix, F., 2007. Assessing habitat and resources availability for an endangered desert bird
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Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Arthropods as a prey resource: Patterns of diel, seasonal, and spatial availability M. Vonshak*, T. Dayan, N. Kronfeld-Schor Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 July 2008 Received in revised form 26 November 2008 Accepted 27 November 2008 Available online 4 January 2009
We studied the distribution in time and in space of desert arthropods as a food resource in order to gain insight into the relationship between foraging activity, foraging microhabitat use, and temporal changes in these parameters, and resource availability. We focused on two primarily insectivorous congeneric species of spiny mice, the common spiny mouse (Acomys cahirinus) and the golden spiny mouse (Acomys russatus), that overlap in their ecology, but differ in their diel activity patterns. Arthropod availability was higher during the night, suggesting that in terms of resource availability, night should be the preferred activity time for spiny mice. Different taxa were active during day and night, suggesting that temporal partitioning could indeed be a mechanism of coexistence between the two species. Seasonal variation in arthropod availability is reflected in spiny mouse diets, with more arthropods taken during summer, allowing temporal partitioning to be a viable mechanism of coexistence. In winter when arthropod availability drops, the two species exhibit trade-offs in foraging microhabitat use. Seasonal and spatial variability in arthropod availability between habitats conforms to habitat choice. Thus resource availability appears to be a significant factor structuring this rocky desert rodent community. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Acomys Arthropods availability Food habits Resource base Temporal partitioning
1. Introduction Life on Earth is dependent upon energy; in fact, ecosystems are shaped by the level of energy available (Begon et al., 2006). Energy availability affects species richness and community structure and, at a finer scale, population sizes, their spatial distributions, and the behavior of individuals (e.g., Brown and Maurer, 1989; Damuth, 2007; Evans et al., 2006; Hillebrand, 2004; Steiner and Pfeiffer, 2007; Storch et al., 2005). Individuals require energy for growth, maintenance, and reproduction, so energy acquisition plays a major role in the life history strategies of species and populations. Ecological theory postulates that energy availability will affect population densities (Fretwell and Lucas, 1970; Sutherland, 1983). However, energy acquisition may entail costs that differ in time and in space. In the past two decades a large volume of research has focused on foraging trade-offs, the interplay between the need to acquire energy by foraging and the costs incurred in this life-sustaining activity (e.g., Brown, 1989; Brown and Kotler, 2004; Fedriani and Manzaneda, 2005; Watson et al., 2007). Much of this research has focused on mammals, in particular on desert rodents (e.g., Bouskila, 1995; Jacob and Brown, 2000; Jones and Dayan, 2000; Ziv et al.,1993) as a model system. A surprisingly few studies address resource distribution and its effect on community structure; those in desert
* Corresponding author. Tel.: þ972 3 6409024; fax: þ972 3 6409403. E-mail address: [email protected] (M. Vonshak). 0140-1963/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2008.11.013
settings have focused on the spatial and temporal variations in seed availability (Ben-Natan et al., 2004; Lortie et al., 2000; Mull and MacMahon, 1996; Price and Joyner, 1997; Price and Reichman, 1987). We studied the distribution of desert arthropods as a food resource in time (at the diel and seasonal scale) and in space (at the habitat scale) in order to gain insight into the relationship between foraging activity, foraging microhabitat use, and temporal changes in these parameters, and resource availability. We focused on a model desert ecosystem where the competitive relationships between two rodent species and their response to predation risk have been thoroughly studied in past years. We studied patterns of resource availability at diel, seasonal, and spatial scales in order to investigate the role of resources in shaping a rocky desert rodent community that comprises two largely insectivorous (KronfeldSchor and Dayan, 1999) temporally segregated congeners, the common spiny mouse (Acomys cahirinus) and the golden spiny mouse (Acomys russatus). The two species overlap significantly in their ecology but differ diametrically in their activity patterns: the common spiny mouse is nocturnal while the golden spiny mouse is diurnally active (Kronfeld-Schor and Dayan, 2008; Shkolnik, 1971). Upon removal of the common spiny mouse from the shared habitat, the golden spiny mouse exhibits also some nocturnal activity, suggesting that the common spiny mouse competitively displaces the golden spiny mouse into diurnal activity (Gutman and Dayan, 2005; Shkolnik, 1971). Food resources may vary at the diel and seasonal scale, and their abundance may also vary between habitats. The extreme climatic
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conditions in hot deserts require special adaptations of the inhabitants, especially from arthropods (reviewed by CloudsleyThompson, 2001). The reaction of most desert beetles is largely behavioral, avoiding the harsh conditions by hiding or borrowing during the day (Cloudsley-Thompson, 2001). Holm and Edney found that tenebrionid beetles in the Namib Desert differ in season and daily cycle activity, and in addition winter and summer population were substantially different from each other (Holm and Edney, 1973). Krasnov and Shenbrot (1997) found that most tenebrionid species studied in the Negev Desert (Israel) changed their microhabitat preferences seasonally. In the past decade we have been studying temporal activity patterns of spiny mice, as well as foraging behavior and foraging microhabitat choice at the diel, lunar, and seasonal scale, factoring in varying levels of perceived risk of predation (reviewed by Kronfeld-Schor and Dayan, 2003, 2008). We found that the two spiny mouse species overlap in food habits, with a preference for arthropods, taken in extremely high quantities by both species in summer (Kronfeld-Schor and Dayan, 1999). In winter spiny mice showed trade-offs in foraging efficiency that may enable their coexistence (Jones et al., 2001). In summer, however, a shift in habitat preferences of both species increases ecological overlap between them (Jones et al., 2001). This shift may result from predator activity (Jones et al., 2001), but may also reflect a shift in the spatial distribution of available resources. This microhabitat use overlap may be the driver for temporal partitioning (Gutman and Dayan, 2005). During summer both species turn primarily insectivorous. Because arthropod prey of A. cahirinus and A. russatus are likely to show diel patterns in availability, temporal partitioning among species of spiny mice could well promote resource partitioning and coexistence (Jones et al., 2001; Kronfeld-Schor and Dayan, 1999). Previous research has revealed diel, seasonal, and spatial shifts in foraging microhabitat use by spiny mice. These shifts have been ascribed to interspecific competition and to predation risks in different habitats (Jones et al., 2001; Mandelik et al., 2003). Temporal partitioning as a mechanism of coexistence assumes different resource availability during the day and night (KronfeldSchor and Dayan, 2003; Schoener, 1974), but this hypothesis has yet to be tested. Furthermore, spatial shifts in foraging patterns may result not only from predation and competition but also the spatial distribution of resources. Data of spiny mice prey species are scarce, since the mice probably digest insects’ cuticle, and even stomach pumping revealed only a small number of identifiable elements (KronfeldSchor and Dayan, 1999), which cannot be taken as representative. We studied the arthropod fauna at En Gedi, near the Dead Sea, in order to gain insight into the possible effects of varying resource levels in time and in space. We used pitfall traps in order to learn about the prey available for spiny mice; specifically, we asked: Are different arthropod taxa available during the day and during the night? Such differences would imply that temporal partitioning is a viable mechanism for coexistence between spiny mouse species. Do seasonal differences in spiny mouse diets reflect differences in resource availability? We found seasonal shifts in the arthropod component in spiny mouse diets (Kronfeld-Schor and Dayan, 1999) and ask whether they reflect resource availability in different seasons and during different activity times. Are there seasonal differences in arthropod availability between the different habitats? Seasonal differences in resource availability in different habitats could affect foraging habitat use of spiny mice during the day and night.
459
When resources are limiting, they can be expected to impact not only population dynamics but also animal foraging behavior and microhabitat use and thus also affect ecological overlap of competing species and their risk of predation. Consequently, resource availability can impact community level interactions both directly, by regulating population growth, and indirectly, by affecting diel and seasonal patterns of niche overlap. Our study was designed to investigate the effect of diel and seasonal resource availability on the community structure of rocky desert rodents. 2. Materials and methods 2.1. Study site The study was conducted at the En Gedi Nature Reserve, in the Judean Desert, near the Dead Sea (31280 N, 35 230 E, 300 m below sea level), between September 2002 and August 2003. Three habitats were chosen in which the foraging behavior of spiny mice was previously studied: (1) boulder habitat; (2) open habitat, where traps were set 5 m away from a rock terrace; (3) wadi bed – a nearby dry stream bed, with both open and boulder habitats. 2.2. Faunal sampling We sampled arthropods using pitfall traps. A caveat: our study focuses on active prey availability (see Hingrat et al., 2007) rather than on prey actually chosen. Pitfall traps are biased towards ground-dwelling active arthropods (Southwood, 1978), those we assume are most likely to be preyed by spiny mice. Inactive arthropods at En Gedi usually seek refuge under stones and in tight crevices, where they are sheltered from predators, so they are less likely to be preyed. Other studies have shown that active prey are usually more susceptible to predation than inactive individuals (Lima, 1998). In each habitat 35 pitfall traps were dug into the ground, at 5 m intervals. Pitfall traps consisted of plastic cups (10 cm in diameter, 10.5 cm deep), a plastic funnel, and tissue paper (in order to increase available surfaces and thus reduce the chance of predation). The traps were opened every month for three days and nights. They were checked twice a day – at first and last light. All organisms were identified to the lowest taxonomic unit possible, measured for body length, and usually released on site. Individuals which could not be identified in the field were taken to the Tel-Aviv University Zoological Museum for further identification. We used morphospecies for groups for which there are no taxonomists in Israel. We analyzed the cumulative data of number of individuals and the individuals’ length for each season (as an estimate of biomass). Because the wadi habitat was not checked during autumn and the first month of winter, we performed the analysis twice: once for the open and the boulder habitats without the wadi, for the entire year, and once for all three habitats but without autumn and the fist winter sampling. 2.3. Statistical analysis The length and number of individuals’ data were square root transformed and analyzed by three-way ANOVA (analysis of covariance), followed by Tukey multiple comparisons (using Statistica 7.1, StatSoft Inc., Oklahoma, USA), with season, habitat and time of activity as factors. Again, we performed the analysis twice: once for the open and the boulder habitats, for the whole year, and once for all the three habitats, without the autumn and the first winter sampling.
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3. Results 3.1. Taxon level analyses 1916 individual arthropods, of 5 mm and over, were sampled in the three habitats. Most taxa were nocturnal (18); only four were diurnal (Fig. 1). The number of active arthropods was greater at night. Nearly 80% of identified taxa were either diurnal or nocturnal (Fig. 1). The few taxa that did not exhibit a pattern are: a) ones that
we could not identify to a low taxonomic level (a part of the Zygenthoma, Bombicidae – larvae, and Grilopsis?). It is quite possible that at the species level these taxa do have a typical activity pattern; b) Acrididae – this is not a suitable method for catching them, and their trapping was much lower than their visual activity in the field; and c) Diplopoda, whose sample size is small. The workers of Messor ebeninus also did not have a fixed activity pattern; it is known that this species’ activity is set by surface temperature rather than daylight (Avidov, 1968).
Family Formicidae
Order Thysanura Lepismatidae - a
56
Lepismatidae - b
40
Machilidae
Cataglyphis lividus
15
6
2
6
0
43
305
Camponotus sp.
1
Others
312
Aphenogaster sp.
3
81
18
126
Messor ebeninus
169
Order Orthoptera Acrididae
11
3
Order Isopoda 23
Eremogryllodes sp.
0 20
Sowbug Grilopsis?
3
10
Others
Pillbugs
6
70
Adesmia abbreviata
Order Araneae
6
2
Lycosidae
3
20
Trachyderma philistina
0
9
2
18
53
Gnaphosidae
Salticidae
28
Others
15
0
Order Coleoptera Mesostena punctata
13
3
41
Others
8
74
Order Lepidoptera
21
Other arthropods Scutigeridae
Moth larva a
64
3
Others 0%
6
7 20%
4 40%
0
15
5 Scolopendridae
Moth larva b
0
60%
80%
21
Galeodidae
65
Scorpiones
20
Diplopoda 100%
3
0%
1 0
5 20%
3 40%
60%
80%
100%
Fig. 1. Activity patterns of the major arthropod taxa according to trapping times at En Gedi. The black and white bars represent the percentage of night and day activity, respectively, while the numbers inside the bars represent the number of individuals collected using pitfall traps. Taxa are the lowest taxonomic unit possible of the abundant species (more than 5% of the entire order/family).
Within most taxonomic groups no significant difference in diel activity pattern was found between habitats or seasons. 3.2. Patterns of arthropod availability The number of individuals and cumulative length showed similar trends, so we present results only for the former. Significant differences were found in number of individuals between seasons and time of activity, when only the boulder and open habitat were studied (three-way ANOVA, season: F ¼ 49.47, df ¼ 3, p < 0.0001; time: F ¼ 7.83, df ¼ 1, p < 0.0001). Significant differences were found between seasons, time of activity and habitat when data for three habitats were analyzed (season: F ¼ 80.05, df ¼ 2, p < 0.0001; habitat: F ¼ 10.08, df ¼ 2, p < 0.0001; time: F ¼ 23.448, df ¼ 1, p < 0.0001). There was a significant seasonal difference in number of individuals, lowest in winter (three-way ANOVA, F ¼ 49.47, df ¼ 3, p < 0.0001. Fig. 2). In spring the numbers increased and peaked in summer. Species richness was high in spring and summer and lower in autumn and winter. In winter and spring the number of individuals was lowest at the open habitat, but in summer and autumn it was greatest (Fig. 3). Significant differences were found between day and night when only the boulder and open habitats were studied (Tukey, F ¼ 1.46, df ¼ 1, p < 0.01. Fig. 3), and significant only in the wadi when the three habitats were studied (Tukey, F ¼ 1.46, df ¼ 1, p < 0.0001). 4. Discussion Patterns of resource availability contribute to our understanding of the structure of a rocky desert rodent community. More arthropods were trapped during the night, the activity time of common spiny mice, from which golden spiny mice are excluded. Activity patterns of mammals may be determined by extrinsic factors (Halle, 1995; Meyer et al., 2005), selective forces and phylogenetic constraints (Daan, 1981; Kronfeld-Schor and Dayan, 2003; Roll et al., 2006); nocturnality is probably the ancestral state in mammals and in rodents. Notwithstanding, it appears that night offers more feeding opportunities than day in this ecosystem. By shifting activity from night to day, golden spiny mice encounter a different resource spectrum and must take different arthropod prey. Thus, temporal partitioning at the diel scale is a viable mechanism of coexistence reducing overlap between these competitors.
No. of individuals 70
Species richness
900 800 50 700 600 500
30
400 300 10
Species richness
Accumulated no. of individuals
1000
200 100 0
-10 Winter
Spring
Summer
Autumn
Season Fig. 2. Distribution of number of individuals and species richness of arthropods sampled by pitfall traps in the research site at En Gedi.
Accumulated no. of individuals
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461
400 350 300 250 200 150 100 50 0
Open Bolder Wadi Open Bolder Wadi Open Bolder Wadi Open Bolder
Winter
Spring
Summer
Autumn
Fig. 3. Distribution of number of individuals of diurnal (white bars) and nocturnal (black bars) arthropods between seasons and habitats.
Seasonal variation in arthropod abundance, high in summer and low in winter, is reflected in spiny mouse diets; therefore, in winter both species overlap in a largely vegetarian diet (Kronfeld-Schor and Dayan, 1999). However, in winter the two species differ in their foraging behavior, thus reducing niche overlap between the species (Jones et al., 2001). Diel, lunar, and seasonal patterns in predation risk appear to affect foraging activity patterns and foraging microhabitat use, to minimize risk (Eilam et al., 1999; Jones et al., 2001; Mandelik et al., 2003). Here we asked how resource availability relates to these patterns. Both species prefer to forage in the boulder habitat where they are protected from avian and mammalian predators, and during the day, from the sun’s radiation (Gutman and Dayan, 2005; Jones et al., 2001; Kronfeld-Schor et al., 2001; Mandelik et al., 2003; Shargal et al., 2000). However, it appears that foraging in the boulder habitat is also advantageous in terms of resource availability: during three of four seasons, arthropods are more abundant in this habitat than in the open habitat. In summer, arthropods become more abundant in the open habitat. During summer spiny mice shift their activity to more open habitats. We previously ascribed this shift in foraging behavior to saw scaled vipers (Echis coloratus), seasonally active spiny mouse predators (Jones et al., 2001; Weissenberg et al., 1997). This shift also conforms to resource availability, which may be an additional force affecting foraging microhabitat use. Without experimentation (e.g., Price and Waser, 1985; Tilman, 1982) we are unable to prove the precise role of resource levels in producing these activity patterns, but we can certainly note the perceived relationship. The shift in summer microhabitat use increases predation risk from avian and mammalian predators (Jones et al., 2001), thus affecting also community level interspecific interactions. However, it should be noted that even with this shift in summer, spiny mice still forage significantly more in the protected boulder habitat (Jones et al., 2001). Thus it appears that predation risk by avian and mammalian predators, and thermal load from the sun during the day still exert stronger pressure than do predation risk by snakes and patterns of resource availability. Of numerous studies of interspecific interactions, few address patterns in resource availability and their possible role in affecting community structure (e.g., Kneitel and Chase, 2004; Kotler and Brown, 1990; Price and Joyner, 1997). Resource availability is a significant variable in ecological communities, both as a lead force in population dynamics and indirectly through diel, seasonal, and spatial variations in habitat use. Here we find a strong relationship between patterns of resource availability and community structure:
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preferred activity times are those at which resource availability is greatest, foraging microhabitat choice conforms to patterns of resource availability at the seasonal scale and diel patterns of prey activity can support temporal partitioning as a mechanism of coexistence. When arthropod availability declines during winter, their significance in spiny mouse diets drops and an alternative mechanism of coexistence comes into action (Jones et al., 2001). These patterns and choices impact both competitive and predatory interspecific interactions. Thus resource availability appears to be a significant factor structuring this rocky desert rodent community. Acknowledgments We sincerely thank Enav Vidan and Ariella Gotlieb for all the hard work in the field, Arieh Landsman for fighting the world’s bureaucracy, the En Gedi Field School of the Society for the Protection of Nature in Israel for the residence, and the Israel Nature and Parks Authority for their help. We thank Mary V. Price for her useful remarks to an early version of the manuscript. Vladimir Chikatunov, Vassiliy Kravchenko, Tova Feller, Amnon Freidberg, Leybele Friedman, Alex Shlagman and Dany Simon of the Tel Aviv University Zoological Museum helped with arthropod identifications and David Wool provided statistical advice. This research was supported by the Israel Science Foundation (grant No. 720/01-4). References Avidov, Z., 1968. The Harvester Ant in Israel. Sifriath Hassadeh, Tel Aviv, Israel (in Hebrew). Begon, M., Townsend, C.R., Taper, J.L., 2006. Ecology: from Individuals to Ecosystems. Blackwell Publishing, Maldan, MA. Ben-Natan, G., Abramsky, Z., Kotler, B.P., Brown, J.S., 2004. Seeds redistribution in sand dunes: a basis for coexistence of two rodent species. Oikos 105, 325–335. Bouskila, A., 1995. Interactions between predation risk and competition – a fieldstudy of kangaroo rats and snakes. Ecology 76, 165–178. Brown, J.S., Kotler, B.P., 2004. Hazardous duty pay and the foraging cost of predation. Ecology Letters 7, 999–1014. Brown, J.H., Maurer, B.A., 1989. Macroecology – the division of food and space among species on continents. Science 243, 1145–1150. Brown, J.S., 1989. Desert rodent community structure – a test of 4 mechanisms of coexistence. Ecological Monographs 59, 1–20. Cloudsley-Thompson, J.L., 2001. Thermal and water relations of desert beetles. Naturwissenschaften 88, 447–460. Daan, S., 1981. Adaptive daily strategies in behavior. In: Aschoff, J. (Ed.), Handbook of Behavioral Neurobiology. Biological Rhythms, vol. 4. Plenum, New York, pp. 275–298. Damuth, J., 2007. A macroevolutionary explanation for energy equivalence in the scaling of body size and population density. American Naturalist 169, 621–631. Eilam, D., Dayan, T., Ben-Eliyahu, S., Schulman, I., Shefer, G., Hendrie, C.A., 1999. Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Animal Behaviour 58, 1085–1093. Evans, K.L., Jackson, S.F., Greenwood, J.J.D., Gaston, K.J., 2006. Species traits and the form of individual species–energy relationships. Proceedings of the Royal Society B – Biological Sciences 273, 1779–1787. Fedriani, J.M., Manzaneda, A.J., 2005. Pre- and post-dispersal seed predation by rodents: balance of food and safety. Behavioral Ecology 16, 1018–1024. Fretwell, S.D., Lucas Jr., H.L., 1970. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheoretica XIX, 16–36. Gutman, R., Dayan, T., 2005. Temporal partitioning: an experiment with two species of spiny mice. Ecology 86, 164–173. Halle, S., 1995. Effect of extrinsic factors on activity of root voles, Microtus oeconomus. Journal of Mammalogy 76, 88–99. Hillebrand, H., 2004. On the generality of the latitudinal diversity gradient. American Naturalist 163, 192–211. Hingrat, Y., Ysnel, F., Saint Jalme, M., Le Cuziat, J., Be´ranger, P.M., Lacroix, F., 2007. Assessing habitat and resources availability for an endangered desert bird
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