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Article history: The classical paradigm describe desert communities as being controlled by abiotic conditions and
Received 11 February 2015 therefore it was assumed that predation had a limited role in the determination of desert community
Received in revised form structure and that only one effective trophic level was expected. In the Negev desert, the desert isopod
28 November 2015
(Hemilepistus raeumuri) is common in the less productive habitats but almost absent from the more
Accepted 4 August 2016
Available online 25 August 2016
productive wadis. In the present study we tested whether predation by ectothermic predators has a role
in controlling isopod populations in wadis. We hypothesized that plant cover provides a refuge for these
predators from secondary endothermic predators. We addressed this hypothesis by comparing isopod
Keywords:
Community structure
survivorship with and without predation exclusion, and with and without plant cover removal. Isopods
Desert protected from predation had a sustainable population whereas unprotected isopods had an unsus-
Food-web tainable sink population. Removal of plant cover did not affect the survivorship of predator-protected
Macrodetritivores isopods, however it did increase the survivorship and reduced predation pressure when not protected
Ectothermic predators from predators, for at least four years. Hence, we conclude that predation controls isopod population and
causes an unsustainable sink population in wadis. We have shown that plant cover mediates predation
and that some habitats in the desert have an effective third trophic level, suggesting that energy is not
the major limiting factor in determining the length of food chains.
© 2016 Elsevier Ltd. All rights reserved.
1. Introduction controlled (Hairston et al., 1960; Oksanen et al., 1981; Oksanen and
Oksanen, 2000; Bond, 2005). In resource-poor hot deserts, only one
One of the central issues in community ecology is the relative effective trophic level is expected (i.e., deserts represent a “green”
importance of bottom up (e.g., water) limitation and top-down (e.g., state) and plants are water limited and therefore herbivores and
consumers) control in shaping terrestrial communities (Hopcraft predators are expected to play a minor role in shaping hot desert
et al., 2010). It has been suggested that, in terrestrial commu- communities (Noy-Meir, 1973, 1985; Shmida, 1985; Megias et al.,
nities, there is a positive correlation between productivity and the 2011).
number of effective trophic levels (Fretwell, 1977; Oksanen et al., However, an alternative explanation suggests that deserts could
1981). A trophic level was defined as effective if it effectively con- have more trophic levels and that predation can play an important
trols the trophic level below it (Fretwell, 1977) suggesting that the role in shaping hot desert communities (Polis, 1991; Moore et al.,
effect of removal of one trophic level will cascade to lower trophic 2004; Borer et al., 2005; Ayal, 2007). Hot deserts accumulate
levels. Accordingly, Fretwell (1977) recognized two different states detritus which is more predictable and long lasting food source for
in terrestrial communities, namely, a “green” state, where the primary consumers, especially macrodetritivorous arthropods
number of trophic levels is odd (i.e., one or three) and consequently (Noy-Meir, 1979). The macrodetritivorous arthropods serve as a
plants are resource limited, and a “brown” state, where the number major conduit transferring energy from primary producers to
of trophic levels is even (i.e., two or four) and plants are herbivore- higher trophic levels (Crawford, 1981; Ayal et al., 2005). The
abundant macrodetritivores can support two additional trophic
levels, namely, primary ectothermic predators (e.g., arachnids and
* Corresponding author. Current address: Ramat Negev Desert Agro-Research reptiles) and secondary endothermic predators (i.e., mammals and
Center, Negev, Israel. birds). Ayal (2007) suggested that the distribution of the primary
E-mail address: moran.segoli@gmail.com (M. Segoli).
http://dx.doi.org/10.1016/j.jaridenv.2016.08.008
0140-1963/© 2016 Elsevier Ltd. All rights reserved.
34 M. Segoli et al. / Journal of Arid Environments 135 (2016) 33e38
Fig. 1. The suggested features of the trophic control in the Negev Highlands (after Ayal
et al., 2005). The direction of the arrows point on the affected group and their width on
the intensity of the interactions. Secondary predators efficiency is higher in the low
productivity habitat than in the wadi due to plant cover. Hence, in the low productivity Fig. 2. A schematical representation of the experimental design. Intact & Removed
habitat secondary predators efficiency controls primary predators and macro- plots are 750 m2, Protected and Unprotected sub-plots are 25 m2. Solid lines represent
detritivores are released from predation and become food limited. In the wadi primary fences that reduce movement of predators (see Fig. A1 & A2). Solid circles represent
predators find refuge in the plant cover, maintain high densities and efficiently control isopods that were transferred in the first year. Hollow circles represent natural
the macrodetritivores. occurring isopods.
M. Segoli et al. / Journal of Arid Environments 135 (2016) 33e38 35
(Intact). In between the plots we left a buffer zone that was not 2.5. Population dynamics
manipulated, at least 50 m between the plots. A barrier fence
(Fig. A1) was installed on both sides between the Removed plot and Thirty dry pitfall traps were placed in each plot in Boker in 2003.
the buffer zone that reduced the movements of most of the isopod's Each pit fall trap (10 cm in diameter and 10 cm in depth) was
predators (i.e., primary ectothermic predators). sampled daily for 2e3 weeks during the July and August between
In the second year (2004), woody vegetation was again removed 2003 and 2007, except for 2004 that was sampled during
from the two plots and both were used as the Removed plot. We did September and October due to technical problems. Collected iso-
not manipulate the Intact plot. pods were counted and released back into the plot.
Fig. 5. Ratio between the density of the isopods at the end of the experiment to the
density at the beginning of the experiment, in Boker. Line represents the minimum
ratio needed for a sustainable population. Data are represented as means ± SE.
Fig. 3. The percent of surviving isopod families (active burrows) for the (a) first and (b)
second year.
Fig. 6. Percent of tethered isopods that were preyed upon in the different manipula-
tions. Data are represented as means ± SE.
between the isopod densities in the Removed and Intact treatments and Hairston, 1993; Ayal and Groner, 2009). In addition, ecto-
(R2 ¼ 0.97, P < 0.01). The increase in the ratio was due to an increase thermic food webs are very efficient physiologically and enable
in the density of isopods in the Removed treatment compared to a longer food chains than endothermic food webs (Yodzis, 1984).
constant density in the Intact treatment. The lower densities in This suggests that desert communities are not as simple as
2004 are probably due to sampling two months later than the suggested in the past (Oksanen et al., 1981) and the mechanisms
sampling dates in the other years. controlling desert communities should be revised (Polis, 1991). In
addition, this study emphasizes the importance of plants in the
4. Discussion desert not only as a food resource but also as a structure mediating
predation intensity and can determine community structure.
Ecologists have long debated on the relationship between pro-
ductivity and number of trophic levels, and consequently on the Acknowledgements
role of predation in the determination of desert communities
(Fretwell, 1977; Oksanen et al., 1981; Polis, 1991; Ayal, 2007; Holt We thank Sonya Rozin for laboratory assistance, Ittai Renan for
and Barfield, 2013). In the present study we tested whether pre- field assistance, and Moshe Shachak for scientific contributions.
dation has a role in controlling isopod populations in wadis and if This study was supported by grant # 505/02 to YA by the Israel
this predation is mediated by plant cover. Top-down control (i.e., Science Foundation (ISF) managed by Israel Academy of Sciences.
predation) as opposed to bottom-up limitation (i.e., resources) This is publication No. 889 of the Marco and Louise Mitrani
supports the notion that an effective third trophic level exists (Ayal, Department of Desert Ecology.
2007).
Isopod survivorship in the Predator-protected plots was higher Appendix A. Supplementary data
than in the Unprotected plots (Figs. 1b and 3). In the first year,
removal of plant cover did not affect survivorship of isopod fam- Supplementary data related to this article can be found at http://
ilies, as opposed to the second year where removal of plant cover dx.doi.org/10.1016/j.jaridenv.2016.08.008.
increased survivorship of isopod families in the Unprotected plots
(Fig. 3). This difference is probably due to a time lag in the effect of References
predation of ectothermic predators by endothermic predators, as
suggested by the population dynamics (Fig. 7). Additionally, Ayal, Y., 2007. Trophic structure and the role of predation in shaping hot desert
communities. J. Arid. Environ. 68, 171e187.
removal of plant cover did increased isopod family size and reduced
Ayal, Y., Groner, E., 2009. Primary consumer body size and food-chain length in
predation intensity in the Unprotected treatment, but did not affect terrestrial communities. Isr. J. Ecol. Evol. 55, 329e343.
the survivorship of Predator-protected isopod burrows (Figs. 1b and Ayal, Y., Merkl, O., 1994. Spatial and temporal distribution of tenebrionid species
2). The effect of reduced plant cover continued to increase natural (Coleoptera) in the Negev Highlands. Isr. J. Arid. Environ. 27, 347e361.
Ayal, Y., Polis, G.A., Lubin, Y., Goldberg, D.E., 2005. How can high animal diversity be
occurring isopod densities for at least four years, while the den- supported in low productivity deserts? the role of macrodetritivory and habitat
sities in the Intact were constant (Fig. 7). Replacement rate showed physiognomy. In: Shachak, M., Gosz, J.R., Pickett, S.T.A., Perevolotsky, A. (Eds.),
that the Unprotected isopods had survivorship too low to replace Biodiversity in Drylands: toward a Unified Framework. Oxford University Press,
New York, pp. 15e29.
the initial number of settled isopods, suggesting that the popula- Baker, M.B., 2004. Sex biased state dependence in natal dispersal in desert isoponds,
tion is not sustainable (Fig. 5). However, isopods protected from Hemilepistus reaumuri. J. Insect Behav. 17, 579e598.
predators had a higher number of surviving individuals at the end Baker, M.B., Shachak, M., Brand, S., 1998. Settling behavior of the desert isopod
Hemilepistus reaumuri in response to variation in soil moisture and other
of the year compared to the initial number of settled isopods environmental cues. Israel J. Zool. 44, 345e354.
(Fig. 5). This suggests that the isopod population in the wadi is a Bond, W.J., 2005. Large parts of the world are brown or black: a different view on
sink population since predation causes an unsustainable isopod the ‘Green World’ hypothesis. J. Veg. Sci. 16, 261e266.
Borer, E.T., Seabloom, E.W., Shurin, J.B., Anderson, K.E., Blanchette, C.A., Broitman, B.,
population in the wadi that cannot persist without immigration
Cooper, S.D., Halpern, B.S., 2005. What determines the strength of a trophic
from the adjacent slopes (Schreiber and Kelton, 2005). Since cascade? Ecology 86, 528e537.
removing the plant cover increases isopods densities, our results Coenen-Stass, D., 1984. Observations on the distribution of the desert woodlouse
Hemilepistus reaumuri (crustacea, isopoda, oniscoidea) in North Africa. In:
partly support Ayal (2007) hypotheses that the low abundance of
Symposium of the Zoological Society of London, vol. 53, pp. 369e380.
isopods in the wadi is facilitated by predation and that this pre- Crawford, C.S., 1981. Biology of Desert Invertebrates. Springer-Verlag, Berlin; New
dation is mediated by plant cover. York.
We have shown that some habitats in the desert have an Fretwell, S.D., 1977. Regulation of plant communities by food-chains exploiting
them. Perspect. Biol. Med. 20, 169e185.
effective third trophic level. In the Negev highland, the third trophic Groner, E., Ayal, Y., 2001. The interaction between bird predation and plant cover in
level is made of insectivores that feed on the macrodetritivores. determining habitat occupancy of darkling beetles. Oikos 93, 22e31.
This predation is mediated by shrubs that protect the ectotherm Hairston, N.G., Hairston, N.G., 1993. Cause-effect relationships in energy-flow, tro-
phic structure, and interspecific interactions. Am. Nat. 142, 379e411.
small predators from their endotherm large predators. The absence Hairston, N.G., Smith, F.E., Slobodkin, L.B., 1960. Community structure, population
of isopods from the vegetated wadies due to predation by scorpions control, and competition. Am. Nat. 94, 421e425.
is an evidence of predation shaping the desert foodweb. This con- Holt, R.D., Barfield, M., 2013. Direct plant-predator interactions as determinants of
food chain dynamics. J. Theor. Biol. 339, 47e57.
tradicts Oksanen et al. (1981) hypothesis and suggests that energy Hopcraft, J.G.C., Olff, H., Sinclair, A.R.E., 2010. Herbivores, resources and risks:
is not the limiting factor in determining the length of food chains alternating regulation along primary environmental gradients in savannas.
(Holt and Barfield, 2013). Ayal (2007) suggested that the desert food Trends Ecol. Evol. 25, 119e128.
Hutchinson, G.E., 1959. Homage to Santa-Rosalia or why are there so many kinds of
webs have different properties that enable a high number of tro- animals? Am. Nat. 93, 145e159.
phic levels with low productivity. Deserts have low microbial Kaplan, E.L., Meier, P., 1958. Nonparametric-estimation from incomplete observa-
decomposition and most of the plant biomass dries up and enters tions. J. Am. Stat. Assoc. 53, 457e481.
Megias, A.G., Sanchez-Pinero, F., Hodar, J.A., 2011. Trophic interactions in an arid
the above ground food web through consumption by macro-
ecosystem: from decomposers to top-predators. J. Arid. Environ. 75, 1333e1341.
detritivores (Ayal et al., 2005). Macrodetritivores are donor- Moore, J.C., Berlow, E.L., Coleman, D.C., de Ruiter, P.C., Dong, Q., Hastings, A.,
controlled and therefore they have no negative effects on plant Johnson, N.C., McCann, K.S., Melville, K., Morin, P.J., Nadelhoffer, K.,
productivity. Most of the macrodetritivores in the desert are small Rosemond, A.D., Post, D.M., Sabo, J.L., Scow, K.M., Vanni, M.J., Wall, D.H., 2004.
Detritus, trophic dynamics and biodiversity. Ecol. Lett. 7, 584e600.
and similar in size and therefore allow longer food chains than food Noy-Meir, I., 1973. Desert ecosystems: environment and producers. Annu. Rev. Ecol.
webs that are based on larger animals (Hutchinson, 1959; Hairston Syst. 4, 25e51.
38 M. Segoli et al. / Journal of Arid Environments 135 (2016) 33e38
Noy-Meir, I., 1979. Structure and function of desert ecosystems. Isr. J. Bot. 28, 1e19. and dispersal in the desert scorpion, Scorpio maurus palmatus. Oecologia 60,
Noy-Meir, I., 1985. Desert ecosystem structure and function. In: Evenari, M., Noy- 371e377.
Meir, I., Goodall, D.W. (Eds.), Ecosystems of the World. Elsevier, Amsterdam, Shachak, M., Brand, S., 1991. Relations among spatiotemporal heterogeneity, pop-
pp. 93e104. ulation abundance, and variability in a desert. In: Kolasa, J., Pickett, S.T.,
Oksanen, L., Fretwell, S.D., Arruda, J., Niemela, P., 1981. Exploitation ecosystems in Allen, T.F.H. (Eds.), Ecological Heterogeneity. Springer-Verlag, New York,
gradients of primary productivity. Am. Nat. 118, 240e261. pp. 202e223.
Oksanen, L., Oksanen, T., 2000. The logic and realism of the hypothesis of exploi- Shachak, M., Chapman, E.A., Steinberger, Y., 1976. Feeding, energy-flow and soil
tation ecosystems. Am. Nat. 155, 703e723. turnover in desert isopod, Hemilepistus reanumuri. Oecologia 24, 57e69.
Polis, G.A., 1991. Complex trophic interactions in deserts e an empirical critique of Shmida, A., 1985. Biogeography of the desert flora. In: Evenary, M.E.A. (Ed.), Hot
food-web theory. Am. Nat. 138, 123e155. Deserts and Arid Shrublands. Elsevier, Amsterdam, pp. 23e77.
Schreiber, S.J., Kelton, M., 2005. Sink habitats can alter ecological outcomes for Tarone, R.E., Ware, J., 1977. Distribution-free tests for equality of survival distribu-
competing species. J. Animal Ecol. 74, 995e1004. tions. Biometrika 64, 156e160.
Shachak, M., 1980. Energy allocation and life-history strategy of the desert isopod Yodzis, P., 1984. Energy-flow and the vertical structure of real ecosystems. Oecologia
H. Reaumuri. Oecologia 45, 404e413. 65, 87e88.
Shachak, M., Brand, S., 1983. The relationship between sit and wait foraging strategy Zar, J.H., 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River.